Rhizosphere Microbes: Soil and Plant Functions (Microorganisms for Sustainability, 23) 9811591539, 9789811591532
Plants create a dynamic micro-biosphere in the soil, around the roots, called as ‘rhizosphere’, which harbors diverse nu
100 76 13MB
English Pages 702 [689] Year 2021
Preface
Contents
Editors and Contributors
1: Microbial Interactions in the Rhizosphere Contributing Crop Resilience to Biotic and Abiotic Stresses
1.1 Introduction
1.2 Rhizosphere Structure and Function
1.3 Microbe-Mediated Mechanisms of Plant Defence to Biotic Stress
1.3.1 Phenolics and Plant Resistance
1.3.2 Induced/Systemic Disease Resistance
1.4 Microbe-Mediated Mechanisms of Plant Defence to Abiotic Stresses
1.4.1 Generation of Reactive Oxygen Species and Their Effects Under Abiotic Stress
1.4.2 Site of Synthesis of ROS
1.4.3 Type of ROS Synthesized During Abiotic Stresses
1.4.4 Mechanisms to Scavenge ROS During Abiotic Stresses
1.4.5 Mechanisms of Plant Defence
1.4.6 MAPK Signalling
1.5 Endophytes in Biotic and Abiotic Stress Management
1.6 The `Holobiome´: Significance of Microbes in Host Development and Behaviour
1.7 Rhizosphere Engineering for Stress Management
1.8 Application of Nano-Bio-Technology
1.9 Conclusion
1.10 Future Prospects
References
2: Rhizosphere Microbes for Sustainable Maintenance of Plant Health and Soil Fertility
2.1 Introduction
2.2 Rhizosphere: A Hub for Plant Beneficial Rhizosphere Microbes
2.3 Factors Influencing Rhizosphere Microbiota
2.4 Interaction between Rhizosphere Microbe and Plant via Root Exudates
2.5 Role of Rhizosphere Microbes in Plant Health
2.5.1 Nitrogen Fixation
2.5.2 Phosphate Solubilization
2.5.3 Potassium Solubilization
2.5.4 Iron Chelators or Microbial Siderophore Producers
2.5.5 Production of Plant Growth Regulators and Secondary Metabolites by Rhizosphere Microbes
2.6 Effect of Plant Beneficial Rhizosphere Microbes on Soil Fertility
2.6.1 Carbon Sequestration
2.6.2 Nutrient Mineralization
2.7 Rhizodeposition-Mediated Enhancement of Soil Fertility
2.8 Rhizoremediation
2.9 Conclusion
References
3: Dissecting Structure and Function of Plant Rhizomicrobiome: A Genomic Approach
3.1 Introduction
3.2 Rhizomicrobiome
3.3 Root Exudate-Rhizomicrobiome Relationship
3.3.1 Signal Exchange Between Rhizomicrobiome and Plant Roots
3.3.1.1 Rhizomicrobiome-Mediated Phytohormone Production
3.3.2 Signalling: Microbe to Plant
3.3.3 Signalling: Plants to Rhizomicrobiome
3.4 Communication in the Rhizomicrobiome
3.4.1 Signal Molecules
3.4.2 Communication Within Rhizomicrobiome: Operational Molecular Machinery
3.5 The Direct Role of Rhizomicrobiome in Plant Growth Promotion
3.5.1 Phosphate Solubilization
3.5.2 Nitrogen Fixation
3.5.3 Potassium Solubilization
3.5.4 Siderophore Production
3.6 Indirect Plant Growth Promotion
3.6.1 Antibiosis
3.6.2 Lytic Enzymes
3.6.3 Induced Systemic Resistance (ISR)
3.7 Endophytic Root Microbiome
3.8 Classical Approach to Study the Microbiome
3.8.1 Culture-Dependent Methods
3.8.1.1 Isolation and Culturing
3.8.1.2 Functional Characterization
3.8.1.3 16S rRNA Gene Sequencing
Identification of Novel Pathogen
Identification of Unculturable Bacteria
3.9 Modern Approach
3.9.1 Functional Genomics
3.9.2 DNA Microarray
3.9.3 Next-Generation Sequencing
3.9.4 Mass Spectrometry
3.9.5 Transcriptomics
3.9.5.1 Transcriptomics and Agriculture
3.9.6 Proteomics
3.9.6.1 Proteomics and Agriculture
3.9.7 Metabolomics
3.9.7.1 Metabolomics and Agriculture
3.9.8 Interactomics
3.9.9 Metagenomics
3.9.9.1 Metagenomics and Agriculture
3.9.10 Metatranscriptomics
3.9.10.1 Metatranscriptomics and Agriculture
3.9.10.2 Metatranscriptomics Tools
3.9.10.3 Factors Affecting Metatranscriptomic Analysis
3.9.10.4 Computational Analysis of Metatranscriptomic Data
3.9.11 Comparative Metatranscriptomics
3.9.11.1 Comparative Metatranscriptomics and Agriculture
3.9.11.2 Applications
3.10 Future Prospects
References
4: Plant Root Exudates as Determinant of Rhizomicrobiome
4.1 Introduction
4.2 Chemical Composition of Root Exudates
4.3 Transport Mechanism of Exudate Chemicals Releasing from Root System
4.3.1 Exudates-Releasing Mechanism from Root
4.3.1.1 Movement of Exudate Chemicals to Root Tips
4.3.1.2 Release of Exudate Chemicals from Root Tips to Soil
4.4 Plant-Plant Interactions via Exudate Chemicals Release
4.4.1 Factors Influencing the Secretion of Exudate Chemicals for Plant-Plant Interaction
4.5 Interaction Between Plants and Microbes through Root Exudate Chemicals
4.5.1 Root Exudates as Rhizomicrobiome Determinants
4.5.2 Root Exudates as Defense Chemicals against Soil-Borne Pathogens
4.5.2.1 Root Exudates as Volatile Compounds
4.6 Conclusion and Future Perspective
References
5: Rhizospheric Microbial Community: Ecology, Methods, and Functions
5.1 Introduction
5.2 Microbial Communities in Rhizosphere
5.2.1 Bacteria
5.2.2 Fungi
5.2.3 Others
5.3 Factors Affecting Microbial Communities
5.3.1 Biotic Factors
5.3.2 Abiotic Factors
5.4 Methods of Studying Microbial Ecology in Rhizosphere
5.4.1 Traditional Approaches
5.4.1.1 Plate Count Analysis
5.4.1.2 Carbon Source Utilization Profile
5.4.2 Molecular Approaches
5.4.2.1 PCR Independent Approaches
5.4.2.2 PCR-based Techniques
5.5 Functions of Microbial Community in Rhizosphere
5.5.1 Nutrient Mobilization
5.5.1.1 Nitrogen Fixation
5.5.1.2 P Mobilization
5.5.1.3 Potassium Solubilization
5.5.1.4 Fe Sequestration
5.5.2 Plant Protection
5.5.3 Decomposition
5.6 Conclusion
5.7 Future Prospects
References
6: Signaling in the Rhizosphere for Better Plant and Soil Health
6.1 Introduction
6.2 Rhizosphere Communication: Plant to Microbe Signaling
6.2.1 Root Exudates as a Signal
6.2.2 Plant Volatile Organic Compounds (PVOCs) as a Signal
6.2.3 Strigolactones
6.3 Rhizosphere Communication: Microbe-to-Plant Signaling
6.3.1 Microbial Volatile Organic Compounds (MVOCs) as a Signal Molecule
6.3.2 Microbial Phytohormones as a Signal
6.3.2.1 Auxin
6.3.2.2 Gibberellins and Cytokinin
6.3.2.3 Ethylene
6.3.3 Microbial Exometabolites as Signaling for Suppression of Plant Disease Caused by Pathogens
6.3.4 Role of Microbial Signal in the Elicitation of Induced Systemic Resistance in Plants
6.4 Rhizosphere Communication: Microbe-to-Microbe Signaling
6.5 Some Examples of Microbial Signal in Plant-Microbe Symbiosis
6.5.1 Rhizobium-Legume Interactions
6.5.2 Signaling in Mycorrhizal Symbiosis
6.6 Manipulation of Rhizospheric Signals for Better Plant Fitness and Soil Health
6.7 Conclusion
References
7: Microbial Transformation of Nutrients in Soil: An Overview
7.1 Introduction
7.2 Nutrient Transformation of Macronutrients
7.2.1 Nitrogen Transformation
7.2.1.1 Nitrogen Mineralization and Immobilization
7.2.1.2 Nitrification
7.2.1.3 Denitrification
7.2.1.4 Biological Nitrogen Fixation (BNF)
7.2.1.5 Mechanism of Nodule Formation and Nitrogen Fixation
7.2.2 Phosphorus Transformation
7.2.3 Potassium Transformation
7.2.4 Sulfur transformation
7.3 Microbial Transformation of Micronutrients
7.3.1 Nutrient Transformation of Zinc
7.3.2 Nutrient Transformation of Iron
7.3.3 Nutrient Transformation of Manganese
7.4 Role of Mycorrhiza in the Nutrient Transformation Cycle
7.5 Conclusion and Future Directions
References
8: Microbial Indicator of Soil Health: Conventional to Modern Approaches
8.1 Introduction
8.2 Indicators of Soil Health
8.2.1 Microbiological Indicators of Soil Health
8.2.1.1 Characteristics of a Good Microbiological Indicator
8.2.2 Microbiological Indicators of Soil Health
8.2.2.1 Microbial Biomass
Direct Method
Indirect Methods
8.2.2.2 Soil Microbial Eco-Physiological Indices
8.2.2.3 Microbial Diversity
BIOLOGTM
Phospholipid Fatty Acid(PLFA) Analysis
Fluorescent In Situ Hybridization (FISH)
Molecular Microbial Diversity
8.2.2.4 Microbial Activity
Basal Respiration Rate
Organic Matter Decomposition
Soil Enzymes
Metabolic Quotient (qCO2)
Measurement of Specific Soil Microbial Processes
8.3 Conclusion
References
9: Rhizosphere Microbes: Driver for Soil Health Management
9.1 Introduction
9.2 Need of Soil Health Management
9.3 The Rhizosphere: Junction of Microbial Activities
9.4 Effect of Rhizosphere Microorganisms on Soil Quality
9.4.1 Microbe-Mediated Rhizosphere Interactions and Its Implication on Soil Nutrient Availability and Crop Productivity
9.4.2 Biological Control of Soil-Borne Phytopathogens and Insect Pests
9.4.2.1 Siderophore Production
9.4.2.2 Antibiosis and Production of Volatile Compounds
9.4.2.3 Induction of Plant Systemic Resistance
9.4.3 Organic Matter Decomposition and Nutrient Supply
9.4.4 Bioremediation of Polluted Soil
9.4.5 Drought, Salinity and Nutrient Stress Management
9.5 Management of Rhizosphere System for Sustainable Production
9.5.1 Reduction of Chemical Inputs by IBNM
9.5.2 Biofertilizer and Organic Inputs Application
9.5.3 Cultural Practices in Crops
9.6 Conclusion
References
10: Ralstonia solanacearum: Biology and its Management in Solanaceous Vegetable Crops
10.1 Introduction
10.2 Economic Impact of R. solanacearum
10.3 Symptomatology
10.4 Taxonomy of Ralstonia solanacearum
10.5 Diversity of R. solanacearum
10.6 Pathogen Classification
10.7 Diagnosis and Detection
10.8 Mechanisms of Bacterial Wilt Disease Development in Solanaceous Vegetables
10.9 Pathogenicity Determinants of R. solanacearum
10.10 Transmission, Spread, Survival, and Inoculum Source
10.11 Integrated Disease Management
10.11.1 Host Plant Resistance
10.11.2 Biological Control
10.11.3 Chemical Control
10.11.4 Cultural Control
10.12 Conclusion
References
11: Seed Endophytes: The Benevolent Existence in the Plant System
11.1 About Endophytes
11.2 Significance of Seed Endophytes
11.3 Diversity of Seed Endophytes in Different Crops
11.4 Population of Seed Endophytes in Different Crops
11.5 Entry and Colonization of Endophytes
11.6 Seed Endophytes in Climate Resilient Agriculture
11.7 Plant Beneficial Mechanisms of Seed Endophytes
11.8 Endophytic Microorganisms Influence Plant Gene Expression
11.9 Conclusion and Future Prospects
References
12: Exploitation of Plant Tissue Invading Rhizospheric Microbes as Bio-Fertilizers
12.1 Introduction
12.2 Entry and Colonization of Plant Tissues by Endophytes
12.2.1 Chemotactic Migration Towards Roots
12.2.2 Attachment on Root Surface
12.2.3 Entry and Distribution Inside Roots
12.3 Plant Responses upon Colonization by Endophytes
12.4 Endophytes as Bio-fertilizers
12.4.1 Nutrient Uptake
12.4.1.1 Nitrogen Fixation
12.4.1.2 Phosphate Solubilization
12.4.1.3 Sequestering Iron
12.4.1.4 Zinc Solubilization
12.4.2 Modulating Phytohormone Levels
12.4.2.1 Cytokinins and Gibberellins
12.4.2.2 Indole Acetic Acid (IAA)
12.4.2.3 Ethylene
12.4.3 Induced Systemic Resistance
12.5 Conclusion
References
13: Contribution of Microbe-Mediated Processes in Nitrogen Cycle to Attain Environmental Equilibrium
13.1 Introduction
13.2 Nitrogen Cycle: The Role of Microorganisms
13.2.1 Nitrogen Fixation
13.2.2 Nitrification
13.2.2.1 Autotrophic Nitrification
Aerobic Nitrification
Comammox
Anammox
13.2.2.2 Urea Hydrolysis
13.2.2.3 Heterotrophic Nitrification
13.2.3 Denitrification
13.2.4 Ammonification
13.3 Dissimilatory and Assimilatory Nitrate Reduction to Ammonia (DNRA and ANRA)
13.4 Codenitrification
13.5 Microbial Diversity: N Cycle
13.6 Different Ecosystems: Microbial Diversity (Gene Based) and N Cycle
13.6.1 Forest Ecosystem
13.6.2 Agroecosystems
13.6.2.1 Agroecosystem: Legume-Cultivated Soils
13.6.2.2 Agroecosystem: Paddy-Cultivated Soil
13.6.3 Terrestrial Antarctic Soils
13.6.4 Tropical Peatland: Drained and Natural Soils
13.7 Strategies to Maintain N Equilibrium
13.8 Conclusion
13.9 Future Perspective
References
14: Contribution of Zinc-Solubilizing and -Mobilizing Microorganisms (ZSMM) to Enhance Zinc Bioavailability for Better Soil, P...
14.1 Introduction
14.2 Contributions of Zinc in Different Life Forms
14.2.1 Microorganisms
14.2.2 Plants
14.2.3 Human
14.3 Zinc Deficiency and Malnutrition
14.4 Status and Fate of Zinc in Soil
14.5 Zinc-Solubilizing and -Mobilizing Microorganisms (ZSMM)
14.5.1 Solubilization by Bacteria
14.5.2 Solubilization by Fungi
14.6 Mechanisms of Zinc Solubilization and Mobilization by Microorganisms
14.6.1 Organic Acid Production
14.6.2 Zinc Chelation
14.6.3 Changes in Root Architecture for Zinc Uptake
14.6.4 Zinc Solubilization and Mobilization by Exopolysaccharide-Producing Microorganisms
14.7 Soil Zinc Mobilization by Zinc-Solubilizing and -Mobilizing Microorganisms (ZSMM) for Crop Zinc Assimilation and Producti...
14.8 Genetic Engineering of Zinc-Solubilizing and -Mobilizing Microorganisms (ZSMM)
14.9 Conclusion
14.10 Future Line of Work
References
15: Fungal Siderophore: Biosynthesis, Transport, Regulation, and Potential Applications
15.1 Introduction
15.2 Iron in the Environment
15.3 Microbial Siderophores
15.4 Fungal Siderophores and Classification
15.5 Siderophore Biosynthesis
15.6 Siderophore-Mediated Iron Transport by Fungi
15.7 FRE Family of Reductases
15.8 The Fet3p/Ftr1p Oxidase/Permease Complex
15.9 Non-reductive Uptake Systems: The Siderophore-Iron Transporters
15.10 Regulation
15.11 Biotechnological Applications
15.11.1 Medical
15.11.2 Remediation
15.11.3 Growth-Promoting Activity and Biocontrol of Plants Pathogen
15.11.4 Siderophores as Enzyme Inhibitors
15.12 Conclusions
References
16: Status of Silicon in Ecosystem, Silicon Solubilization by Rhizospheric Microorganisms and Their Impact on Crop Productivity
16.1 Introduction
16.2 Accumulation of Silicon in Different Microbiota and Sponges
16.2.1 Diatoms
16.2.2 Radiolarians
16.2.3 Silicoflagellates (Dictyochophyceae)
16.2.4 Siliceous Sponge
16.3 Biogeochemical Cycle of Silicon
16.4 Terrestrial Silicon Cycle
16.4.1 Sources
16.4.2 Sinks
16.5 Marine Silicon Cycle
16.5.1 Sources
16.5.2 Sinks
16.6 Role of Microbes in Silicate Weathering
16.6.1 Solubilization of Silicates by Ligands
16.6.2 Solubilization of Silicates by Organic and Inorganic Acids
16.6.3 Solubilization of Silicates by Alkali
16.6.4 Solubilization of Silicates by Extracellular Polysaccharide and Polymers
16.7 Rhizosphere Microbes and Silicon Availability
16.8 Influence of Silicate Solubilizing Bacteria on Crop Productivity
16.9 Conclusion
16.10 Future Line of Work
References
17: Diversity and Function of Microbes Associated with Rhizosphere of Finger Millet (Eleusinecoracana)
17.1 Introduction
17.2 Nutraceutical Value of Finger Millet
17.3 Microflora and Finger Millet
17.4 Microbial Diversity in Finger Millet
17.4.1 Bacterial Association with Finger Millet Rhizosphere
17.4.2 Fungi Association with Finger Millet Rhizosphere
17.4.3 Synergistic Effect of Dual Inoculation (Bacteria and Fungi) on Finger Millet
17.5 Conclusion
17.5.1 Future Aspects
References
18: Diversity and Community Structure of Arbuscular Mycorrhizal Fungi in the Rhizosphere of Salt-Affected Soils
18.1 Introduction
18.1.1 Arbuscular Mycorrhizal Fungi (AMF)
18.1.2 AMF Mediated Plant Growth Promotion
18.2 Soil Salinity and its Impact on Plant Growth
18.2.1 Salt-Affected Ecosystem
18.2.2 Mitigation of Salt Stress by AMF
18.3 AMF Phylogenetic Position and Classification
18.3.1 Impact of Soil Salinity on AMF Symbiosis
18.3.2 Soil Salinity on AMF Community Changes
18.4 Future Prospects
References
19: Beta-Glucanolytic Soil Actinomycetes: Diversity and Applications
19.1 Introduction
19.2 Actinobacteria
19.3 Beta Glucanase: A Glycosyl Hydrolase (GH)
19.4 Beta-Glucanolytic Actinomycetes: Diversity
19.5 Western Ghats in Kerala: Excellent Resource of Beta-Glucanolytic Soil Actinomycetes
19.6 Conclusion
References
20: Microbial Diversity of Chickpea Rhizosphere
20.1 Introduction
20.2 Microbial Diversity of Chickpea Rhizopshere
20.2.1 Chickpea Rhizosphere
20.2.2 Rhizobial Species
20.2.3 Root-Associated Bacterial Endophytes of Chickpea
20.2.4 Actinobacteria of Chickpea
20.2.5 Chickpea Rhizosphere Fungi
20.3 Functional Properties of Chickpea Rhizobacteria
20.3.1 Phosphate Solubilization
20.3.2 Biotic Stress Management
20.3.3 Abiotic Stress Management
20.4 Microbial Consortia and Chickpea Growth
References
21: The Rhizosphere Microbiome and Its Role in Plant Growth in Stressed Conditions
21.1 Introduction
21.2 The Idea of Rhizosphere Microbiome
21.3 Dynamics of the Microbiome in Rhizosphere in Stress Environment
21.3.1 Crop Rotation Changes Microbiome
21.3.2 Phosphorus Shapes Microbiome
21.3.3 Saline Stress Shapes Microbiome
21.3.4 Invaders Shape Microbiome Dynamics
21.4 Root Exudates(RE) Shape Microbiome to Improve Plant Growth in Stress Conditions
21.5 Application of PGPR Shape the Rhizosphere Microbiome to Improve the Plant Growth in Stress Conditions
21.6 Specific Rhizospheric Microbiome Improves the Plant Growth in Stress Conditions
21.6.1 Specific Microbiome Supports the Plant Growth in Abiotic Stress Conditions
21.6.2 Specific Microbiome Supports the Plant Growth in Biotic Stress Conditions
21.7 Modern Molecular Sequencing Techniques: To Know the Functions of the Rhizospheric Microbiome in Plant Growth in Stress Co...
21.7.1 Metaproteomics
21.7.2 Metagenomics
21.7.3 Metatranscriptomics
21.7.4 Introduction of Stable Isotope Probe (SIP) with Molecular Biology Techniques
21.8 Conclusion and Prospects
References
22: Rhizobacteria-Mediated Alleviation of Abiotic Stresses in Crops
22.1 Introduction
22.2 Impact of Abiotic Stresses on Crop Plants
22.3 Mitigation of Abiotic Stresses Using Rhizospheric Microbes
22.4 Mechanisms of Tolerance Provided by Soil Bacteria/Rhizobacteria
22.4.1 Mitigation of Stresses via Secreted Phytohormones
22.4.2 Mitigation of Stresses via the Production of Osmoprotectants
22.4.3 Mitigation of Stresses by Maintaining Ion Homeostasis and Detoxification
22.5 Omics Strategies for Cross-Tolerance
22.5.1 Genomics Approaches
22.5.2 Proteomics Approaches
22.5.3 Metabolomics Approaches
22.6 Conclusion
22.7 Future Prospect
References
23: Rhizospheric Microbes as Potential Tool for Remediation of Carbofuran: An Overview
23.1 Introduction
23.2 Remedial Measures for Carbofuran
23.2.1 Physicochemical Treatments
23.2.2 Rhizospheric Microbes for Carbofuran Removal
23.2.2.1 Microbial Degradation of Carbofuran
23.2.2.2 Fungal Degradation of Carbofuran
23.2.3 Pathways for Microbial Degradation of Carbofuran
23.3 Advanced Strategies for Enhanced Carbofuran Degradation by Microbes from Contaminated Soil
23.3.1 Organic Amendments: Biostimulants for Soil Applications
23.3.2 Immobilized Potential Microbes: Soil Inoculants for Onsite Applications
23.4 Conclusion
References
24: Trichoderma spp.: A Unique Fungal Biofactory for Healthy Plant Growth
24.1 Introduction
24.2 Root Colonization Mechanism of Trichoderma spp.
24.3 Trichoderma in Biotic Stress Alleviation
24.3.1 Trichoderma as Inducer for Defense Signaling Pathways
24.4 Trichoderma in Abiotic Stress Alleviation
24.5 Nutrient Immobilization and Solubilization
24.6 Mycoparasitism
24.7 Antibiosis
24.8 Conclusion
References
25: Management of Sclerotium rolfsii Induced Diseases in Crops by Trichoderma Species
25.1 Introduction
25.2 Sclerotium rolfsii
25.3 Management Practices Adopted for Control of S. rolfsii
25.3.1 Biological Control
25.3.1.1 Trichoderma Species
25.3.1.2 Historical Background of the Taxonomy of Trichoderma
25.3.1.3 Biological Control Using Trichoderma Species
25.4 Mechanism of Action
25.4.1 Mycoparasitism
25.4.2 Antibiosis
25.4.3 Competition
25.4.4 Induced Resistance
25.5 Biological Management of S. rolfsii by Trichoderma Species
25.5.1 Trichoderma in Consortium
25.6 Bioformulations of Trichoderma Species
25.7 Challenges in Bioformulations of Trichoderma Species
25.8 Conclusion
References
26: Biotic Stress Management in Horticultural Crops Using Microbial Intervention
26.1 Introduction
26.2 Microbial Interventions for Plant Disease Management
26.2.1 Root Pathogens
26.2.2 Foliar and Above Ground Pathogens
26.2.3 Postharvest Pathogens
26.2.4 Mode of Action of Biological Control Agents against Plant Diseases
26.2.5 Induction of Systemic Resistance (ISR)
26.2.6 Mass Production Technology for Biocontrol Agents of Plant Pathogens
26.2.6.1 Mass Production of Fungal Bioagents
26.2.6.2 Mass Production of Bacterial Antagonists
26.2.6.3 Fermentation
26.2.7 Development of Formulations of Bioagents
26.2.7.1 Development of Formulations of Trichoderma spp.
26.2.7.2 Formulation of Antagonistic Bacteria
26.2.8 Delivery of Biocontrol Agents used Against Plant Pathogens
26.2.9 Compatibility with Fugicides
26.2.10 Compatibility with Biofertilizers
26.2.11 Biological Control of Bacterial Diseases using Bacteriophages
26.3 Microbial Interventions for Insect Pest Management
26.3.1 Entomopathogens
26.3.1.1 Viruses
26.3.1.2 Mode of Action
26.3.1.3 Symptoms of Virus Infection in Insects
26.3.1.4 Formulations Available, Commercialization of the ViralBioagents
26.3.2 Entomopathogenic Fungi
26.3.2.1 Mode of Action of Entomopathogenic Fungi
26.3.3 Entomopathogenic Bacteria
26.3.3.1 Mode of Action of Bacillus thuringiensis
26.3.4 Bioefficacy of Entomopathogenic Microbes Against Pests of Horticultural Crops
26.4 Microbial Interventions for Nematode Management in Horticultural Crops
26.4.1 Fungal Bioagents for Nematode Control
26.4.1.1 Purpureocillium lilacinum (=Paecilomyces lilacinus)
26.4.1.2 Mode of Action of Purpureocillium lilacinum on Phytonematodes
26.4.1.3 Bioefficacy of P. lilacinum on Plant Parasitic Nematodes in Horticultural Crops
26.4.2 Pochonia chlamydosporia (=Verticillium chlamydosporium)
26.4.2.1 Mode of Action of Pochonia chlamydosporia
26.4.2.2 Biocontrol Potential of P. chlamydosporia in Managing Nematodes of Horticultural Crops
26.4.3 Trichoderma spp.
26.4.3.1 Mode of Action of Trichoderma spp.
26.4.3.2 Commercialization of Trichoderma spp.
26.4.3.3 Biocontrol Potential of Trichoderma spp. Against Plant Parasitic Nematodes in Horticultural Crops
26.4.4 Arbuscular Mycorrhizal (AM) Fungi
26.4.4.1 Mode of Action of AM Fungi Against Phytonematodes
26.4.4.2 Biocontrol Potential of AM Fungi Against Plant Parasitic Nematodes
26.4.5 Bacterial Bioagents for Nematode Control
26.4.5.1 Obligate Parasitic Bacteria, Pasteuria spp.
26.4.5.2 Antagonistic Bacteria
26.4.5.3 Rhizobacteria
Bacillus spp.
Pseudomonas spp.
26.4.5.4 Commercial Rhizobacterial Products as Bionematicides
26.4.5.5 Cry protein-forming Bacteria
26.4.5.6 Other Soil Bacteria
26.4.5.7 Field Application of Microbials for Nematode Management
26.5 Challenges Facing Commercialization of Microbial Biopesticides in India
26.6 Conclusion
References
27: Commercial Aspects of Biofertilizers and Biostimulants Development Utilizing Rhizosphere Microbes: Global and Indian Scena...
27.1 Introduction
27.2 Biostimulants
27.3 Rhizospheric Bacteria
27.4 Rhizospheric Fungi
27.5 Rhizospheric Endophytes
27.6 Microbial Biostimulants and Induced Systemic Resistance in Plants
27.7 Commercial Aspects of Biostimulants
27.8 Plant Biostimulants and Regulations
27.9 Biofertilizers
27.10 Market Demand and Global Opportunities
27.11 Global Regulatory Guidelines for Biofertilizers
27.12 Potential for Biofertilizers and Biostimulants-Indian Perspective
27.13 Commercial and Regulatory Challenges-Guidelines vs. Ground Reality
27.14 Conclusions
References
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Microorganisms for Sustainability 23 Series Editor: Naveen Kumar Arora
Sushil Kumar Sharma Udai B. Singh · Pramod Kumar Sahu Harsh Vardhan Singh Pawan Kumar Sharma Editors
Rhizosphere Microbes Soil and Plant Functions
Microorganisms for Sustainability Volume 23 Series Editor Naveen Kumar Arora, Environmental Microbiology, School for Environmental Science, Babasaheb Bhimrao Ambedkar University, Lucknow, Uttar Pradesh, India
More information about this series at http://www.springer.com/series/14379
Sushil Kumar Sharma • Udai B. Singh • Pramod Kumar Sahu • Harsh Vardhan Singh • Pawan Kumar Sharma Editors
Rhizosphere Microbes Soil and Plant Functions
Editors Sushil Kumar Sharma NAIMCC ICAR-National Bureau of Agriculturally Important Microorganisms Maunath Bhanjan, Uttar Pradesh, India ICAR-National Institute of Biotic Stress Management Raipur, Chhattisgarh, India Pramod Kumar Sahu Plant-Microbe Interaction and Rhizosphere Biology Lab ICAR-National Bureau of Agriculturally Important Microorganisms Maunath Bhanjan, Uttar Pradesh, India
Udai B. Singh Plant-Microbe Interaction and Rhizosphere Biology Lab ICAR-National Bureau of Agriculturally Important Microorganisms Maunath Bhanjan, Uttar Pradesh, India
Harsh Vardhan Singh Plant-Microbe Interaction and Rhizosphere Biology Lab ICAR-National Bureau of Agriculturally Important Microorganisms Maunath Bhanjan, Uttar Pradesh, India
Pawan Kumar Sharma Plant Pathology ICAR-National Bureau of Agriculturally Important Microorganisms Maunath Bhanjan, Uttar Pradesh, India
ISSN 2512-1901 ISSN 2512-1898 (electronic) Microorganisms for Sustainability ISBN 978-981-15-9153-2 ISBN 978-981-15-9154-9 (eBook) https://doi.org/10.1007/978-981-15-9154-9 # Springer Nature Singapore Pte Ltd. 2020 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore
Preface
Plants are an incredible gift of nature not only to mankind but also to a myriad of other organisms for their survival on the planet Earth. The impact of plants on the environment including the microbiome and viceversa is enormous and is of great significance to all the component partners. The system consisting of plants, their environment, and all the associated organisms including microorganisms in this environment is cumulatively known as phytobiome, while plants with their associated extra- and endo-cellular microbiome constitute the holobiont. The genome of such associated microbiome is referred to as the ‘second genome’ of the plant. The plant genome and microbial genome collectively constitute ‘hologenome’. Similar to phytobiome, there is a concept of ‘rhizobiome’ which consists of roots, their surrounding environment and all associated organisms living in that particular environment. The rhizosphere is the zone around roots of the plants in the soil that may extend from a millimetre to 3 centimetre and beyond around the root surface. This zone contains sloughed off root, mucilage, root exudates and gases. The gases released from roots in the soil dissipate to comparatively longer distances leading to the extended size of rhizospheric zone up to many centimetres. The rhizosphere is of paramount importance for ecosystem services, namely carbon and water cycling, nutrient trapping/cycling or mobilization, carbon uptake and storage etc. The rhizosphere, one of the most dynamic interfaces on Earth, contains up to 1011 microbial cells per gram of soil representing over 30,000 bacterial species. Such rhizomicrobiome plays an important role in the regulation of biogeochemical cycles, global climate and sustaining plant growth. The health and productivity of plants are governed by various microbial mechanisms such as nutrient solubilization and mineralization, biological nitrogen fixation, induced systemic resistance (ISR), systemic acquired resistance (SAR), production of plant growth regulators, siderophores, proton extrusion, organic acids, secondary metabolites and volatile organic compounds (VOCs) as well as protection by enzymes like 1-aminocyclopropane-1-carboxylate (ACC)-deaminase, chitinase and glucanase functioning in the rhizosphere. Ward off biotic stress, the plants protect themselves by recruiting a group of disease-resistance inducing and plant growth-promoting microorganisms (PGPM) in the rhizosphere which is under perpetual pressure from soil-borne pathogens and helps to maintain PGPM descendents in the rhizosphere soil. This phenomenon is called ‘soil-borne legacy’. Likewise, plants also have a v
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unique mechanism of deploying microbes that confer tolerance to abiotic stresses such as drought, salinity, alkalinity, temperature etc. Hence, the plant system is equipped with unique mechanisms of combating biotic and abiotic stresses via beneficial microbes (Defense Biome) which tends to ameliorate the ultimate impacts of these stresses and almost ensures the maintenance of better plant growth and development. Manipulation of the rhizospheric system is, though an effective strategy, yet a major challenge for modulating plant growth and development. Traditionally, this manipulation is done by natural interventions with aim to improve soil health but with greater understanding and advancement in technology, external stimuli are now being provided in the form of certain biomolecules by introducing PGPM or metabolites to make biased/engineered rhizosphere suitable for desirable results. The soil characteristics and associated agricultural management practices such as tillage, organic management and crop rotation also shift the soil microbiome and determine soil quality in terms of plant growth and development. This book addresses various issues of plant and soil that are to be modulated either by resident microbes or by their external application. The book covers (1) the role of microbes in soil and plant health, (2) methods for assessment of microbial diversity in the rhizosphere, (3) microbes as the driver of nutrient transformation and soil quality, (4) the role of microbes in bioremediation, and biotic and abiotic stress management, (5) microbes associated with solubilization and mobilization of micronutrients for biofertilization and biofortification, (6) signalling in the rhizosphere and (7) commercial aspects of rhizospheric microbes. We expect that the book would be useful for students, researchers, industrialists, entrepreneurs, academicians and policymakers to understand the roles of rhizospheric microorganisms in sustainable agriculture and provide directions for the future course of action. Uttar Pradesh/ Chhattisgarh Uttar Pradesh
Sushil K. Sharma Udai B. Singh Pramod K. Sahu Harsh V. Singh Pawan K. Sharma
Contents
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Microbial Interactions in the Rhizosphere Contributing Crop Resilience to Biotic and Abiotic Stresses . . . . . . . . . . . . . . . . . . . . Deepti Malviya, Udai B. Singh, Shailendra Singh, Pramod K. Sahu, K. Pandiyan, Abhijeet S. Kashyap, Nazia Manzar, Pawan K. Sharma, H. V. Singh, Jai P. Rai, and Sushil K. Sharma
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Rhizosphere Microbes for Sustainable Maintenance of Plant Health and Soil Fertility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Madhurankhi Goswami, Chandana Malakar, and Suresh Deka
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Dissecting Structure and Function of Plant Rhizomicrobiome: A Genomic Approach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hemant Dasila, Samiksha Joshi, and Manvika Sahgal
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Plant Root Exudates as Determinant of Rhizomicrobiome . . . . . . V. Balasubramanian, Arunima Sur, Kush Kumar Nayak, and Ravi Kant Singh
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Rhizospheric Microbial Community: Ecology, Methods, and Functions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Amir Khan, Manisha Joshi, and Ajay Veer Singh
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Signaling in the Rhizosphere for Better Plant and Soil Health . . . Hemant S. Maheshwari, Richa Agnihotri, Abhishek Bharti, Dipanti Chourasiya, Pratibha Laad, Ajinath Dukare, B. Jeberlin Prabina, Mahaveer P. Sharma, and Sushil K. Sharma
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Microbial Transformation of Nutrients in Soil: An Overview . . . . Deep Mohan Mahala, Hemant S. Maheshwari, Rajendra Kumar Yadav, B. Jeberlin Prabina, Abhishek Bharti, Kiran K. Reddy, Chiranjeev Kumawat, and Aketi Ramesh
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Microbial Indicator of Soil Health: Conventional to Modern Approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dolamani Amat, J. K. Thakur, Asit Mandal, A. K. Patra, and Kampati Kiran Kumar Reddy
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Rhizosphere Microbes: Driver for Soil Health Management . . . . . H. K. Patel, R. V. Vyas, A. Ramesh, and J. P. Solanki
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Ralstonia solanacearum: Biology and its Management in Solanaceous Vegetable Crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Balamurugan, K. Sakthivel, R. K. Gautam, Sushil K. Sharma, and A. Kumar
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Seed Endophytes: The Benevolent Existence in the Plant System . . Shrey Bodhankar and Minakshi Grover
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Exploitation of Plant Tissue Invading Rhizospheric Microbes as Bio-Fertilizers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Himani Chaturvedi and Anil Prakash
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Contribution of Microbe-Mediated Processes in Nitrogen Cycle to Attain Environmental Equilibrium . . . . . . . . . . . . . . . . . . . . . . Humera Quadriya, Mohammed Imran Mir, K. Surekha, S. Gopalkrishnan, M. Yahya Khan, Sushil K. Sharma, and Hameeda Bee Contribution of Zinc-Solubilizing and -Mobilizing Microorganisms (ZSMM) to Enhance Zinc Bioavailability for Better Soil, Plant, and Human Health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ramesh Chandra Yadav, Sushil K. Sharma, Aketi Ramesh, Kusum Sharma, Pawan K. Sharma, and Ajit Varma Fungal Siderophore: Biosynthesis, Transport, Regulation, and Potential Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Keshawanand Tripathi, Narendra Kumar, Meenakshi Singh, and Ravi Kant Singh
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Status of Silicon in Ecosystem, Silicon Solubilization by Rhizospheric Microorganisms and Their Impact on Crop Productivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Prakash B. Nagabovanalli, Sabyasachi Majumdar, and Sandhya Kollalu
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Diversity and Function of Microbes Associated with Rhizosphere of Finger Millet (Eleusine coracana) . . . . . . . . . . . . . . . . . . . . . . . Renu Choudhary, Geeta Rawat, Vijay Kumar, and Vivek Kumar
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Diversity and Community Structure of Arbuscular Mycorrhizal Fungi in the Rhizosphere of Salt-Affected Soils . . . . . . . . . . . . . . . R. Krishnamoorthy, R. Anandham, M. Senthilkumar, and Tongmin Sa
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Beta-Glucanolytic Soil Actinomycetes: Diversity and Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lekshmi K. Edison and N. S. Pradeep
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Microbial Diversity of Chickpea Rhizosphere . . . . . . . . . . . . . . . . Balram Sahu, Deep Chandra Suyal, Pramod Prasad, Vinay Kumar, Anup Kumar Singh, Sonu Kushwaha, P. Karthika, Annand Chaubey, and Ravindra Soni
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The Rhizosphere Microbiome and Its Role in Plant Growth in Stressed Conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bhrigu Bhuyan, Sourav Debnath, and Piyush Pandey
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Rhizobacteria-Mediated Alleviation of Abiotic Stresses in Crops . . Priyanka Gupta and Manjari Mishra
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Rhizospheric Microbes as Potential Tool for Remediation of Carbofuran: An Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mohd Aamir Khan, Abhishek Sharma, Sonal Yadav, and Satyawati Sharma
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Trichoderma spp.: A Unique Fungal Biofactory for Healthy Plant Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hesham Ali El Enshasy, Kugan Kumar Ambehabati, Siti Zulaiha Hanapi, Daniel J. Dailin, Elsayed Ahmed Elsayed, Dalia Sukmawati, and Roslinda Abd Malek Management of Sclerotium rolfsii Induced Diseases in Crops by Trichoderma Species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ratul Moni Ram, Rahul Singh Rajput, and Anukool Vaishnav Biotic Stress Management in Horticultural Crops Using Microbial Intervention . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . R. Umamaheswari, N. R. Prasannakumar, S. Sriram, Sushil K. Sharma, M. S. Rao, and M. K. Chaya Commercial Aspects of Biofertilizers and Biostimulants Development Utilizing Rhizosphere Microbes: Global and Indian Scenario . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. John Peter, E. Leo Daniel Amalraj, and Venkateswara Rao Talluri
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Editors and Contributors
About the Editors Sushil Kumar Sharma, National Agriculturally Important Microbial Culture Collection (NAIMCC), ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India. Present Address: ICARNational Institute of Biotic Stress Management, Raipur, Chhattisgarh, India Dr Sushil K. Sharma is currently working as a Principal Scientist (Agricultural Microbiology) at ICAR-National Institute of Biotic Stress Management, Raipur, Chhattisgarh, India in the area of microbial resource conservation, secondary metabolites and antimicrobial peptides for biotic stress management of crops. In the recent past, he worked at ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India in the capacity of officer in-charge/focal point, National Agriculturally Important Microbial Culture Collection [NAIMCC-International Depository Authority (IDA)-Budapest Treaty Notification No. 338]. He has delivered talks in International PGPR Conference in Medellin, Columbia in June 2012 and subsequently in Asian PGPR Conference, Tashkent, Uzbekistan in 2019. So far, he had published 110 articles (research, review, book chapter, book, etc.) in both national and international journals/book/ conferences. Udai B. Singh, Plant–Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India. Dr. Udai B. Singh is presently working as Scientist (Senior Scale) in the Plant– Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India. His specialized area is plant–microbe interactions in the rhizosphere with special reference to biotic and abiotic stress management/molecular biology/biotechnology/plant pathology. He has been awarded Fellow of Society for Applied Biotechnology, ‘DST Young Scientist’ under Fast-Track Scheme, ‘Young Scientist Award’ of RASSA, New Delhi, Bharat Shiksha Ratan Award, Scientist of the Year Award-2019, K.P.V. Menon and Prof. K.S. Bilgrami Best Poster Award for the Year 2018 by Indian Phytopathological Society, New Delhi and Indian Society xi
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of Mycology and Plant Pathology, Udaipur. He has published several research articles in the national and international journals of scientific reputes, books, scientific magazines, technical bulletins, book chapters and scientific poplar articles. He is also the editor the journal ‘Indian Phytopathology’ published by Springer Nature. Pramod Kumar Sahu, Plant–Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India. Dr. Pramod Kumar Sahu has completed B.Sc. from IGKVV, M.Sc. (GoldMedalist) and Ph.D. (Agricultural Microbiology) from UAS, Bengaluru, India. He was a DST-Inspire Fellow and was selected in various national level exams including ICAR-JRF, ICAR-SRF, ICAR-NET, ARS and GATE. Being a Scientist of Agricultural Microbiology at ICAR-NBAIM, Mau, India, working on plant–endophyte interaction, consortium of bioinoculants and biological control and has more than 45 publications, 6 training manuals, 13 extension folders, 3 popular articles and 30 abstracts to his credit. He has won Dr. B. P. Pal’s Prize Gold Medal, Dr. G. Rangaswamy Gold Medal, Willium Rigo award, several best posters and best oral presentation awards along with Young Scientist in Agricultural Microbiology 2018 award. Harsh Vardhan Singh, Plant–Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India. Dr. Harsh Vardhan Singh is currently working as a Principal Scientist (Plant Pathology) at ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India. He is specialized in the areas of plant–microbe Interactions, biological control, biotic and abiotic stress management. He has vast research experience in the field of plant pathology with special reference to temperate crops of Jammu and Kashmir and grasses and fodder crops. He has served as a Junior Scientist-cum-Assistant Professor in Plant Pathology (2002–2007) at RARSS, SKUAST-K, Kargil, Programme Coordinator (2007–2009) at KVK, Poonch, SKUAST-J and Senior Scientist (Plant Pathology) at ICAR-IGFRI, Jhansi from 2009 to 2018. Pawan Kumar Sharma, National Agriculturally Important Microbial Culture Collection (NAIMCC), ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India. Dr. Pawan Kumar Sharma did his M.Sc. and Ph.D. in Plant Pathology at DR YSP University of Horticulture and Forestry, Solan, HP. He is working as Principal Scientist at ICAR-NBAIM at Mau, UP since September 2013. He had been associated with 14 projects as PI or Co-PI sponsored by various agencies. Currently, he is working on biological control of wilt and collar rot diseases through liquidbased formulation of Trichoderma and is also in-charge of National Agriculturally
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Important Microbial Culture Collection. He has published 46 research papers in national and international journals, edited 4 books and authored 1 book.
About the Series-Editor Naveen Kumar Arora, Fellow of International Society of Environmental Botanists (FISEB), PhD in Microbiology, is Professor and Head, Department of Environmental Science at Babasaheb Bhimrao Ambedkar University (a Central University), Lucknow, Uttar Pradesh, India. He is a renowned researcher in the field of environmental microbiology and biotechnology. His specific area of research is plant– microbe interactions, particularly plant growth-promoting rhizobacteria. He has more than 75 research articles published in premium international journals and several articles published in magazines and dailies. He is an editor of 25 books, published by Springer. He is a member of several national and international societies, Secretary General of Society for Environmental Sustainability, in editorial board of 4 journals and reviewer of several international journals. He is also the editor in chief of the journal ‘Environmental Sustainability’ published by Springer Nature. He has delivered lectures in conferences and seminars around the globe. He has a long-standing interest in teaching at the PG level and is involved in taking courses in bacteriology, microbial physiology, environmental microbiology, agriculture microbiology and industrial microbiology. He has been an advisor to 134 postgraduate and 11 doctoral students. He has been awarded for excellence in research by several societies and national and international bodies/organizations. Although an academician and researcher by profession, he has a huge obsession for the wildlife and its conservation and has authored a book, Splendid Wilds. He is the President of Society for Conservation of Wildlife and has a dedicated website www. naveenarora.co.in for the cause of wildlife and environment conservation.
Contributors Richa Agnihotri ICAR-Indian Institute of Soybean Research, Indore, Madhya Pradesh, India E. Leo Daniel Amalraj Prof. TNA Innovation Centre, Varsha Bioscience and Technology India Private Limited, Jiblakpally, Yadadri District, Telangana, India Kugan Kumar Ambehabati Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Johor, Malaysia A. Balamurugan Department of Plant Pathology, Centre for Plant Protection Studies, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India V. Balasubramanian Amity Institute of Biotechnology, Amity University Chhattisgarh, Raipur, Chhattisgarh, India
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Hameeda Bee Department of Microbiology, Osmania University, Hyderabad, Telangana, India Abhishek Bharti ICAR-Indian Institute of Soybean Research, Indore, Madhya Pradesh, India Bhrigu Bhuyan Department of Microbiology, Assam University, Silchar, Assam, India Shrey Bodhankar ICAR- Central Research Institute for Dryland Agriculture, Hyderabad, Telangana, India Present address: ICAR-Indian Institute of Oilseeds Research, Hyderabad, Telangana, India Himani Chaturvedi Department of Microbiology, Barkatullah University, Bhopal, Madhya Pradesh, India Annand Chaubey Banda University of Agriculture and Technology, Banda, Uttar Pradesh, India Rajan Chaurasia Institute of Environment & Sustainable Development, Banaras Hindu University, Varanasi, Uttar Pradesh, India M. K. Chaya ICAR-Indian Institute of Horticultural Research, Bengaluru, Karnataka, India Renu Choudhary Himalayan School of Biosciences, Swami Rama Himalayan University, Dehradun, Uttarakhand, India Dipanti Chourasiya ICAR-Indian Institute of Soybean Research, Indore, Madhya Pradesh, India Daniel J. Dailin Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Johor, Malaysia School of Chemical and Energy Engineering, Faculty of Engineering, Universiti Teknologi Malaysia (UTM), Johor Bahru, Johor, Malaysia Hemant Dasila Department of Microbiology, G.B.Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India Sourav Debnath Department of Microbiology, Assam University, Silchar, Assam, India Suresh Deka Resource Management & Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India Ajinath Dukare ICAR- Central Institute of Post-Harvest Engineering and Technology (CIPHET), Abohar, Panjab, India Lekshmi K. Edison Microbiology Division, KSCSTE-Jawaharlal Nehru Tropical Botanic Garden and Research Institute, Thiruvananthapuram, Kerala, India
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Hesham Ali El Enshasy Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Johor, Malaysia School of Chemical and Energy Engineering, Faculty of Engineering, Universiti Teknologi Malaysia (UTM), Johor Bahru, Johor, Malaysia City of Scientific Research and Technology Application, New Burg Al Arab, Alexandria, Egypt Elsayed Ahmed Elsayed Bioproduct Development Chair, Zoology Department, Faculty of Science, Kind Saud University, Riyadh, Kingdom of Saudi Arabia Chemistry of Natural and Microbial Products Department, National Research Centre, Cairo, Egypt R. K. Gautam Division of Germplasm Evaluation, ICAR - National Bureau of Plant Genetic Resources, New Delhi, India S. Gopalkrishnan ICRISAT-International Crops Research Institute for the Semi Arid Tropics, Hyderabad, Telengana, India Madhurankhi Goswami Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India Minakshi Grover ICAR-Indian Agriculture Research Institute, New Delhi, India Priyanka Gupta Department of Biotechnology, Maharashtra Education Society’s Abasaheb Garware College, Savitribai Phule Pune University, Pune, Maharashtra, India Siti Zulaiha Hanapi Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Johor, Malaysia Manisha Joshi Department of Microbiology, G.B.Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India Samiksha Joshi Department of Microbiology, G.B.Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India P. Karthika Department of Agricultural Microbiology, College of Agriculture, Indira Gandhi Krishi Vishwavidyalaya, Raipur, Chhattisgarh, India Abhijeet S. Kashyap Plant-Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India Amir Khan Department of Microbiology, G.B.Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India Mohd Aamir Khan Centre for Rural Development and Technology, Indian Institute of Technology Delhi, Delhi, India Yahya Khan M Kalam Biotech Private Limited, Hyderabad, Telengana, India
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Sandhya Kollalu Department of Soil Science and Agricultural Chemistry, University of Agricultural Sciences, Gandhi Krishi Vignana Kendra, Bangalore, Karnataka, India Anup Kumar Singh Department of Agricultural Microbiology, College of Agriculture, Indira Gandhi Krishi Vishwavidyalaya, Raipur, Chhattisgarh, India A. Kumar Division of Plant Pathology, ICAR - Indian Agricultural Research Institute, New Delhi, India Narendra Kumar Department of Biotechnology, IMS Engineering College, Ghaziabad, Uttar Pradesh, India Vijay Kumar Himalayan School of Biosciences, Swami Rama Himalayan University, Dehradun, Uttarakhand, India Vinay Kumar ICAR-National Institute of Biotic Stress Management, Raipur, Chhattisgarh, India Vivek Kumar Himalayan School of Biosciences, Swami Rama Himalayan University, Dehradun, Uttarakhand, India Chiranjeev Kumawat SKN Agriculture University, Jobner, Rajasthan, India Sonu Kushwaha Department of Agricultural Microbiology, College of Agriculture, Indira Gandhi Krishi Vishwavidyalaya, Raipur, Chhattisgarh, India Pratibha Laad ICAR-Indian Institute of Soybean Research, Indore, Madhya Pradesh, India Deep Mohan Mahala ICAR-Indian Institute of Maize Research, Ludhiana, Punjab, India Hemant S. Maheshwari Ecophysiology of Plants, Faculty of Science and Engineering, GELIFES-Groningen Institute for Evolutionary Life Sciences, Groningen, The Netherlands Past Address: ICAR-Indian Institute of Soybean Research, Indore, Madhya Pradesh, India Sabyasachi Majumdar Department of Soil Science and Agricultural Chemistry, University of Agricultural Sciences, Gandhi Krishi Vignana Kendra, Bangalore, Karnataka, India Present address: College of Agriculture, Central Agricultural University — I, Kyrdemkulai, Meghalaya, India Chandana Malakar Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India Department of Biotechnology, Gauhati University, Guwahati, Assam, India Roslinda Abd Malek Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Johor, Malaysia
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Deepti Malviya Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India Nazia Manzar Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India Mohammed Imran Mir Department of Botany, Osmania University, Hyderabad, Telangana, India Manjari Mishra Plant Stress Biology, International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg, New Delhi, India Prakash B. Nagabovanalli Department of Soil Science and Agricultural Chemistry, University of Agricultural Sciences, Bangalore, Karnataka, India Kush Kumar Nayak Amity Institute of Biotechnology, Amity University Chhattisgarh, Raipur, Chhattisgarh, India Piyush Pandey Department of Microbiology, Assam University, Silchar, Assam, India K. Pandiyan Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India H. K. Patel Department of Agricultural Microbiology, College of Agriculture, Indira Gandhi Krishi VishwaVidyalaya, Raipur, Chhattisgarh, India A. John Peter Prof. TNA Innovation Centre, Varsha Bioscience and Technology India Private Limited, Jiblakpally, Yadadri District, Telangana, India B. Jeberlin Prabina Department Of Soil Science and Agricultural Chemistry, Agricultural College and Research Institute Killikulam, Tamilnadu Agriculture University, Killikulam, Tamil Nadu, India N. S. Pradeep KSCSTE-Malabar Botanical Garden and Institute of Plant Sciences, Kozhikode, Kerala, India Anil Prakash Department of Microbiology, Barkatullah University, Bhopal, Madhya Pradesh, India Pramod Prasad Regional Station, ICAR-Indian Institute of Wheat and Barley Research, Shimla, Himachal Pradesh, India N. Prasannakumar ICAR-Indian Institute of Horticultural Research, Bengaluru, Karnataka, India Humera Quadriya Department of Microbiology, Osmania University, Hyderabad, Telangana, India
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J. P. Rai Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India Rahul Singh Rajput Faculty of Agricultural Sciences and Allied Sciences, Rama University, Kanpur, Uttar Pradesh, India Krishnamoorthy Ramasamy Department of Crop Management, Vanavarayar Institute of Agriculture, Pollachi, Tamil Nadu, India Aketi Ramesh ICAR-Indian Institute of Soybean Research, Indore, Madhya Pradesh, India Ratul Moni Ram Department of Plant Pathology, A.N.D.U.A & T, Kumarganj, Ayodhya, Uttar Pradesh, India M. S. Rao ICAR-Indian Institute of Horticultural Research, Bengaluru, Karnataka, India Geeta Rawat Himalayan School of Biosciences, Swami Rama Himalayan University Dehradun, Uttarakhand, India Kiran K. Reddy ICAR- Directorate of Groundnut Research, Junagarh, Gujarat, India Manvika Sahgal Department of Microbiology, G.B.Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India Balram Sahu Department of Agricultural Microbiology, College of Agriculture, Indira Gandhi Krishi Vishwavidyalaya, Raipur, Chhattisgarh, India Pramod K. Sahu ICAR-National Bureau of Agriculturally Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India
Important
K. Sakthivel Crop Protection Section, ICAR -Indian Institute of Oilseed Research, Hyderabad, Telangana, India Abhishek Sharma Amity Food and Agriculture Foundation, Amity University, Noida, Uttar Pradesh, India Kusum Sharma ICAR- Indian Institute of Pulses Research, Kanpur, Uttar Pradesh, India Mahaveer P. Sharma ICAR-Indian Institute of Soybean Research, Indore, Madhya Pradesh, India Pawan K. Sharma Plant-Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India Satyawati Sharma Centre for Rural Development and Technology, Indian Institute of Technology Delhi, Delhi, India
Editors and Contributors
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Sushil K. Sharma ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India ICAR—National Institute of Biotic Stress Management, Raipur, Chhattisgarh, India Ajay Veer Singh Department of Microbiology, G.B.Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India Harsh V. Singh Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India Meenakshi Singh Department of Botany, Banaras Hindu University, Varanasi, Uttar Pradesh, India Ravi Kant Singh Amity Institute of Biotechnology, Amity University Chhattisgarh, Raipur, Chhattisgarh, India Shailendra Singh Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India Udai B. Singh Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India J. P. Solanki Department of Agricultural Microbiology, B A College of Agriculture, Anand Agricultural University, Anand, Gujarat, India Ravindra Soni Department of Agricultural Microbiology, College of Agriculture, Indira Gandhi Krishi Vishwavidyalaya, Raipur, Chhattisgarh, India S. Sriram ICAR-Indian Institute of Horticultural Research, Bengaluru, Karnataka, India Dalia Sukmawati Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Negeri Jakarta, Jakarta, Indonesia Arunima Sur Amity Institute of Biotechnology, Amity University Chhattisgarh, Raipur, Chhattisgarh, India K. Surekha ICAR-Indian Institute of Rice Research, Rajendranagar, Hyderabad, Telangana, India Deep Chandra Suyal Department of Microbiology, Eternal University, Baru Sahib, Himachal Pradesh, India Venkateswara Rao Talluri TNA Innovation Centre, Varsha Bioscience and Technology India Private Limited, Hyderabad, Telangana, India Keshawanand Tripathi Centre for Conservation and Utilization of Blue-Green Algae, ICAR-Indian Agricultural Research Institute, New Delhi, India
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Editors and Contributors
R. Umamaheswari ICAR-Indian Institute of Horticultural Research, Bengaluru, Karnataka, India Anukool Vaishnav Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India Ajit Verma Amity University, Noida, Uttar Pradesh, India R. V. Vyas Department of Agricultural Microbiology, B A College of Agriculture, Anand Agricultural University, Anand, Gujarat, India Rajendra Kumar Yadav Agriculture University, Kota, Rajasthan, India Ramesh Chandra Yadav ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India Amity University, Noida, Uttar Pradesh, India Sonal Yadav Centre for Rural Development and Technology, Indian Institute of Technology Delhi, Delhi, India
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Microbial Interactions in the Rhizosphere Contributing Crop Resilience to Biotic and Abiotic Stresses Deepti Malviya, Udai B. Singh, Shailendra Singh, Pramod K. Sahu, K. Pandiyan, Abhijeet S. Kashyap, Nazia Manzar, Pawan K. Sharma, H. V. Singh, Jai P. Rai, and Sushil K. Sharma
Abstract
Rhizosphere is a hot spot where specific kinds of diverse microbial communities develop under the influence of exudates from plant roots and in turn modulate growth and development of the plant. Such communities with or without interactions perform an array of functions, including nitrogen fixation, P, Zn, Si and K-solubilization, siderophore production, ammonification, hormones production, ACC deaminase production, ethylene production, anammox, comammox, nitrification, denitrification, antagonisms, induce resistance to plant, C-sequestration, volatile production, secondary metabolites production and many others that are known to modulate soil and plant health contributing to the corresponding responses to various stresses of biotic and abiotic nature. The magnitude of resilience of plant to biotic and abiotic stresses is completely dependent on types of communities and their interactions. With enhanced knowledge and understanding about rhizosphere, researchers are evaluating various Deepti Malviya and Udai B. Singh have contributed equally. All authors contributed in the preparation of manuscript. All authors have approved the final version of the manuscript. D. Malviya · U. B. Singh (*) · S. Singh · P. K. Sahu · K. Pandiyan · A. S. Kashyap · N. Manzar · P. K. Sharma · H. V. Singh Plant-Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India J. P. Rai Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India S. K. Sharma Plant-Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India Present Address: ICAR-National Institute of Biotic Stress Management, Raipur, Chhattisgarh, India # Springer Nature Singapore Pte Ltd. 2020 S. K. Sharma et al. (eds.), Rhizosphere Microbes, Microorganisms for Sustainability 23, https://doi.org/10.1007/978-981-15-9154-9_1
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approaches to engineer rhizosphere in such way that it enables plant to enhance the productivity and sustain it while maintaining soil health. This chapter highlights detailed account of microbial interactions in the rhizosphere with associated mechanisms that contribute to resilience of plants to stress for better growth and development. Keywords
Plant microbiome · Rhizosphere interaction · Biotic stresses · Abiotic stresses · PAMPs · MAMPs · Rhizosphere engineering
1.1
Introduction
Plants existed before the arrival of the man on this planet and numerous species of these serving as source of nutrition and medicine later became the security for man against starvation and illness. Dependence of man on plants for food dates back to more than 12,000 years (Singh et al. 2013). Plants are most widely accepted source of food and nutrition for majority of the species on this planet, including vertebrates, invertebrates, fungi, bacteria, and even other plants and humans in one way or the other (Singh et al. 2019a, b). In the beginning, the life of man was that of a hunter and food gatherer depending on consumption of whatever grew as wild. Later, he started domesticating useful plant species first by vegetative propagation and then by planting seeds (Rowley-Conwy and Layton 2011) and thus ensuring continuous supply of food and eliminating the problem of food vagaries. With growing dependence on plant-based sources of food and rapid increase in human population, the global demand of plant-based food sources has increased tremendously. This is reflected by the fact that nearly 1400 million ha of land (12% of the earth surface) is under cultivation and 80% of the cultivated land area is under some form of food crops. In spite of this, food production and food security are still the major challenges before the agricultural scientists and researchers (Agrios 2005; Singh et al. 2016a, b, 2019a, b). More than 800 million people across the world lack adequate food and 1.3 billion people live on daily expenses being less than $1. The availability of food to human population in reasonable quantity is largely governed by the population density, cultivated land area available for food production, production of food per unit area and most importantly, losses caused by biotic and abiotic factors, including natural calamities (Gahukar 2011). The worldwide annual yield losses caused by plant diseases and pests are estimated at USD$ 220 billion (Liu et al. 2020). Among these, available land for cultivation is a limited resource and that too is shrinking day by day owing to increased urbanization and developmental activities (Singh et al. 2020a, b). Moreover, increase in production from per unit land area available for food production cannot be proportionate to that in human population principally on account of pest infestation and abiotic stresses, which our
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crops are exposed to. However, researchers continue their efforts to increase the productivity every year (Agrios 2005; Singh et al. 2013) to meet the ever-growing demands for quality food. Apart from biotic stress factors of pest and parasite infestation, there are several abiotic stresses, viz. soil salinity, unfavourable (higher and lower than optimum) temperatures, floods, droughts/frequent dry spells, air pollution, organic contaminants, heavy metals and ultra violet light also take a heavy toll on field crops (Bray et al. 2000), which contribute to reduction in the crop productivity. A number of natural enemies as well as rhizosphere microorganisms have been identified and used against wide range of pests and pathogens to improve plant growth, production and crop productivity directly and/or indirectly (Singh et al. 2013, 2016a, b, 2019a, b). Considering all the aspects of productivity enhancement in food crops, plant-growth-promoting microorganisms (PGPM) are the best examples of harnessing microbial activities for the purpose (Singh et al. 2016a, b). Bio-augmentation of a specific PGPM or consortia of compatible PGPM in a specific niche modulates the microbial community and plays a crucial role in the plant growth (Sarma et al. 2015; Singh et al. 2016a, b). Colonization of the roots by certain PGPMs induces systemic responses against subsequent biotic and abiotic stresses at whole plant level due to a phenomenon called induced systemic resistance (Singh et al. 2016b, 2019a, b) whereby resistance/tolerance (Singh et al. 2016a, 2020a, b) is induced in the plant. These beneficial microbes initiate localized and systemic cellular mechanisms in associated plants against pathogens/stress factors. There is no ambiguity in the fact that plants can use an array of cellular mechanisms to defend themselves from stresses (Dixon et al. 2002; Harman et al. 2004; Shoresh et al. 2010; Harman 2011). Root colonization by T. harzianum, apart from improving root growth and development with improved nutrients uptake and use efficiency, also contributes to increase in the productivity of crop and its resistance to biotic stress factors (Harman et al. 2004; Sarma et al. 2015). Strains of Pseudomonas fluorescens, Trichoderma harzianum, T. viride, T. asperellum and strains of Bacillus spp. are notable examples. Many researchers have reported that the proteome, transcriptome and metabolome of plants alter due to the interaction of metabolites of bacteria secreted into rhizosphere and plant system (Singh et al. 2016a, b; Malviya et al. 2020). Thus, they re-programme the expression of plant genes leading to changes in responses of plants to their environment. For this, the beneficial microbial community in the rhizosphere could be enhanced through the inoculation of microorganisms externally or bio-augmentation of native microbial community by creating favourable micro-environment in the rhizosphere and/or incorporation of organics and nutritional sources externally (Beckman 2000; Sarma et al. 2015). The concept ‘Defence Biome’ gives the holistic overview of recruitment of microbiome, plant-microbe interaction under stressed condition (Interactome) and interactiondependent modulation of physio-biochemical and molecular mechanisms in the plant system such as: (1) stress modulate the exudate profile, which directly affects the microbial community in the specific niche and (2) an increase in the abundance of beneficial microbiota to compete for resources and space using bio-weapons and quorum-sensing quenching of specific molecules (Liu et al. 2020). Moreover, abiotic stresses can increase the community of particular plant-associated microbes via
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(1) change in the physico-biochemical properties of niche (pH, EC, nutritional status, etc.), which favour the specific community, (2) change in the physiology and immunity, which alter the plant secretome profile and favour particular plantassociated microbes, and (3) co-increase in the abundance of beneficial as well as pathogenic microorganisms (Liu et al. 2020).
1.2
Rhizosphere Structure and Function
The plant rhizosphere is the key hot spot for plant-microbe interaction where attraction of microbes during stressed conditions is mediated by diversified root exudates and harbour vast microbial diversity being one of the most complex ecosystems on the Earth (Liu et al. 2020). Rhizosphere harbours complex and diverse community of microbes, including epiphytes, endophytes, saprophytes, pathogens and also plenty of beneficial microbes (Avis et al. 2008; Buchholz and Collins 2013). Plant-growth-promoting rhizosphere microorganisms (PGPM) comprising diverse microbial groups are able to promote plant growth and health directly and/or indirectly. There is preponderance of bacterial genera, viz. Pseudomonas, Bacillus, Alcaligenes, Azotobacter, Mycobacterium, Arthrobacter, Rhizobium, Agrobacterium, Flavobacter, Cellulomonas and Micrococcus in the rhizosphere (Malviya et al. 2020). Plant-associated beneficial microorganisms can have positive effects on seed germination, seedling vigour, nourishment, plant growth and development, disease suppression, and productivity. Plant–microbe interactions play a key part in crucial ecosystem processes, viz. carbon sequestration, soil aggregation and nutrient cycling in the rhizosphere ecosystem (Singh et al. 2004). The rhizosphere microbiome is part of a composite food web that utilizes a large amount of photosynthates released by the plant roots. During the microbial recruitment, roots of plants generate biochemical signals that cause microorganisms, mostly zoospores of oomycetes, to move towards the root (Gow 1999; Van West et al. 2003). Further, the plant genotype, root exudates, border cells and mucilage are major driving forces. The species of bacterial genera, viz. Bacillus, Azospirillum, Pseudomonas, Streptomyces, Klebsiella, Flavobacterium, Azotobacter, Enterobacter, Alcaligenes, Bradyrhizobium, Mesorhizobium, Rhodococcus, Arthrobacter, Serratia, and Burkholderia, etc. are known to promote growth of plants (Singh et al. 2016a, b, 2019a, b). Moreover, mycorrhizal fungi are also an important component of the rhizosphere ecosystem, which are referred to as mutualistic micro-symbionts. They perform ecosystem services such as nutrient mobilization, enhancement of plant establishment and nutrient uptake, protection of plant from biotic and abiotic stresses and also help maintain structure of the soil (Smith and Read 1997). Root exudate/ secretome comprises water-soluble sugars, amino acids and organic acids along with a small amount of sugar, phosphate esters, hormones, vitamins, phenolics, flavonoids and small peptides (Uren 2000; Bais et al. 2006). The stressors, viz. temperature extremes, deficiency of nutrients and/or pathogenic stresses that influence membrane integrity and improve the efficiency of the exudation process (Ratnayake et al. 1978; Singh et al. 2020d). The rhizosphere microorganisms utilize these compounds leading to improvement in microbial biomass and activity in areas
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surrounding the roots. This is referred to as rhizosphere effect. ATP-binding cassette and the key transporters in the roots. These transporters activate and regulate root exudation, which is an active process and thereby causes phytochemicals translocation into the rhizosphere (Loyola-Vargas et al. 2007; Badri et al. 2008). Flavonoids are low-molecular-weight compounds that can mimic quorum-sensing molecules, thereby influencing the bacterial metabolism (Hassan and Mathesius 2012). In plant rhizosphere, quorum sensing plays vital role in the recruitment of microbial community, establishing root–microbe associations, whether they are beneficial, symbiotic or pathogenic. Thus, the quorum-sensing system controls the fundamental processes of bacterial life such as formation of biofilms and motility (Lowery et al. 2008, 2009) and is expected to influence the quantity and quality of volatile organic compounds. Further, border-like cells from plant root tips and mucilage, which contains arabinogalactan proteins in large amounts, are released into the rhizosphere. These proteins fit in to the hydroxyl proline-rich glycoprotein super family of plant cell wall proteins (Nguema-Ona et al. 2007, 2012, 2013) and play key roles in various interaction processes between rhizospheric microbes and plant roots in the rhizosphere ecosystem (Fig. 1.1).
1.3
Microbe-Mediated Mechanisms of Plant Defence to Biotic Stress
A wide range of biotic and abiotic stimuli continuously challenge plants during development (Genre et al. 2009). Therefore, in their quest for survival, plants have to defend themselves against these stresses. Biotic stresses are induced by fungi, bacteria, viruses, invertebrates and other plants. The effect of pathogenic challenge and its extent naturally depends on the nature of the organism involved. Biotrophic pathogens require a living host for their survival, while necrotrophic or hemibiotrophic pathogens first kill the host cells and then obtain nutrients from attacked host cells (Abramovitch and Martin 2004). Natural openings, viz. stomata, hydathodes, lateral roots, accidental wounds act as portals of entry for the pathogens. Pathogens can also form appressoria and penetration pegs for direct penetration of plant surface (Gudesblat et al. 2009; Melotto et al. 2006). Plant in itself is subjected to stress when it activates its pathogen stress responses and therefore reduction in yield can be attributed to both the disease and plant defence mechanisms (Heil et al. 2000) employed to counter foil the pathogenic attack or at least reduce its impact on the plant as a whole, negotiating productivity. Plant mutants have reduced growth phenotypes or develop disease-like lesions when they show constitutive SA-dependent responses like PR protein biosynthesis (e.g. cpr mutants) (Alvarez 2000) and their fitness in the field is compromised (Heidel et al. 2004). Plants are equipped with a multilayered system to recognize pathogenic invaders and trigger defence responses against colonization (Muthamilarasan and Prasad 2013; Wirthmueller et al. 2013). Responses of plants to different stressors are complex and entail alterations at cellular, physiological and transcriptome levels (Atkinson and Urwin 2012). Plants have arsenals of preformed physical or chemical barriers on
Fig. 1.1 Multi-trophic interactions in the rhizosphere ecosystem define the active rhizosphere effects
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their surface, i.e. leaf hair, wax layers, rigid cell walls, antimicrobial secondary metabolites and others. Induction of endogenous multi-component defence system occurs when plant recognizes pathogens. If the pathogen overcomes physical barriers of the plant, the plant recognizes the pathogen by means of its characteristic chemical signatures, including chitin and flagellin, and then triggers comparatively more specific biochemical defence responses. This defence response operates in different plants with various extents of similarity against a common pathogenic agent. It is operative even in the simple moss where in response to fungal cell wall extract a peroxidase is produced (Lehtonen et al. 2009). The peroxidase prevents the pathogenic growth. Plants are also known to produce an array of toxic defence compounds, which are active against various pathogens. Pathogens suppress plant defence responses and re-programme the host cell responses to pathogen metabolism by producing effector proteins that are delivered into the cells. The effectors produced by pathogens are recognized by the plant eventually leading to activation of plant defence mechanisms controlled by resistance genes (Dodds et al. 2009). A very good example of this can be seen in the case of Botrytis cinerea, which, upon infection in sunflower, shifts the carbohydrate metabolism from hexose production and alters it towards the mannitol pathway, which is required by the pathogen (Dulermo et al. 2009). Rhizosphere microbial populations are affected by plant defences. This happens either through recruitment of beneficial bacteria or suppression of pathogen proliferation. Direct and indirect mechanisms are employed by PGPMs to promote growth of different plants (Harman et al. 2004; Sarma et al. 2015). Processes like atmospheric nitrogen fixation, production of siderophores, solubilization of phosphates, synthesis and release of plant hormones are involved in direct plant growth promotion. Promotion of plant growth indirectly results in control of diseases through reduction in harmful effects of pathogens. Various metabolites, viz. cyanide, antibiotics, antimicrobial peptides, extracellular lytic enzymes, including chitinases, proteases, β-1,3 glucanases, cellulases, laminarinases cause suppression of pathogens (Harman et al. 2004). The plant-growth-promoting bacteria produce 1-aminocyclopropane-1-carboxylate (ACC) deaminase enzyme (Glick et al. 2007) in the rhizosphere. This enzyme is involved in stress signalling and negatively regulates processes that cause elongation of roots. The enzyme ACC deaminase causes hydrolysis of ACC to ammonia and α-ketobutyrate. Plants release ACC into the rhizosphere, which is hydrolysed by the bacterial ACC deaminase, thereby reducing ethylene-mediated repression of root growth. This interface is beneficial for bacteria, as ammonia and α-ketobutyrate are sources of N and C, respectively. Plants release ample amounts of secondary metabolites such as terpenes, flavonoids, glucosinolates, phenylpropanoids, strigolactones (hormones) and antimicrobial peptides into the rhizosphere. Plant-associated bacteria can trim down the activity of pathogenic microorganisms by activating the plant to better defend itself, a phenomenon termed ‘induced systemic resistance’ (ISR) (Shoda 2000; Van Loon 2007). The systemic resistance responses are, depending on the inducing microorganisms, regulated by the plant hormones jasmonic acid, salicylic acid and ethylene, foremost to an oxidative burst, the fabrication of secondary metabolites
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and cell wall reinforcement. Sometimes, the mechanism of ISR elicited by rhizosphere microorganisms overlaps to some degree with that of pathogen-induced systemic acquired resistance (SAR).
1.3.1
Phenolics and Plant Resistance
Phenolic compounds are widespread in plants. These are secondary metabolites and can be defined as a substance, which has an aromatic ring bearing one (phenol) or more (polyphenol) hydroxyl substituent, including functional derivatives (esters, methyl ethers, glycosides, etc.). They arise from the shikimate-phenylpropanoidsflavonoids pathways, producing monomeric and polymeric phenols and polyphenols (Harborne 1989). Phenolic compounds have antibiotic, anti-nutritional or unpalatable properties and, thus, they play a role in plant defence. They are involved in plant-microorganism, plant–animal relationships and act as antioxidants and metal chelators. These compounds act as UV light screens and signalling agents between plant and other organisms in both below and aboveground environments (Wink 1997). Plant phenolics are of two types: preformed (constitutive) phenolics, which are formed during plant development; and induced phenolics, which are synthesized in plant in response to infection, physical injury, or upon exposure to abiotic stresses. Induced phenolics are called phytoalexins (Nicholson and Hammerschmidt 1992; Hammerschmidt 1999, 2003; Harborne 1999; Hammerschmidt et al. 2001; Dixon et al. 2002; Sirvent and Gibson 2002; Winkel Shirley 2002). Pre-existing antifungal phenolics are simple phenols, phenolic acids, flavonols and dihydrochalcones that are common in plants and are responsible for non-host resistance to filamentous fungi. They can be referred to as preformed antibiotics due to the fact that enzymes that are involved in their activation are already present in plant. They are separated from their substrates through compartmentalization and their rapid activation does not require transcription of new gene products (Osbourn 1996). Preformed antifungal phenolics are often tissue specific. The flavones, flavonols and other lipophilic compounds are present in leaf wax at surface of plant and bud exudates or in the epidermal cells in the cytoplasmic fraction. In healthy plants, preformed antifungal phenolics are sequestered in conjugated form, usually with glycosidic attachments in vacuoles or organelles (Wink 1997; Beckman 2000; Nicholson and Hammerschmidt 1992; Morrissey and Osbourn 1999; Katagiri et al. 2002). Biotrophs may avoid the release of preformed antibiotics by minimizing the damage to the host, whereas necrotrophs are likely to cause a substantial release of these compounds. Various flavones and flavanones have been found to be active against Aspergillus sp., Botrytis cinerea and Fusarium oxysporum fungi that infect fruits and vegetables during storage (Weidenbörner et al. 1990).
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1.3.2
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Induced/Systemic Disease Resistance
Unlike animals, plants are unable to move when they encounter outside stimulus; therefore, they require more capabilities to cope with stresses and to adapt to environmental fluctuations. There is a functional continuum between the plant cell wall and the plasma membrane to mediate extracellular signals between these two, and this continuum functions as cell wall integrity sensors (Humphrey et al. 2007; Bouwmeester and Govers 2009; Sahu et al. 2016). After a pathogen overcomes constitutive defence barriers on the host plant, it might be recognized at the plasma membrane of plant cell. Pathogen-associated molecular patterns (PAMP) recognition causes activation of inducible plant defence responses. The PAMP are present in all microorganisms (Thomma et al. 2001; Singh et al. 2019c, 2020d). Signalling cascades are triggered by the PAMP perception systems and the recognition of these cascades activates defence responses in natural plant-pathogen encounters (Nürnberger and Lipka 2005). Broad-spectrum innate immune responses in the plant are activated and these responses may be expressed at the site of pathogen locally or in uninfected tissues of other plant parts. The stomata, hydathodes, lateral roots or accidental wounds act as portals of entry for the pathogen or it may penetrate the host directly by formation of specialized structures called appressoria/penetration peg (Ryan 2000; Gudesblat et al. 2009; Melotto et al. 2006). The ability of the plant to recognize the pathogen is the first line of defence, which is governed by cell surface trans-membrane receptors. Two types of molecules can be recognized by pattern recognition receptors or PRRs. The PRRs are present in plants and animals. In plants, membrane-bound receptor-like kinases (RLKs) or receptor-like proteins (RLPs) constitute PRRs (Boller and Felix 2009). Upon entry of pathogen into plant, the damage-associated molecular patterns (DAMPs) are produced in the plant’s apoplast. The DAMPs, which include cell wall fragments such as oligogalacturonides and cellulose fragments, cutin monomers and peptides such as systemin, defensin and phytosulphokines, are recognized by PRRs (Albert 2013; Nühse 2012; Ryan 2000). The pathogen-associated or microbe-associated molecular patterns (PAMPs/MAMPs) that are conserved microbial structures are also recognized by PRRs. The PAMPs/MAMPs are vital for fitness and physiology of pathogen (Newman et al. 2013; Wirthmueller et al. 2013). The PAMPs/MAMPs comprise peptidoglycan in Gram-positive bacteria, lipopolysaccharides in Gramnegative bacteria, bacterial flagellins, eubacterial elongation factors (EF-Tu) and fungal cell-wall-derived glucans, chitins and proteins. The PAMP/MAMP-triggered immunity (PTI/MTI) response is activated upon perception of PAMP/MAMP and DAMP by the PRRs causing downstream intracellular signalling events. Mitogenactivated protein kinases are activated, reactive oxygen species are produced and transcriptional reprogramming occurs. The net outcome is complex output response of the plant that precludes growth of microbes (Wirthmueller et al. 2013). In response to it, pathogens start a counter defence to overcome PTI by expressing specific elicitors or effector proteins that are referred to as avirulence (Avr) proteins (Grant et al. 2006). To inject effectors directly into the cytoplasm of plant cell, pathogenic bacteria use type III secretion mechanisms to cause suppression of
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PRR-dependent signalling to facilitate acquisition of nutrients and to ensure dispersal of pathogens leading to effector-triggered susceptibility (ETS) (Block et al. 2013; Cui et al. 2013). To counteract the pathogens, plants have co-evolved an effector-triggered immunity (ETI), which is a second layer of defence that operates in the plant cell. In ETI, an effector is recognized, leading to encoding of defence proteins by specific resistance (R) genes. The majority of the R proteins have nucleotide-binding leucine-rich repeat (NB-LRR). The PTI/MTI and ETI can result in programmed death of host cell through local activation of a hypersensitive response (HR), or there can be systemic acquired resistance (SAR) that activates defences in distal, non-infected parts of plants. The result is increased resistance throughout the plant (Thomma et al. 2011). Locally induced defence responses are characterized by a hypersensitive response (HR). The plasma membrane potential and its ion permeability are changed upon detection of the pathogen by host resistance (R) genes. There is an increase in the level of extracellular pH and K+, and influx of calcium and hydrogen ions into the cell. The outward K+ and the inward Ca2+ and H+ ion flux are dependent and trigger HR, causing formation of local lesions. Antimicrobial compounds are present in local lesions. Reactive oxygen species (ROS), produced by the cells undergoing the HR, comprise hydrogen peroxide, superoxide anions and hydroxyl radicals. Various enzymes, including copper amine oxidase (which catalyses the oxidative deamination of polyamines releasing hydrogen peroxide and ammonia), xanthine oxidase, peroxidase, NADPH oxidase, oxalate oxidase, may be involved in generation of ROS. Partly some of these cell changes may be due to lipid peroxidation and lipid damage and probably affect membrane function. There is synthesis of phytoalexin and phenolics and other compounds in cells around the lesion. Pathogenesis-related proteins (PRs) are induced and there is deposition of callose and lignin (Singh et al. 2020a, b). These PR proteins comprise four families of chitinases, one β-1, 3-glucanases, one proteinase inhibitors, and one specific peroxidase (Singh et al. 2013, 2016a, b, 2019a, b). Chitinases and glucanases act on the fungal cell walls. The formation of lignin is catalysed by peroxidase resulting in the strengthening of the plant cell wall (Lamb and Dixon 1997; Sticher et al. 1997; Van Loon 1997; Maleck and Lawton 1998; Mauch-Mani and Metraux 1998; Durrant and Dong 2004). Plants possess stressresponsive signalling mechanisms, which are mediated by hormonal regulations (Fig. 1.2). Phytohormones like salicylic acid are involved in both biotic (Vlot et al. 2008, 2009; Dempsey et al. 2011) and abiotic stress adaptation (Kunihiro et al. 2011; Liu et al. 2012; Drzewiecka et al. 2012). The signal transduction pathways in plants are regulated by salicylic acid, jasmonic acid, and ethylene phytohormones. The regulation of these pathways does not take place in an isolated manner (Fig. 1.2). There is a complex regulatory network connecting different pathways to help or antagonize the others so as to ensure the defence response to pathogens. Salicylic acid is responsible for activation of defence response against biotrophic pathogens. Jasmonic acid and ethylene play a role in defence against necrotrophic pathogens. There is mutual antagonism between ethylene/jasmonic acid and salicylic acid pathways (Thomma et al. 2011; Kunkel and Brooks 2002; Turner et al. 2002; Rojo et al. 2003; Glazebrook 2005; Lorenzo
Microbial Interactions in the Rhizosphere Contributing Crop Resilience to. . .
Fig. 1.2 Cross-talk and interactions between the jasmonic-acid-dependent and salicylic-acid-dependent pathways in the plants under biotic stress conditions
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and Solano 2005; Van Loon et al. 2006). Plants produce ethylene to regulate defence to pathogens (Chen et al. 2009). Fusarium graminearum infection in wheat causes production of mycotoxins. To defend itself from the fungus, the wheat produces ethylene, which stimulates the spread of the mycotoxin around the plant, causing death of the host. Reduction in the level of ethylene production reduces the spread of disease. Till date, only a few models have been studied to decipher plant defence responses. Therefore, we do not know what the true capacity of plants to protect themselves against pathogens. Through random sequencing approaches of microbial populations from seawater samples, it became clear that our knowledge of gene functions existing in nature is very limited (Venter et al. 2004).
1.4
Microbe-Mediated Mechanisms of Plant Defence to Abiotic Stresses
Environmental stress refers to adverse effects on plant growth and development. At the ecosystem level, any external constraint that limits productivity below the genetic potential of the plants may be considered as stress. Stress can be defined as a set of physical and chemical factors of the environment that are unfavourable for growth of an organism (Tripathi et al. 2008; Singh et al. 2020a, b). Abiotic stress is the negative impact of non-living factors on the plants in a specific environment. On the basis of nature of source, abiotic stress may be of different types such as radiation (visible, ultraviolet) salinity (salt/NaCl concentration), high temperature (heat shock), low temperature (cold shock), water deficit (drought, desiccation), excess water (flooding, anoxia), chemical stressors (pesticides, pollutants), heavy metals, etc. (Doyon et al. 2010; Rhodius et al. 2012; Meena et al. 2017; Jiang et al. 2017).
1.4.1
Generation of Reactive Oxygen Species and Their Effects Under Abiotic Stress
When oxygen comes in contact with metabolic systems having unpaired electron, it transforms into more reactive and toxic forms, commonly referred to as reactive oxygen species (ROSs). All ROSs are tremendously harmful to plants at higher concentrations (Meena et al. 2017; Jiang et al. 2017). When the level of ROS exceeds, the defence mechanisms are activated and a cell is said to be in a state of ‘oxidative stress’. Low concentration of ROS acts as messengers in various phytohormone responses that include closure of stomata, gravitropism of root, germination of seed, biosynthesis of lignin, programmed cell death, hypersensitive responses and osmotic stress (AbdElgawad et al. 2016; Sun et al. 2018). Higher concentration of ROS is responsible for the oxidative stress and is deleterious for the lipid, protein, and DNA synthesis and function. ROS show the harmful effects at lipid level, such as chain breakage, which increases the membrane fluidity and permeability. However, at protein level, ROS affect in various ways such as site-specific amino acid modification, fragmentation of the peptide chains, and aggregation of cross-linked
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reaction products, altered electric charge, and enzyme inactivation, which increase the susceptibility of proteins to proteolysis (Yamaguchi and Blumwald 2005; Bais et al. 2006; Liu et al. 2006; Young et al. 2013; Mahmood et al. 2016; Bokhari et al. 2019; Wang et al. 2020). The consequence of higher accumulation of ROS also affects the deoxyribose oxidation, strand breakage, removal of nucleotides, modification of bases, DNA-protein cross-links (Zimmermann et al. 2010; Zhang et al. 2018).
1.4.2
Site of Synthesis of ROS
Chloroplast: PSI: electron transport chain, Fd, 2Fe-2S, and 4Fe-4S cluster, PSII: electron transport chain, QA and QB, and chlorophyll pigment. Mitochondria: Complex I: NADH dehydrogenase segment, Complex II: reverse electron flow to complex I, Complex III: ubiquinone-cytochrome region, and Enzyme:aconitase,1-galactono-y lactone dehydrogenase. Peroxisome: Enzyme: xanthin oxidase, membrane: electron transport chain flavoprotein, NADH and Cyt b, metabolic processes: glycolate oxidase, fatty acid oxidation, flavinoxidases. Plasma membrane: Electron-transporting oxido-reductases, and NADPH oxidase, quinone oxidase. Endoplasmic reticulum: NADPH-dependent electron transport involving CytP450. Cell-wall: Cell-wall-associated peroxidase and diamine oxidases. Apoplast: Oxalate oxidase and amine oxidase.
1.4.3
Type of ROS Synthesized During Abiotic Stresses
Activation of O2 may arise by two different mechanisms: (1) absorption of sufficient energy to reverse the spin-on-one of the unpaired electrons and (2) stepwise monovalent reduction. The ROS may be divided into four major categories: Superoxide radical (O2˙ˉ): It reacts with double bond-containing compounds, viz. iron-sulphur (Fe-S) clusters of proteins; reacts with nitric oxide (NO) to form peroxynitrite (ONOOˉ). Hydroxyl radical (OH˙): It is extremely reactive with protein, lipids, DNA, and other macromolecules. Hydrogen peroxide (H2O2): It oxidizes proteins; reacts with O2˙ˉ in an Fe-catalysed reaction to form OH˙. Singlet oxygen (1O2): It directly oxidizes protein and poly unsaturated fatty acids.
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Mechanisms to Scavenge ROS During Abiotic Stresses
1. Presence of systems in cells, which react with reactive forms of oxygen and keep them at low level, i.e. superoxide dismutase (SOD), catalase, permease, total peroxidase, proline, etc. 2. Presence of systems that regenerate oxidized antioxidants, i.e. glutathione reductase (GR), ascorbate (ASA), glutathione (GSH), mono and dihydroascorbate reductase, etc.
1.4.5
Mechanisms of Plant Defence
Plants possess biochemical defence mechanisms, which reduce damage from ill effects of biotic/abiotic stressors (Singh et al. 2019a, 2019b, 2020a, b, c). This mechanism involves the induction of both de novo biosynthesis and rapid accumulation of secondary metabolites, referred to as antioxidants. They have several alternative mechanisms in the form of defence genes. These genes are consistently present in plants, irrespective of whether they are resistant or susceptible to those stresses. Signal transduction in plants in the direction of activating defence genes is mainly accomplished by several inducers in the plant system (Zong et al. 2009; Zhu 2002, Zhu et al. 2003; Zahra et al. 2018). They have no direct inhibitory effect against these stresses. The cascade of events that occurs in response to abiotic stress consists of (1) it should be mobilizing a network of signal transduction pathways and inducing the expression of sets of downstream genes and (2) It should be synthesizing specific proteins, and accumulating compatible metabolites such as specific sugars and proline (Fig. 1.2). The secondary messengers (ABA, ROS, Ca2 + , inositol phosphates) can alter the levels of intracellular Ca2+, calcium binding proteins (Colcombet and Hirt 2008). The phytohormone ABA is considered to play a crucial role in the regulation of cellular responses to abiotic stresses (Danquah et al. 2014). They initiate a protein phosphorylation cascade after interacting with analogous interacting partners. Transcriptome analyses using microarrays and proteomic studies have given insight into plant signal transduction and gene regulation. Gene chip and cDNA microarrays along with massive whole-genome sequencing have enabled identification of new signalling determinants on a whole-genome scale in response to different various stressors (Popescu et al. 2009). Proteomics approach is handy in investigating post-translational modifications of the proteins. It can be used to clone unique genes using differential analysis that will speed up our understanding of stress-signalling mechanisms in plants (Shinozaki and Yamaguchi-Shinozaki 2007). Further, SNAREs are small, abundant, sometimes tail-anchored proteins, which are often post-translationally inserted into membranes via a C-terminal transmembrane domain. These proteins were originally identified as membrane attached receptors for soluble NSF attachment proteins or SNAPs where NSF is an NEM-sensitive factor. Plant SNAREs provide crucial physiological responses such as abiotic stress, gravitropism, pathogen defence and developmental processes such as autophagy, cytokinesis, morphogenesis idioblast (Lipka et al. 2007). A cDNA
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screen in Xenopus laevis oocytes led to the recognition of a tobacco syntaxin, NtSYR1, which interferes with ABA-triggered potassium and chloride ion fluxes in both Xenopous oocytes and Nicotiana tabacum guard cell protoplasts. NtSYR1 appears to interact with a tobacco homolog of the Qb + Qc-SNARE, AtSNAP33 and it plays important role in abiotic stress responses (Geelen et al. 2002). In abiotic stress tolerance, trehalose is one of the important elicitors in plant defence mechanisms and induces WRKY6 and other genes, which activate the several defence cascades in a cooperative manner (Fig. 1.3). It has been shown that trehalose scavenge ROS under abiotic stresses in a concentration-dependent manner and protect plants from ill-effects of abiotic stresses (Fernandez et al. 2010; Lunn et al. 2014; Shi et al. 2019).
1.4.6
MAPK Signalling
Plant mitogen-activated protein kinases (MAPK) receive signals from receptors or sensors and phosphorylate downstream MAPK kinases, which subsequently activate MAPKs that control the activities and synthesis of transcription factors (TFs), enzymes, hormones, peptides and antimicrobial chemicals (Zhu et al. 2019; Xu et al. 2020). The fungi and plants have histidine kinase transduction systems. These sensors are incorporated into more complex pathways. MAPKs are activated by ROS. This activation is important for mediation of cellular responses. This preliminary increase in ROS may be further enhanced by various stresses and production centres. Transient increases in ROS may start signal transduction cascades that involve cross-talk with jasmonates (JAs), salicylic acid (SA), ethylene (ET), abscisic acid (ABA), polyamines and nitric oxide (NO) (de Zelicourt et al. 2016). It can amplify the subsequent cascade through transducer sensors and targets of ROS-dependent and cell-death-related gene expression. There is also cross-talk with the plant-pathogen signal transduction pathway, which might rely on detection of pathogen by the gene-for-gene mechanism and can lead to an opposite effect on the regulation of production of ROS and ROS-scavenging mechanisms, and on the activation of programmed cell death (Smékalová et al. 2014). Besides MAPKobsessed phosphorylation cascades, other regulatory post-translational modifications, such as protein oxidation and nitrosylation, might be involved in ROS-dependent cell death pathways (Thomma et al. 2001; Colcombet and Hirt 2008).
1.5
Endophytes in Biotic and Abiotic Stress Management
In last few decades, there has been a huge development in the endophyte research with respect to the plant growth and health promotion (Compant et al. 2005; Sahu et al. 2017a, 2018, 2019a, b, 2020a, b; Singh et al. 2020a). Endophytic microbes are plant dwellers, which do not cause any harm to their hosts (Schulz and Boyle 2006; Backman and Sikora 2008). History indicates tremendous potential of endophytic
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Fig. 1.3 An overview of microbe-mediated modulation of physio-biochemical mechanisms of abiotic stress tolerance in plants. CW represents cell wall, PM plasma membrane, POx peroxidase, OOx oxalate oxidase, AOx Ascorbate oxidase, SOD superoxide dismutase, CAT catalase, APx ascorbate peroxidase, HR hypersensitive response, IAA Indole acetic acid, MAPK Mitogenactivated protein kinase, CWR crown root. Overall figure depicts how the plant recruits microbiome under stressed condition and how the microbiome serves as the first line of defence and maintains ion homeostasis and plants growth and development under stress conditions
microbes for novel secondary metabolites and other bioactive compounds. In recent past, endophytes were explored for production of growth hormones, antimicrobial compounds, stress-alleviating compounds, organic and inorganic acids for nutrient solubilization, etc. which, in turn, help plants in nutrient uptake, growth promotion (Sahu et al. 2017b, 2018), nutrient fortification (Singh et al. 2018), biotic (Ting et al.
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2010; Thomma et al. 2001; Sahu et al. 2020a) and abiotic stress tolerance (Meena et al. 2017; Singh et al. 2020b). New dimensions have been realized in biocontrol of fungal pathogens using endophytes (Sahu et al. 2020b). Endophytes have advantage of being close to plant cells to influence and protect plants against pathogens (Compant et al. 2005; Kloepper and Ryu 2006; Bakker et al. 2013). It is not evident that all endophytes provide protection against pathogens, but report indicates strongly that the endophytes are having huge potential to be used as excellent biocontrol agents (Table 1.1) as they endorse disease tolerance against wide array of plant pathogens (Berg 2009). Induced systemic resistance (ISR) (Feng et al. 2013; Sahu et al. 2019a, b, 2020a), production of antifungal compounds - iturin, surfactin, fengycin (Wang and Liang 2014; Sahu et al. 2020b), proteases, chitinases, siderophore production, competition for nutrients, volatile organic compounds (Sahu and Brahmaprakash 2018), etc. are few of the major mechanisms of pathogen suppression by endophytes (Nimnoi et al. 2010; Sahu et al. 2017b). After Wei et al. (1991) reported ISR for first time by bacteria Pseudomonas fluorescens strain G8-4 against anthracnose disease of cucumber, massive efforts have been poured to harness it for suppressing plant pathogens using endophytes (Sahu et al. 2019a, a). ISR against plant pathogens involves interaction of plants with microbial-associated molecular patterns (MAMPs) present in beneficial microbes. There are reports of ISR by endophytes against several pathogens like cauliflower mosaic virus (CMV; Murphy et al. 2003), Sclerotium rolfsii (Sahu et al. 2019a), Fusarium oxysporum (Chen et al. 1995; Constantin et al. 2019), Rhizoctonia solani (Sahu et al. 2020a), Agrobacterium tumifaciens (Asghari et al. 2020), etc. Five fungal endophytes were studied for compatibility with the host (oil palm) and suppressive ability to Ganoderma in endophyte-calli and endophyte-ramet tests. Antagonists were found to produce volatile, non-volatile compounds and competition against Ganoderma boninense (Cheong et al. 2017). Endophyte BTF08 (Penicillium citrinum) was found to enhance calli weight (1013 mg) by promoting its growth. In vitro screening of endophytes from poplar and willow plants has shown the efficiency of endophytes in growth promotion, abiotic stress mitigation and suppression of pathogen. These endophytes were found to have antagonism against Gaeumannomyces graminis, Rhizoctonia solani, Pythium ultimum and Fusarium culmorum apart from having different plant growth-promotion activities (Kandel et al. 2017). Study of antibiotic marker labelled endophytic bacterium Bacillus subtilis DZSY21 from Eucommia ulmoides indicated its effective colonization in maize plant and suppression of southern corn leaf blight (Bipolaris maydis). Production of antimicrobial compounds surfactin A, surfactin B and fengycin by the endophyte was detected by MALDI-TOF-MS analysis. Up-regulation of PDF1.2 and pathogenesis-related genes PR1 and LOX is found as a result of ISR (Ding et al. 2017). Apart from direct biocontrol activity, endophytes also improve plant yield under biotic stress by producing plant growth promoting substances like indole acetic acid, indole pyruvic acid, isopentenyl adenine, gibberellic acid, isopentenyl adenosine,
Pythium aphanidermatum Ralstonia solanacearum
B. pumilus strain SE34 and Serratia marcescens strain 90-166 Streptomyces griseorubiginosus Endophytic actinomycetes Endophytic actinomycetes Actinoplanes, Micromonospora, Streptomyces Endophytic actinomycetes Streptomyces sp. Bacillus amyloliquefaciens BZ6-1
ISR
Siderophore production
ISR
β-1,3, β-1,4 and β-1,6-glucanases, phytohormones production
Production of antibiotics (NRPS and PKS genes) Surfactin and fengycin
Siderophores and protease
Siderophore production
–
Tomato
Cucumber
Aquilariacrassna
Pythium aphanidermatum
Tomato
Banana
Banana
Tomato
Tomato
Cucumber
Host Cucumber
Arabidopsis thaliana Cucumber
Erwinia carotovora
Ralstonia solanacearum
Fusarium oxysporum f. sp. cubense
BBTV
Fusarium oxysporum f.sp. lycopersici and Verticillium alboatrum CMV
Erwinia tracheiphila
Bacillus subtilis
Chitinases
ISR
ISR
Pathogen Anthracnose pathogen
Endophyte Pseudomonas fluorescens strain G8-4 Bacillus pumilus strain INR7 Streptomyces plicatus
Mechanism of action ISR
Table 1.1 Major mode of actions of endophytic biocontrol agents
Nimnoi et al. (2010) Zhao et al. (2011) Wang and Liang (2014)
Cao et al. (2005) Tan et al. (2006) Conn et al. (2008) El-Tarabily et al. (2009).
Reference Wei et al. (1991) Zehnder et al. (2001) Abd-Allah (2001) Murphy et al. (2003) Zhang et al. (2004)
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Antibiosis, ISR, siderophores, ammonia, HCN Induction of stilbenic phytoalexin; upregulation of PR1, PR2, and PR4 gene expression
Antibiosis, ISR, siderophores, ammonia, HCN
Pseudomonas sp. Sn48 and Pantoea sp. Sa14
Bacillus sp. 1PR7a, Bacillus sp. 2P2; Bacillus sp. 2PR9b Bacillus altitudinis GTS-16 Agrobacterium tumefaciens
Rhizoctonia solani
Sclerotium rolfsii
Fusarium oxysporum
Fusarium endophyte Fo47
Grapevine
Rice
Tomato
Tomato
Maize
Bacillus subtilis DZSY21
Surfactin A, surfactin B and fengycin production; up-regulation of PDF1.2 and pathogenesis-related genes ISR, antibiosis
Maize
Poplar and willow plants
Penicillium citrinum BTF08 Endophytes
Volatile, non-volatile compounds and competition Growth promotion, abiotic stress mitigation and suppression of pathogen
Bipolaris maydis
Pepper
Gaeumannomyces graminis, Rhizoctonia solani, Pythium ultimum, and Fusarium culmorum Bipolaris maydis
Bacillus subtilis DZSY21
Surfactin A, surfactin B, fengycin and ISR
Ralstonia solanacearum
–
Oil palm
Bacillus subtilis
2,3-Butanediol
Plant pathogens
Ganoderma boninense
Endophytes
VOCs
Sahu et al. (2020a) Asghari et al. (2020)
Constantin et al. (2019) Sahu et al. (2019a)
Ding et al. (2017)
Chung et al. (2016) Yi et al. (2016) Ding et al. (2017) Cheong et al. (2017) Kandel et al. (2017)
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ammonia, etc. (El-Tarabily et al. 2009; Nimnoi et al. 2010) enhance nutrient uptake (Malinowski et al. 2000), anti-herbivory substances (Sullivan et al. 2007) and augment sulphur nutrition (Aziz et al. 2016). With all these effects, endophytes provide protection against several plant pathogens, which can be harnessed for sustainable yield enhancement. Abiotic stress alleviation by endophytes is also well documented (Yu et al. 2019). Production of stress-reducing compounds by the endophytes is reported as a mechanism for mitigating abiotic stress in plants (Zhu 2002; Schulz et al. 2002). Increased nutrient assimilation, plant growth, and decreased toxicity to sodium ions by inoculation of Phoma glomerata and Penicillium sp. were reported under salt and drought stress (Waqas et al. 2012). Production of ACC-deaminase enzyme is one of the key mechanisms in reducing the harmful effects of stress (Yue et al. 2019). Change in the expression of stress-responsive genes is another strategy of endophytes that provides protection against abiotic stresses (Meena et al. 2017; Bilal et al. 2020). Govindasamy et al. (2020) reported upregulation of drought-responsive genes sbP5CS2 and sbP5CS1 in the plants treated with bacterial endophytes Ochrobactrum sp., Microbacterium sp., and Enterobacter sp. against the control and Escherichia coli-inoculated plants. Down regulation of heavy metal ATPase gene expression (GmHMA13, GmHMA14 and GmHMA18) and upregulation of drought-responsive genes (such as GmDREB2) in the Glycine max L. inoculated with fungal endophytes Paecilomyces formosus LHL10 and Penicillium funiculosum LHL06 reduced the accumulation of heavy metals in the plants (Bilal et al. 2020).
1.6
The ‘Holobiome’: Significance of Microbes in Host Development and Behaviour
In recent past, a series of studies have unveiled that an individual is actually an arrangement of ‘biomolecular networks’ consisting of visible hosts plus millions of invisible microbes. These microorganisms have a significant effect not only on the host development and its behaviour but also on its susceptibility to the diseases and possibly determine its social interactions with surrounding environment (Suárez 2020). As a whole, the individual behaves as a ‘holobiome’, which is made up of ‘own genome’ and associated ‘microbiome’ (Kim and Lee 2020). A lot more applied values of this concept are being investigated in clinical microbiology to cure diseases. With respect to the plants, Leach et al. (2017) have described it as phytobiome consisting of plants, the organisms associated and the environment. Next-generation sequencing, metagenomics, metatranscriptomics, metabolomics, metaproteomics, etc. have made the complex analysis possible to decipher the impacts of microbiome on the plant system. The importance of the phenomenon could be understood from the fact that microbiome has been proposed as a platform for the next green revolution (Čatská et al. 1997; Rodriguez and Durán 2020). The microbiota and the plants have been co-evolved for maintaining the balance under different biotic and abiotic stresses. Thus, the investigative studies on ‘holobiome’
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could provide novel insights for plant growth and health promotion in the lieu of second green revolution.
1.7
Rhizosphere Engineering for Stress Management
Improving tolerance towards biotic and abiotic stresses by crop plants remains an issue that can be solved with molecular tools and techniques. However, in general, different mechanisms have been evolved by the plant to cope with environmental stresses (Zhu 2002; Dixit et al. 2015). Plants respond to stresses by accumulation of compatible osmolytes, metabolites and macro-molecules at cellular level. Now a days, focus has been given to explore the feasibility of molecular biology tools and techniques for plant as well as microbes engineering to increase the tolerance against abiotic and biotic stresses with the enhancement in productivity. Genetic engineering gives base to transfer one or more genes involved in regulation and pathways signalling that encodes for the functional and structural defence compounds (osmolytes and antioxidants). Different techniques, viz. differential display PCR, suppression subtractive hybridization, serial analysis of gene expression, DNA microarray and cDNA-amplified fragment length polymorphism, have been described to identify the genes expressed during different biotic and abiotic stresses in the plants. Genetically modified stress-tolerant crops, developed by bioengineering of stress signalling pathways, are the major goal for agricultural research. Transgenic plant of Arabidopsis thaliana was developed as an osmotolerant by introduction of proBA genes derived from Bacillus subtilis that produced higher level of free proline and increased the tolerance against osmotic stress (Chen et al. 2007). Further, designing of the rhizosphere and plant-associated microorganism for a specific plant species is an approach to achieve better crop growth and productivity under stressed conditions (Blount et al. 2012). Advancement in tools for the genetic manipulation like genetic engineering, genome sequencing, metabolic engineering and synthetic biology helps in design of microbes as per requirement of desirable traits (Lovley 2012).
1.8
Application of Nano-Bio-Technology
Annual agricultural crop losses through plant diseases are caused by various groups of microorganisms, including fungi, bacteria, viruses and nematodes that result in yield reduction, and poor product quality and shelf life. To meet food demand by global population and changing climate, the need to enhance agricultural productivity with simultaneous reduction in use of inorganic chemicals for plant stress management is being underlined. For long-term strategy, novel platforms for crop disease management are critically needed. However, considering the possible alternatives, studies on effects of nano-particles on management of plant pathogens have indicated better prospects in this regard. After application of bio-fabricated silver nanoparticles, significant reduction in Bipolaris sorokiniana infection was
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recorded in wheat plants. Bio-fabricated silver nano-particles at 2, 4 and 10 μg ml 1 concentrations exhibited complete conidial germination inhibition, but in the absence of bio-fabricated silver nano-particles conidial germination was 100%. Histochemical studies revealed lignin deposition in vascular bundles induced after bsAgNPs treatment (Mishra et al. 2014). Nanoparticle TiO2 with Zn 500 to 800 ppm (μg ml 1 or μg g 1) formulation exhibited significant reduction in the survival of Xanthomonas sp. strain Xr-1 causing bacterial leaf spot on Rosa ‘Noare’. In non-coated or non-illuminated controls, there was no reduction of bacterial viability. Light-activated nano-particle TiO2 with Zn activity was a better option for management of rose diseases (Paret et al. 2013). The MgO and ZnO nano-particles had an antifungal activity and were evaluated for Alternaria alternata, Fusarium oxysporum, Rhizopus stolonifer and Mucor plumbeus. From this study, it was revealed that nano-particles of MgO and ZnO at highest concentration (0.5 ml) caused maximum inhibition in the spore germination of Mucor plumbeus, Alternaria alternata, Fusarium oxysporum and Rhizopus stolonifer followed by 0.3, 0.2 and 0.1 ml concentrations of nano-particles, whereas least reduction in spore germination was found in untreated control (Wani and Shah 2012). Silver nano-particles had shown antifungal activities at various concentrations. The disease incidence of powdery mildew on cucumber and pumpkin was 53.4, 34.4, 25 and 20% when treated with 10, 30, 50 and 100 ppm silver nano-particles, respectively. The highest inhibition rate of powdery mildew was observed at 100 ppm silver nano-particles. It was suggested that silver nano-particles were more effective for microorganisms, which show less sensitivity to antibiotics due to poor penetration of some antibiotics. Silver nano-particles may disrupt the ion efflux transport systems, which can cause rapid accumulation of silver ions that leads to interruption of cellular processes. For example, they produce reactive oxygen species leading to dysfunction of cells, including damage to proteins, nucleic acids and lipids. This study revealed that when silver nano-particles were applied 3–4 weeks before disease incidence, even 50 ppm concentration of silver nanoparticles was able to inhibit powdery mildew effectively and in vivo tests showed significant inhibition of the growth of fungal hyphae and conidial germination (Lamsal et al. 2011). Jo et al. (2009), upon evaluation, reported that the application of silver nano-particles in vivo at a 500-ppm concentration significantly reduced the pathogenicity as well as colony formation of Bipolaris sorokiniana and Magnaporthe grisea in the plants. Treatment of Artemisia absinthium-mediated AgNP with concentration of 1.56 μg ml 1 significantly showed zoospore encystment, less spore germination and reduced the germ tube elongation of Phytophthora parasitica as compared to untreated control. The silver nano-particle effectively reduced swimming of zoospores of Phytophthora parasitica. Thus, the silver nano-particle with higher concentration effectively managed the disease of tobacco plants caused by Phytophthora parasitica. The 2.5 ppm (μg ml 1 or μg g 1) of silver nano-particles incubated with Fusarium culmorum spores had significantly reduced the germinating spores and sprout length compared to control (FC spores in a sterile
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water solution), as germinating process is very important for Fusarium culmorum pathogenesis process in crops (Kasprowicz et al. 2010).
1.9
Conclusion
Rhizosphere has been defined more than 100 years ago and since then a number of studies have established its role in affecting plant health and its productivity. The diverse microbial community of plant rhizosphere known as rhizosphere microbiome extends the functional scope beyond imagination as indicated by studies across the world. Developments in metagenomics provide detailed pictures of rhizosphere microbiomes. Root exudates of specific plant recruit specific group of rhizosphere microorganisms from main reservoir present in soil. A range of direct and indirect interactions such as plant–plant, microbe–microbe, and plant–microbe occur in the rhizosphere. Rhizosphere is dynamic in nature and is very much influenced by its components. Root and soil are complex microbial habitats harbouring diverse microbial consortia. Understanding, predicting and controlling the structure and function of the rhizosphere will allow us to harness plant-microbe interactions and its activities to increase or restore plant ecosystem productivity, improve plant responses to a wide range of environmental alterations in the function and mitigate effects of climate change by designing ecosystems. A number of strategies have been described to alleviate stress-induced adverse effects on plant growth. Rhizosphere engineering is the process in which manipulation of rhizosphere microorganisms is done for obtaining desired trait(s). This is basically done by the alteration in root exudation pattern of plant, which can be achieved through genetic manipulation in the host plant and by natural induction through interventions in soil. The present chapter helps in understanding of various approaches to manipulate rhizosphere for system sustainability and chemical-free crop production. Efficacy of microorganisms significantly varies with crop and soil. Even reports suggest that agro-ecological zone may also have had significant impacts in the efficacy of microorganisms and this also needs to be considered while going for rhizosphere engineering.
1.10
Future Prospects
The synergistic and complementary mechanisms among microorganisms and of plant-microbe interactions can be deciphered using model plants grown under gnotobiotic conditions. Such investigations may advance our understanding of the phenomenon involved in microbiome-mediated host plant immunity. There is direct influence of microbial interactions on plants and the host plants are able to affect microbiome assembly and thus, the selection of a host-microbial association is an emerging approach to improve plant fitness and productivity. Genetic improvement of plants, relying on an efficient interaction with beneficial microorganisms and selection of agricultural practices with less adverse effects on microbiome, needs to
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be worked out. Number of omic approaches can be helpful in understanding plant microbes’ interaction for specific traits and their exploitation. Therefore, scope of rhizosphere engineering for improved crop performance in future is increasing. Target-oriented rhizosphere engineering is need of the hour. Numbers of laboratories are focusing to find out rhizosphere microbes’ interactions with crop plants and impact of these on crop production and surrounding environment. Protocols may be developed targeting the selection of a characteristic host phenotype influenced by the microbiome function, which can then facilitate the transfer of specific traitassociated microbiome into new plant hosts. Root exudates of plants attract rhizosphere microorganisms the quality of both being interdependent on each other to varying extents. The qualitative and quantitative alteration in the root exudates composition is a major approach to remould the rhizosphere microbiome. The creation of a biased rhizosphere may be novel approach that will involve the expression of specific genes in transgenic plants to enable roots to produce the specific nutritional compound that can then be used/recognized by specific beneficial microorganisms. Acknowledgements We would like to express our special thanks to Dr. Ruchita Dixit and Wasiullah for technical assistance in collecting literatures. The authors wish to thanks Dr. Anil K. Saxena, Director, ICAR-NBAIM, Kushmaur, Maunath Bhanjan, India, for providing technical support during preparation of manuscript. Our special thanks go to Application of Microorganisms in Agriculture and Allied Sectors (AMAAS), ICAR-NBAIM, Kushmaur and Indian Council of Agricultural Research, Government of India, for providing financial support to Udai B. Singh to carry out the research work. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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esculentum mill.) against root knot disease caused by Meloidogyne incognita ?. Appl Soil Ecol 63:45–56 Singh UB, Malviya D, Khan W, Singh S, Karthikeyan N, Imran M, Rai JP, Sarma BK, Manna MC, Chaurasia R, Sharma AK, Paul D and Oh J-W (2018) Earthworm grazed-Trichoderma harzianum biofortified spent mushroom substrates modulate accumulation of natural antioxidants and bio-fortification of mineralnutrients in tomato. Front Plant Sci 9:1017 Singh UB, Malviya D, Singh S, Imran M, Pathak N, Alam M, Rai JP, Singh RK, Sarma BK, Sharma PK, Sharma AK (2016a) Compatible salt-tolerant rhizosphere microbe-mediated induction of phenylpropanoid cascade and induced systemic responses against Bipolaris sorokiniana (Sacc.) shoemaker causing spot blotch disease in wheat (Triticum aestivum L.). Appl Soil Ecol 108:300–306 Singh UB, Malviya D, Singh S, Pradhan JK, Singh BP, Roy M, Imram M, Pathak N, Baisyal BM, Rai JP, Sarma BK (2016b) Bio-protective microbial agents from rhizosphere eco-systems triggering plant defense responses provide protection against sheath blight disease in rice (Oryza sativa L.). Microbiol Res 192:300–312 Singh UB, Malviya D, Singh S, Kumar M, Sahu PK, Singh HV, Kumar S, Roy M, Imran M, Rai JP, Sharma AK (2019a) Trichoderma harzianum-and methyl jasmonate-induced resistance to Bipolaris sorokiniana through enhanced phenylpropanoid activities in bread wheat (Triticum aestivum L.). Front Microbiol 10:1697 Singh UB, Singh S, Khan W, Malviya D, Sahu PK, Chaurasia R, Sharma SK, Saxena AK (2019b) Drechslerella dactyloides and Dactylaria brochopaga mediated induction of defense related mediator molecules in tomato plants pre-challenged with Meloidogyne incognita. Indian Phytopathol 72:309–320 Singh UB, Singh S, Malviya D, Karthikeyan N, Imran M, Chaurasia R, Alam M, Singh P, Sarma BK, Rai JP, Damodaran T (2019c) Integration of anti-penetrant tricyclazole, signaling molecule salicylic acid and root associated Pseudomonas fluorescens enhances suppression of Bipolaris sorokiniana in bread wheat (Triticum aestivum L.). J Plant Pathol 101:943–954. Singh UB, Singh S, Malviya D, Chaurasia R, Sahu PK, Sharma SK, Saxena AK (2020a) Drechslerella dactyloides and Dactylaria brochopaga mediated structural defense in tomato plants pre-challenged with Meloidogyne incognita. Biol Control 143:104202 Singh S, Singh UB, Trivedi M, Sahu PK, Paul S, Paul D, Saxena AK (2020b) Seed biopriming with salt-tolerant endophytic Pseudomonas geniculata-modulated biochemical responses provide ecological fitness in maize (Zea mays L.) grown in saline sodic soil. Int J Env Res Pub He 17:253. Singh S, Singh UB, Malviya D, Paul S, Sahu PK, Trivedi M, Paul D, Saxena AK (2020c) Seed biopriming with microbial inoculant triggers local and systemic defense responses against Rhizoctonia solani causing banded leaf and sheath blight in maize (Zea mays L.). Int J Env Res Pub He 17:1396 Singh DP, Singh V, Shukla R, Sahu P, Prabha R, Gupta A, Sarma BK, Gupta VK (2020d) Stagedependent concomitant microbial fortification improves soil nutrient status, plant growth, antioxidative defense system and gene expression in rice. Microbiol Res 126538 Sirvent T, Gibson D (2002) Induction of hypericins and hyperforin in Hypericum perforatum L. in response to biotic and chemical elicitors. Physiol Mol Plant Pathol 60:311–320 Smékalová V, Doskočilová A, Komis G, Šamaj J (2014) Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol Adv 32:2–11 Smith SE, Read DJ (1997) Mycorrhizal Symbiosis (Second Edition). Academic Press. pp 605 Sticher L, Mauch-Mani B, Metraux JP (1997) Systemic acquired resistance. Annu Rev Phytopathol 35:235–270 Suárez J (2020) The stability of traits conception of the hologenome: an evolutionary account of holobiont individuality. Hist Phil Life Sci 42:1–27 Sullivan TJ, Rodstrom J, Vandop J, Librizzi J, Graham C, Schardl CL, Bultman TL (2007) Symbiont-mediated changes in Lolium arundinaceum inducible defenses: evidence from
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Wink M (1997) Compartmentation of secondary metabolites and xenobiotics in plant vacuoles. Adv Bot Res 25:141–169 Winkel Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223 Wirthmueller L, Maqbool A, Banfield MJ (2013) On the front line: structural insights into plantpathogen interactions. Nat Rev Microbiol 11:761–776 Xu P et al (2020) Integration of Jasmonic acid and ethylene in to auxin signaling in root development. Front Plant Sci 11:271. https://doi.org/10.3389/fpls.2020.00271 Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620 Yi HS, Ahn YR, Song GC, Ghim SY, Lee S, Lee G, Ryu CM (2016) Impact of a bacterial volatile 2, 3-Butanediol on Bacillus subtilis Rhizosphere robustness. Front Microbiol 7:993 Young LS et al (2013) Endophytic establishment of the soil isolate Burkholderia sp. CC-Al74enhances growth and P-utilization rate in maize (Zea mays L.). Appl Soil Ecol 66:40–47 Yu X, Zhang W, Lang D, Zhang X, Cui G, Zhang X (2019) Interactions between endophytes and plants: beneficial effect of endophytes to ameliorate biotic and abiotic stresses in plants. J Plant Boil 62:1–13 Yue Z, Shen Y, Chen Y, Liang A, Chu C, Chen C, Sun Z (2019) Microbiological insights into the stress-alleviating property of an endophytic Bacillus altitudinis WR10 in wheat under low-phosphorus and high-salinity stresses. Microorganisms 7:508 Zahra N, Mahmood S, Raza ZA (2018) Salinity stress on various physiological and biochemical attributes of two distinct maize (Zea mays L.) genotypes. J Plant Nutr 41:1368–1380 Zehnder GW, Murphy JF, Sikora EJ, Kloepper JW (2001) Application of rhizobacteria for induced resistance. Eur J Plant Pathol 107:39–50 de Zelicourt A, Colcombet J, Hirt H (2016) The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21:677–685 Zhang S, Reddy MS, Kloepper JW (2004) Tobacco growth enhancement and blue mold disease protection by rhizobacteria: relationship between plant growth promotion and systemic disease protection by PGPR strain 90–166. Plant Soil 262:277–288 Zhang H et al (2018) The role of promoter-associated histone acetylation of Haem Oxygenase-1 (HO-1) and Giberellic Acid-Stimulated Like-1 (GSL-1) genes in heat-induced lateral root primordium inhibition in maize. Front Plant Sci 9:1520 Zhao K, Penttinen P, Guan T, Xiao J, Chen Q, Xu J, Lindström K, Zhang L, Zhang X, Strobel GA (2011) The diversity and anti-microbial activity of endophytic actinomycetes isolated from medicinal plants in Panxi plateau, China. Curr Microbiol 62:182–190 Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273 Zhu JK et al. (2003) ICE1, a regulator of cold induced transcriptome and freezing tolerance in plants. US Patent App. 10(425):913 Zhu Q et al (2019) A MAPK cascade downstream of IDA–HAE/HSL2 ligand–receptor pair in lateral root emergence. Nat Plants 5:414–423 Zimmermann R, Sakai H, Hochholdinger F (2010) The gibberellic acid stimulated-like gene family in maize and its role in lateral root development. Plant Physiol 152:356–365 Zong XJ et al (2009) Abscisic acid and hydrogen peroxide induce a novel maize group C MAP kinase gene, ZmMPK7, which is responsible for the removal of reactive oxygen species. Planta 229:485–495
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Rhizosphere Microbes for Sustainable Maintenance of Plant Health and Soil Fertility Madhurankhi Goswami, Chandana Malakar, and Suresh Deka
Abstract
Widespread use of fertilizers in the agricultural system has created a continuous pressure on the environment and thus seeks for an immediate response. Biological alternatives are the most feasible and eco-friendly approach for environment, agriculture and for the entire mankind. Plant growth promoting rhizobacteria (PGPR), a group of rhizosphere-colonizing bacteria, is considered to be the most effective candidate for plant health and soil fertility. Moreover, implementation of PGPR for sustainable agriculture can also help in reducing environmental pollution as a result of agricultural run-off, which ultimately causes groundwater contamination. This chapter will focus explicitly on the role and potency of the rhizosphere microbes in growth promotion of plants while reflecting their efficiency in enhancing soil health and soil microbial diversity.
M. Goswami Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India Life Sciences Division, Department of Molecular Biology and Biotechnology, Cotton University, Guwahati, Assam, India C. Malakar Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India Department of Biotechnology, Gauhati University, Guwahati, Assam, India S. Deka (*) Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India # Springer Nature Singapore Pte Ltd. 2020 S. K. Sharma et al. (eds.), Rhizosphere Microbes, Microorganisms for Sustainability 23, https://doi.org/10.1007/978-981-15-9154-9_2
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Keywords
PGPR · Soil health · Soil fertility · Plant growth · Sustainable agriculture
2.1
Introduction
Meeting the global demand for food to feed the growing human population with limited resources is a major challenge. Conventional agriculture plays a crucial role in meeting the growing demand for food and making the country self-independent in food production, but at the same time it is forcing the agricultural system to completely depend on chemical fertilizers and pesticides (Santos et al. 2012). Undoubtedly, on the one hand, these chemical fertilizers in agriculture have made the country selfindependent in food production (Mahanty et al. 2017), but on the other hand, it is imposing several life-threatening impacts on health and environment, such as development of resistance in phytopathogens and pests, deterioration in soil health and quality, decrease in crop productivity over the years (Avis et al. 2008). For instance, initial application of nitrogen fertilizers to the agricultural crop plants increases the nitrogen availability in plants, while indiscriminate use of these fertilizers reduces the rate of biological nitrogen fixation in soil over the years (Vejan et al. 2016). Reports indicate that long-term usage of chemical fertilizers can cause series of changes in physical, chemical and biological properties of soil. Moreover, it influences important soil properties such as soil structure, density, pH and soil water-holding capacity (Divya and Belagali 2012). To overcome the ill effects of chemical fertilizers, efforts have been channelized more towards the production of biological-based fertilizers as potent alternative to agrochemicals. Biological-based fertilizers or bio-fertilizers in the form of plant growth-promoting rhizobacteria (PGPR) can be one of the reliable alternatives for sustainable agriculture. PGPR are root-associated bacteria that augment plant productivity and immunity (Alizadeh and Parsaeimehr 2011). This group of soil bacteria promotes plant growth either by producing phytohormones or by improving bioavailability of soil nutrients like iron and phosphorus, effective mobilization and decomposition of organic matter for easy uptake by plants (Valencia-Cantero et al. 2007). Moreover, PGPR provide food safety and increments soil microbial diversity with no adverse effects on soil ecosystem. The use of biofertilizers will not only uplift agricultural productivity and soil health, but also would lessen the problems of groundwater and soil contamination (Yang et al. 2009). Due to the multifarious traits exhibited by the rhizosphere microbes, there is a growing body of evidence that demonstrates the potentiality and efficiency of these microbes in soil ecosystem.
2.2
Rhizosphere: A Hub for Plant Beneficial Rhizosphere Microbes
The rhizosphere is a part of the soil ecosystem that includes plant roots, soil and the soil microbiota that are in constant interaction with each other. This positive interaction not only benefits the plants, but also improves soil fertility and increases degradation rate of toxic chemicals (Lynch and de Leij 2012). In simpler words, it is
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a densely populated niche in which the roots compete with neighbouring plant roots for space, nutrition and water and also with the soil microbiome (Ryan and Delhaize 2001). The rhizosphere soil is under the supreme influence of the living plant roots, as manifested by exudation or deposition of a wide selection of essential low-weightmolecular compounds affecting the microbial activities occurring within the root rhizosphere (Hirsch et al. 2003). The intensified microbial activity in the rhizosphere is due to the nutritional benefit derived by microorganisms from the rhizodeposition released from the living roots along with the cortical cells and the sloughed epidermal hairs. Additionally, there are other factors that control and facilitate the intense microbial activities occurring at the root surface (Curl and Truelove 2012). The microbial activity at plant rhizospheric region plays a vital role in overall functioning of the plant, while assisting the plants in soil nutrient uptake and providing defence against plant pathogens (Mazzola 2002). Plant rhizosphere serves as a hub for several microbial cells and for variety of nematodes and arthropods. The rhizosphere microbial population exhibits a number of beneficial properties that contribute towards enhanced acquisition of soil nutrients, tolerance to soil stresses, plant defence against soil-borne pathogens and regulation of plant immune system. The majority of them are part of a complex food web that utilizes the maximum nutrients released by the plant. There are several factors that influence or regulate microbial diversity and activity in the rhizosphere of plants (Mendes et al. 2013).
2.3
Factors Influencing Rhizosphere Microbiota
The structure and diversity of the rhizosphere microbiome mainly depend on the plant genotype, developmental stage of the host plant, root exudates secreted by particular plant roots and basically on the surrounding soil (Dey et al. 2012; Chaparro et al. 2014). Each of the plant species promotes a unique group of rhizosphere microbes and with subsequent increase in phylogenetic diversity between the plant’s species, there occurs a huge diversity in the composition of rhizosphere microbial assemblages. Thus, even a same plant species with different genotypes can actively transform the rhizosphere microbial composition. Likewise, a study by Bulgarelli et al. (2015) with barley plant of same species but with different genotypes shows that it accounts for approximately 5.7% of variance in rhizosphere microbial composition. Sugiyama et al. (2012) have similarly reported different rhizosphere microbial composition with variation in five different Arabidopsis genotypes. Moreover, they have observed that microbial communities belonging to the five different genotypes of Arabidopsis thaliana not only vary in their rhizospheric microbial compositions, but also in their metabolic activity. Berg and Smalla (2009) have studied the effect of different plant species on the rhizosphere microbial community and have observed that the rhizosphere microbiome isolated from various crop plants, vary in their phenotypic, genotypic as well as metabolic activity. Moreover, existing studies show that plant species richness and plant functional diversity have a positive impact on the microbial functional diversity,
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microbial species richness and microbial catabolic activity. Decrease in plant biomass, due to a drop in plant species richness and functional diversity, poses a strong effect on the residing microbial communities since microbial diversity and microbial catabolic activity is linearly related to plant species and plant functional diversity (Dey et al. 2012). Studies have shown that the rhizosphere microbiome or rhizosphere microbial communities differ according to the plant developmental gradient (Chaparro et al. 2014). Micallef et al. (2009) have studied Arabidopsis plant rhizosphere throughout its developmental stages. They observed that the rhizosphere microbial communities vary with each developmental stage and the microbial richness and diversity in the early plant development were more distinct in the bulk soil, which ceases with succeeding plant age. Similarly, Xu et al. (2009) and Inceoglu et al. (2011) have studied and analysed the changes in the rhizosphere microbiome of soybean and potato plants, respectively, with each succeeding developmental stage. Xu et al. (2009) observed that the rhizosphere microbiome of soybean plants is strictly influenced by plant development and the density of the microbial communities was found to be complex during the early developmental stage as compared to the later stages. Similarly, Inceoglu et al. (2011) demonstrated that the young potato plants had cultivar dependent rhizosphere microbial communities, but these microbial differences were found to disappear as the plants aged. Numerous studies have shown that root exudates play a crucial role in shaping the rhizosphere microbiome. For instance, Zhou and Wu (2012) showed that the addition of p-coumaric acid to the rhizosphere of cucumber seedlings altered the rhizosphere bacterial and fungal communities and increased the microbial density of soil-borne pathogens of cucumber. In another similar study, Zhou and Wu (2013) observed that addition of vanilic acid completely altered the rhizosphere microbiome of cucumber plants. Similarly, phenolic compounds present in the root exudates also have a strong influence on shaping rhizosphere microbial community (Badri et al. 2013). Recent studies have established a positive correlation between phenolic compounds and the diversity in microbial communities occurring in the rhizosphere soil. With increase in phenolic content in root exudate, there is significant increase in rhizosphere microbial communities. Moreover, the influence of phenolics on rhizosphere microbial communities was found to be more pronounced as compared to other group of compounds that includes sugars, sugar alcohols and amino acids. This reflects its prominence as specific substrate or signalling molecule for deciding the composition of the residing rhizosphere microbial communities (Fang et al. 2013; Michalet et al. 2013). Soil type with the assemblage of its physicochemical parameters determines the structure and diversity of rhizosphere microbial communities. Several studies dealing with soil microbiome report on the effect of soil type on the structure and diversity of rhizosphere microbiome. Some of the studies suggested that soil type or soil texture has a stronger influence on the structure of rhizosphere microbial community than plant species richness and plant functional diversity (Groffman et al. 1996). Chiarini et al. (1998) undertook a study to assess the effect of soil type and cultivar and the growth stage of cultivar on the composition of rhizosphere
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microbial community. During their study, they observed that among all the factors, soil type was the most pronounced factor that affected the microbial density and community structure. In a similar study, da Silva et al. (2003) observed that soil type, rather than plant cultivar type, was the prime determinative factor that influences the rhizosphere community structure. Moreover, soil texture can also modulate or structure the rhizosphere microbiome by limiting the root exudates. For example, some amino acids, peptides remain adsorbed to the sand and clay particles in the soil and remain less accessible to the microorganism than when present in unbound or free state (Buyer et al. 1999; Kuske et al. 2002). Reports show that fine texture of soils like clay soil and soil with an increased pH induces a prominent increase in density of endogenous soil pseudomonads. Presently, studies revealed that of all the factors associated with soil parameters, soil pH is believed to be the most influential factor affecting the rhizosphere microbial communities (Fierer and Jackson 2006). Studies show that a close relationship exists between soil pH and the overall structure and diversity of rhizosphere microbiome. The reason behind this connection is the sensitivity of the bacterial cells towards pH as bacterial cells exhibit a narrow pH growth tolerance (Rousk et al. 2010). Thus, the dominant effect of soil type among all environmental factors can be explained by the impact of soil texture on the rhizosphere microbial communities, which are the primary sources for rhizosphere and rhizoplane colonization (Manoharachary et al. 2006).
2.4
Interaction between Rhizosphere Microbe and Plant via Root Exudates
The interaction between the plant roots and the rhizosphere microbiome is a unique metabolic process by which the plants monitor the changes in the surrounding environment and react to the same. Root exudates are a class of chemical compounds secreted by the living plant roots in response to the chemical signals emitted by the soil microorganisms (Chaparro et al. 2012). The type and composition of the plant root exudates vary between plant species, ecological niches and even within distinct roots of a plant (Rovira 1969; Uren 2000; Micallef et al. 2009). Root exudates are composed of sugars (glucose, arabinose, galactose, fructose, sucrose, xylose, pentose, rhamnose, mannitol), amino acids (all 20 proteinogenic amino acids), organic acids (acetic acid, succinic acid, malic acid, 1-glutamic acid, l-aspartic acid, salicylcic acid, shikimic acid, chorismic acid, tartaric acid, gallic acid, ferulic acid, oxalic acid, citric acid), lignins (catechol, benzoic acid, nicotinic acid, cinnamic acid, ferulic acid, coumaric acid, chlorogenic acid, pyroglutamic acid, quinic acid), flavones (naringenin, kaempferol, naringin, rutin, strigolactone), indole compounds (indole-3-acetic acid, brassitin, sinalexin, brassilexin, methyl indole carboxylate, camalexin glucoside), protein and enzymes (proteins, lectins, proteases, acid phosphatises, proxidases, hydrolases and lipase) and stimulators. Broadly, root exudates have traditionally been grouped into low- and highmolecular-weight compounds. The low-molecular-weight compounds form the
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major part of root exudates and it comprises of amino acids, organic acids, sugars, phenolics and various secondary metabolites. High-molecular weight compounds comprises of mucilage and proteins. The composition and concentration of root exudates vary depending on the surrounding soil, signals received from the environment and the rhizosphere, age of the plant and also on the environmental stress conditions. There are various mechanisms that are involved in extrusion of plant root exudates (for example diffusion, ion channels and vesicle transport), necessary for exporting compounds to the rhizospheric soil (Bertin et al. 2003; Neumann and Romheld 2007). The mechanism for the release or secretion of root exudates into the soil vicinity depends on molecular weight of compounds present in the root exudates. Low-molecular-weight compounds are released from the roots via passive diffusion, while the high-molecular-weight compounds are released via active diffusion into the rhizospheric soil (Badri and Vivanco 2009). At the same time, the secondary metabolites, polysaccharides and proteins are released through membrane-bound proteins (Weston et al. 2012). Root exudates released by the living plant roots behave as chemical attractant for soil microorganisms, regulate the soil microbial communities, cope with herbivores, alter physical and chemical properties of soil, inhibit the growth of competing plant species and initiate symbiotic interactions between plant and rhizosphere microorganisms (Estabrook and Yoder 1998; Bais et al. 2006). Carbohydrates and amino acids present in the root exudates predominantly act as chemo-attractants for a wide range of PGPR isolates. Recent studies have reported that arabinogalactan proteins (AGPs) play a key role in various interactions between rhizosphere microbes and plant roots. There are several studies that report the efficiency of AGPs in rhizospheric interactions attracting beneficial microbes (Cannesan et al. 2012). In one of the recent studies, it was reported that AGPs secreted by Arabidopsis root cells and border-like cells affect the colonization efficiency of Rhizobium sp. which indirectly reflects the potency of AGPs in recognition and attachment of rhizobia to plant root surfaces (Vicre et al. 2005). Apart from AGPs, flavonoids, a key constituent of root exudates of legumes, play a crucial role in initiating root-microbe interactions. Particularly, flavonoids facilitate interaction of roots with rhizosphere microorganisms, stimulation of rhizobial nod gene expression, responsible for the synthesis of Nod factors and chemo-attraction of rhizobia towards the host plant roots (Hassan and Mathesius 2012). Similarly, benzoxazinoids secreted by the maize roots help in attracting plant beneficial rhizobacteria towards the plant root surface for colonization (Neal et al. 2012). Additionally, the plant roots also secrete certain protein compounds as root exudates. Few of the studies have mentioned that proteins like lectins, secreted as a part of root exudates, function as defence and recognition factors in symbiotic interactions (De Hoff et al. 2009). The proteomic analysis of Arabidopsis root by De-la-Pena et al. (2008) has shown that these roots secrete a wide range of defence proteins such as chitinases, glucanases and myrosinases during the flowering time. For instance, Pseudomonas syringae pv. tomato DC3000, pathogen of Arabidopsis plants, induces the secretion of several defence proteins like peroxidases, glycosyl hydrolase family 17, chitinase and glycosyl hydrolase family 18 as root exudates.
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2.5
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Role of Rhizosphere Microbes in Plant Health
Rhizosphere microbes are the primary unit of soil nutrient cycling and deciders of soil status, plant health and richness of soil nutrient pool (Meena et al. 2017), They help in nutrient solubilization, mobilization, mineralization as well as in nutrient dissolving and uptake by plants (Verma et al. 2010; Meena et al. 2014a, b; Yadav et al. 2017). The rhizosphere microbes play a dynamic role in aiding the plants in easy acquisition of N, P or K from rhizosphere soil apart from siderophore production, immune modulation, signal transduction and pathogen control.
2.5.1
Nitrogen Fixation
Soil nitrogen (N2) availability fluctuates greatly in both space and time due to a number of factors like precipitation, temperature, soil type and soil pH. The form in which the available soil N can be easily taken up by the plants depends strictly on plant adaption to soil conditions. For instance, plants growing at low pH and basic soil such as those found in arctic tundra or at mature forests tend to take up ammonium or amino acids, while plants growing at high pH and more acidic soils tend to take up nitrate as nitrogen source (Maathuis 2009). In general, N acquisition by the plant roots depends on the availability of N in the surrounding rhizospheric soil. Mostly, N in soil is present in organic form and suitable transformation of soil N is highly essential for enhancing the level of soil fertility (Jetten 2008). According to the existing literature, the transformation of soil N is basically managed by microbial processes and it is significantly essential for N fixation for better acquisition by plants (Adesemoye et al. 2009). The rhizosphere soil microorganisms fix atmospheric N2 in soil and convert it into organic form making it available for the plants. Moreover, the prevailing rhizosphere conditions favour N2 fixation in soil by heterotrophic bacteria that utilizes organic compounds as the source of electrons for the conversion of atmospheric N2 (Dotaniya and Meena 2015). The process of N fixation is a complex process involving interaction between a number of bacterial and plant gene products. Legumes form symbiotic associations with microbes for the purpose of N fixation. Rhizobial symbioses result from formation of root nodules in the host plants roots. It is a symbiotic association of diazotrophic microbes with roots of leguminous plants involved in the conversion of atmospheric nitrogen into ammonia for easy N acquisition by host plants. Specific substances extruded by the plant roots attract the rhizospheric bacteria towards the plant enabling a plant-rhizobia symbiotic association. As a result of plant-microbe symbiosis, infection process starts at the host root system and following infection flavonoid compounds are released by the host root hairs that induce bacterial nodulation genes, which result in the synthesis of Nod factors, a group of biologically active oligosaccharide signals (Lynch and de Leij 2012). Recent studies have unveiled a wide array of PGPR that includes Azospirillum, Alcaligenes, Arthrobacter, Acinetobacter, Bacillus, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Pseudomonas, Rhizobium and Serratia, actively participating in
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atmospheric N2 fixation. Among all symbiotic associations, the majority of biological nitrogen fixation (BNF) occurring in the rhizosphere of terrestrial ecosystem is performed by the well-known symbiotic bacteria belonging to the family Rhizobiaceae and the leguminous plants (Jones et al. 2007). Similarly, the non-leguminous plants form mutualistic association with nitrogen-fixing bacteria (Lynch and de Leij 2012). About 78% of elemental nitrogen is present in the atmosphere, but it remains unavailable to the plants. Interestingly, there are no plant species that can convert or fix atmospheric nitrogen into nitrogenous compounds for making it utilizable by the plants for its proper growth and development. Thus, the atmospheric nitrogen is made available to the plants by a phenomenon known as biological nitrogen fixation that involves few rhizosphere microorganisms that exhibit the ability to fix nitrogen to ammonia (Gaby and Buckley 2012). In order to achieve enhanced plant growth and development, nitrogen fixation seems to be an important property. Islam et al. (2013) have observed that priming of tomato and pepper plants with nitrogen-fixing bacteria has significantly increased growth parameters in plants that include root and shoot length, seedling vigour and dry biomass. Similarly, Tien et al. (1979) have reported that inoculation of Azospirillum brasilense has considerable effect on plant growth. Seed priming with Azospirillum brasilense resulted in enhanced proliferation of the root hairs as well as the lateral roots and an increase in nutrient-absorbing surfaces. These changes have resulted in increased nutrient absorption and, thereby, plant growth. But there are very scanty reports that have shown an in-depth study revealing the mechanism involved in growth promotion by nitrogen-fixing bacteria. Thus, further study is required to explore the potentialities shown by nitrogen-fixing bacteria in plant growth promotion and increase in crop yield.
2.5.2
Phosphate Solubilization
Phosphate is one of the important macronutrients that promote plant root growth and hastens maturity in plants. It plays a crucial role in every aspect of plant growth and development. Soluble form of P in soil is highly limited due to its fixation as insoluble phosphates (Sharma et al. 2013; Walpola and Yoon 2012; Mehrvarz et al. 2008). Plants take up P mainly in the form of P anions like HPO24 or H2PO4 depending on the pH of the soil. Although soil contains a large quantity of phosphate, both in inorganic and organic form, the maximum portion of soil P remains inactive and unavailable to plants. This unavailable portion of soil P can be made available to the plants by a unique group of rhizosphere bacteria. This group of bacteria is known as phosphorus-solubilizing microorganisms (PSM). PSM hydrolyse the insoluble organic and inorganic soil phosphorus into simpler soluble forms, increasing the bioavailability of soil P. A large number of soil microorganisms, including bacteria, fungi, actinomycetes, algae and arbuscular mycorrhizae, exhibit the potentiality of P solubilization and mineralization ability. For instance, several bacterial strains like Bacillus, Paenibacillus, Rhizobium,
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Serratia, Rhodococcus and many others exhibit potential phosphorus-solubilizing ability. Similarly, fungal strains like Aspergillus, Achrothcium, Alternaria, Cephalosporium, Curvularia, Cunninghamella, Fusarium, Helminthosporium, Phoma, Phythium, Rhizoctonia, Rhizopus, Sclerotium, Torula, Trichoderma and Yarrowia also exhibit the inherent ability to solubilize insoluble organic and inorganic soil P (Alori et al. 2017). According to the existing literature, the principal mechanism of P solubilization is through production of organic acids, siderophores, protons, hydroxyl ions and CO2. The acids produced in the periplasmic space by direct oxidation pathway, along with carboxyl and hydroxyl ions, cause chelation or reduction in soil pH that ultimately results in the release of bound P. Moreover, the drop in pH due to bacterial organic acid produced within the microbial cell and also acidification of the surrounding soil causes the release of P ions by substitution of H+ for Ca2+ (Goldstein 1994). According to the theory proposed by Illmer and Schinner (1995), H+ released as a result of H+ substitution by Ca2+ ions causes P solubilization. Cation assimilation by PSM solubilizes soil P either by lowering the soil pH, chelation or by mineralization (Kalayu 2019). An alternative mechanism for P solubilization is the release of H+ in the outer space in exchange for cation uptake through H+ translocation ATPase or via assimilation of NH4+ within microbial cells. This results in the release of protons that causes the solubilization of P without the production of organic acids (Sharma et al. 2013). There is another mechanism of inorganic P solubilization, which is by inorganic acid production or via production of metal chelators. The efficiency shown by inorganic acids or chelating substances in P solubilization is less efficient as compared to P solubilization efficiency shown by organic acids (Alori et al. 2017). Existing literature reports that soil organic phosphorus constitutes around 30–50% of the total P and is present in the form of inositol phosphate. Organic P in soil is solubilized by the action of a number of enzymes and involves the removal of P by dissolution of Ca-P compounds (Rodriguez and Fraga 1999). Plants cannot directly acquire phosphorus from phytate; however, the presence of PSM in the rhizosphere compensates the plant’s inability to acquire phosphate directly from phytate (Richardson and Simpson 2011). The use of PSB as inoculants simultaneously enhances P uptake by plants and hence stimulates plant growth and crop yield. Recent studies portray the effect of PSB on P uptake by plants as well as its role in plant growth and development. Inoculation of PSB isolates in agricultural lands has a significant impact on plant growth in terms of field emergence, root length, plant height, nodule dry weight, nodule per plant, number of seeds and total yield of seeds over control plants (Singh et al. 2010). There are several pieces of evidence that show the efficiency of PSB on plant growth and crop yield. Hariprasad and Niranjana (2009) observed that treating tomato seeds with PSB improved the overall seed quality parameters under in vitro conditions. Under greenhouse conditions, priming of tomato seedlings with efficient PSB isolates showed enhanced root and shoot length, dry and fresh weight and overall phosphorus content of the primed tomato seedlings in comparison to the control plants. Similarly, Li et al. (2017) have reported that priming of maize seedlings with efficient PSB isolates has a marked effect on root and shoot length,
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root and shoot dry weight, total P and N content of maize seedlings, thereby enhancing plant growth. Similarly, Wu et al. (2019) observed that priming of Camellia oleifera Abel. seedlings with two efficient PSB, namely Bacillus aryabhattai (JX285) and Pseudomonas auricularis (HN038), significantly promoted the growth of Camellia oleifera plants. Simultaneous inoculation of the strains significantly increased the plant height and biomass of C. oleifera plants. Moreover, the study reported the beneficial effect of PSB on the chlorophyll content and photosynthetic capacity of C. oleifera plants. Similarly, Batool and Iqbal (2018) observed that potent PSB strains can be further used as bio-inoculants for promoting growth and yield in plants. They have observed that priming of wheat plants with efficient PSB strains potentially enhanced different growth parameters in wheat plants and significantly increased the P content. However, further in-depth study is required to explore their potentialities as biofertilizer and to study the overall genetic stability of the particular strains.
2.5.3
Potassium Solubilization
Potassium is one of the important nutrients that play a key role in plant growth, metabolism and development. It also boosts up plant resistance against a wide number of diseases, pests and abiotic stresses. Additionally, K helps in stimulating a set of 80 different enzymes responsible for plant processes. Soil contains a large amount of K than any other soil nutrients; however, only 1–2% of it is available, while most of the soil K is unavailable to the plants. The unavailable soil K is made available by some soil microorganisms known as potassium-solubilizing bacteria (KSM). The KSM are effective in releasing K from inorganic and insoluble form of soil K through the process of solubilization. There are evidences that suggest that soil KSB are highly efficient in transforming insoluble form of K into simpler soluble K forms that can be easily acquired by the plants. Moreover, recent studies have reported that KSB can improve plant growth through suppression of plant pathogens and also improve soil structure. For instance, these microorganisms can solubilize silicate to release silicon, aluminium and potassium, while secreting biologically active compounds that enhances plant growth (Meena et al. 2014a, b). KSB in soil includes both aerobic and anaerobic forms, but majority of the soil KSB are aerobic and are mostly reported to inhabit the rhizospheric soil in comparison to non-rhizospheric soil. KSBs are ubiquitous in nature and their number varies from soil to soil. There are a wide array of soil bacteria that can solubilize soil K, which includes Acidothiobacillus ferooxidans, Peenibacillus mucilaginosus, P. glucanolyticus, Arthrobacter spp., Enterobacter hormaechei, Bacillus mucilaginosus, B. edaphicus and B. circulanscans (Meena et al. 2016a, b). Among all, Bacillus mucilaginosus, B. edaphicus and B. circulanscans have been reported as effective K solubilizers (Meena et al. 2015, 2014a, b, 2016a, b). Microbial solubilization of K involves mobilization and solubilization of insoluble and unavailable forms of K through production of various organic acids. These acids result in the acidolysis and complexolysis exchange reactions that leads to the
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conversion of insoluble form into soluble phosphates, thereby increasing the availability of the nutrients to the plants (Zarjani et al. 2013; Parmar and Sindhu 2013; Uroz et al. 2009). KSMs solubilize insoluble K either by lowering the soil pH, enhancing chelation of cations bound to K or by acidolysis of the surrounding area of microorganism. The lowering of soil pH is particularly due to the secretion of a wide range of organic acids that either directly dissolves the insoluble K or chelates both Al and Si associated with K minerals (Romheld and Kirkby 2010). Thus, the release of organic acids results in the acidification of microbial cells and the surrounding environment, which ultimately causes the release of K ions from the mineral K by protonation and acidification (Goldstein 1994). Priming of seeds and seedlings with KSM results in significant enhancement of seed germination, seedling vigour, plant growth and total plant yield. Recent studies reported that the application of KSM under field-level test crops like wheat, maize and forage crops could drastically reduce the usage of chemical fertilizers as KSM could meet plant’s demand for nutrient acquisition (Xie 1998). According to few of the researchers, inoculation of KSM to agricultural crop fields have resulted in root growth enhancement and significant increase in the number of root hairs. Moreover, it has also improved the K-use efficiency in agricultural lands, thereby creating a balance in managing nutrient proportion in soil (Meena et al. 2014a, b; Verma et al. 2010; Basak and Biswas 2010). Basak and Biswas (2010) have reported that priming of rye plants with KSB isolates boosts the growth of rye plants, increased K content of plants and its absorption of N and K from soil. Moreover, Zhang and Kong (2014) reported that inoculation of KSB isolates to tobacco plants promoted the growth of tobacco plants through mineralization of K compounds in soil, which increased the total K content in soil, thereby facilitating plant growth. Sheng and He (2006) have reported that KSB priming of wheat plants not only promoted the growth of wheat plants, but also enhanced K uptake by plants. Increased nutrient uptake by plants has been attributed to production of plant growth regulation at plant root interface that ultimately enhances root development, thereby promoting water and nutrient absorption from soil. However, further research is essential to evaluate the overall genetic makeup of the strains and for recommending the bacterial strains for using as biofertilizers replacing chemical fertilizers.
2.5.4
Iron Chelators or Microbial Siderophore Producers
Iron is the fourth most abundant element in the Earth’s crust and exists in two oxidation states Fe (III) and Fe (II). It is highly essential for plant growth and development as it acts as a cofactor for proteins that are involved in a number of metabolic processes like tricarboxylic acid cycle, electron transport chain, oxidative phosphorylation and photosynthesis. Moreover, it plays a key role in biosynthesis of porphyrins, vitamins, cytochromes, antibiotics, siderophores, toxins, pigments, aromatic compounds and also in microbial biofilm formation (Saha et al. 2016). Iron is present in huge quantities in nature, but it is not easily available in the desired state as it tends to form insoluble complexes in aerobic soils of basic or neutral pH (Ma et al.
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2015). Iron is made available to plants by a particular group of rhizosphere microorganisms via production of certain low-molecular-weight organic compounds known as siderophores. Siderophores are small metal-chelating agents that primarily bind or chelate insoluble ferric iron from soil. They are synthesized by both the bacterial groups under iron-deficient environment in both aerobic and anaerobic conditions. Siderophore first binds tightly with the insoluble Fe3+ ions and this complex move across the cell membrane to get inside the bacterial cell with the help of specific receptor proteins such as FepA [for enterobactin FhuA (for ferrichrome) and FecA (for ferric citrate)] in E. coli (Braun and Braun 2002; Ma et al. 2007) and FpvA and FptA in P. aeruginosa (Clement et al. 2004; Greenwald et al. 2008; Nader et al. 2011; Nader et al. 2007). Recent studies report that the domain conformational changes of each of the receptors lead to the passage of substrate into the cells and the energy required for the same is provided by the Ton B protein complex, which is composed of two other membrane proteins ExbD and ExbB (Saha et al. 2016). The membrane network is markedly different between gram-positive and gram-negative microorganisms. In case of gram-positive bacteria, siderophore-binding proteins, permeases and ATPases are involved in the transport of siderophore iron complexes through the cell membrane. Similarly, in case of gram-negative microorganisms, transport of siderophore-iron complex occurs via involvement of a periplasmic-binding protein, an outer membrane protein and a cytoplasmic membrane protein belonging to ATP-binding cassette transporter (ABC-transporter) (Ahmed and Holmstrom 2014). The ferric ions that remain bound to siderophores move to cytosol, where it gets reduced to ferrous form of ion and finally gets released from the siderophores. Once siderophore releases iron, it gets degraded or recycled by excretion through efflux pump system (Saha et al. 2016). Siderophore-producing plant growth-promoting rhizobacteria play a significant role in providing iron nutrition to the plants, thereby enhancing plant growth (Parmar and Chakraborty 2016). There are several pieces of evidence that justify plant growth enhancement by siderophore-producing microorganisms. Masalha et al. (2000) undertook a research study to explore the activity of rhizospheric microorganisms in Fe uptake by plants for suitable growth and development. For this, the plants were grown in both sterile and non-sterile conditions on loess-derived loam soil. The plants grown under non-sterile conditions showed good growth with higher Fe concentrations in the roots, while the plants grown under sterile conditions showed lesser growth with iron deficiency. They finally concluded that the presence of microorganisms is crucial for plant growth, since they produce microbial siderophores that act as iron sources for plants. Pseudomonas strain GRP3A and PRS9 isolated from the rhizoplane and rhizosphere soil of pea plants were reported for maximum siderophore production, which significantly helped in seed germination, induced plant growth and markedly enhanced shoot and root length and dry weight of maize plants (Sharma and Johri 2003). The same strain GRP3 was found to promote plant growth by influencing the iron acquisition rate in mungbean plants. Plants primed with GRP3 strain also increased peroxidase activity and chlorophyll content in plants (Sharma et al. 2003). Similarly, siderophore produced by an
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endophytic Streptomyces sp. isolated from the roots of a Thai jasmine rice plant induced significant plant growth and enhanced length and biomass of root and shoots (Rungin et al. 2012). At the same time, the siderophore-producing rhizobacteria can induce suppression of a wide range of plant pathogens. The siderophores capture Fe present in the vicinity of the plant roots and thus limit the amount of iron required for the growth of fungal pathogens causing severe diseases in crop plants (Saha et al. 2016). For instance, Pseudomonas fluorescens strain Mst8.2, Mst 7.4 and MS-3y showed maximum disease inhibition in wheat plants. The data obtained during the course of study demonstrated that the mechanism behind the suppression in fungal disease in wheat plants is primarily due to siderophore production by the particular strains (Gull and Hafeez 2012). Few of the common siderophore-producing pseudomonads proposed as potential biocontrol agents against the well-known soil-borne fungal pathogens include P. fluorescens CHAO (Couillerot et al. 2009) and P. putida WCS strain (Weller 2007). With the advent of newer molecular techniques, further research is necessary to understand the beneficial aspect of siderophore-producing rhizobacteria in the field of environmental microbiology.
2.5.5
Production of Plant Growth Regulators and Secondary Metabolites by Rhizosphere Microbes
Existing literature on PGPR reveals its potency in synthesis of a wide range of wellknown plant growth regulators that include auxins, gibberellins, cytokinins, abcisic acid and ethylene. The plant responds to any of the phytohormone present in the rhizosphere whether synthesized naturally by the rhizosphere microorganisms or supplemented externally to the soil. These hormones affect cell enlargement, cell division, root initiation, growth rate, phototropism, geotropisms and apical dominance in plants (Ma et al. 2015; Yadav et al. 2017). Indole-3-acetic acid (IAA) auxin, synthesized by PGPR and plants, differs only in the biosynthetic pathway and is an important phytohormone that significantly increases plant growth, stimulates rapid and long-term responses in plants. Almost 80% of the total rhizosphere microbes are involved in the production of IAA, and use of these microbes in the agricultural field will enhance the endogenous IAA content in plants and thereby leaving a remarkable effect on growth of plants. Auxins produced by the rhizosphere soil bacteria principally affect the plant root system increasing its size, weight, branching number and surface area in contact with soil. Additionally, inoculation of auxin-producing microorganisms stimulates the growth of adventitious roots. IAA is produced by rhizosphere microbes via two different pathways that include L-tryptophan-dependent and L-tryptophan-independent pathways. In many cases, IAA produced by rhizosphere microbes is generally produced via L-tryptophan-dependent pathway utilizing L-tryptophan as the precursor molecule (Jha and Saraf 2015; Goswami et al. 2016). The phytohormone IAA has been directly correlated with the growth promotion of plants (Noel et al. 1996; Tsavkelova et al. 2006). Nain et al. (2012) observed that priming of cowpea plants with Bacillus sp. RM-2 resulted in significant plant growth promotion. Further study suggested that the strain exhibited significant plant
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growth promoting ability and effective involvement of each particular phytohormone in plant growth promotion. Similarly, Mohite (2013) observed that priming of plant seedlings with IAA producing strains has profound effect on plant growth. It enhanced seed germination and induced proliferation of lateral roots and root hairs, shoot and root elongation and chlorophyll content in plants. There are several other reports that discuss the growth-promoting effects of bacterial phytohormone IAA on growth of plants (Khanna and Sharma 2011; Etesami et al. 2015). Similarly, the phytohormones gibberellins influence a number of plant processes like germination of seeds, elongation of stems and also setting of flowers and fruits (Hedden and Phillips 2000). Gibberellins promote root growth and root hair enhancement, while inhibiting floral differentiation in woody angiosperms, regulating vegetative and reproductive bud dormancy and delaying senescence in many organs of plant species (Bottini and Luna 1993; Fulchieri et al. 1993; Reinoso et al. 2002; Tanimoto 1987). This group of growth regulators is not only produced by higher plants and fungi, but it is also produced by 7 bacterial species. There are few reports that suggest that PGPR strains produce gibberellins, but there are only two Bacillus sp. that have been reported to produce gibberellins that include B. pumilus and B. licheniformis (Gutierrez-Manero et al. 2001). The pronounced activity of gibberellins is due to the fact that this group of phytohormones can be translocated from the roots to the aerial parts of the plant (Goswami et al. 2016). A significant enhancement in seed germination parameters has been observed in cereals like sorghum (Raju et al. 1999) and pearl millet (Raj et al. 2003, 2004) on inoculation of gibberellins producing rhizobacteria. This may be due to the fact, increased production of gibberellins triggers the activity of specific enzymes like alphaamylase that stimulates early seed germination by increasing the availability of starch assimilation. Apart from growth promotion, gibberellin-producing rhizosphere microbes are involved in induction of stress tolerance in plants. There are several studies that report the induction of abiotic stress tolerance in plants by gibberellin-producing microorganisms. Gibberellin-producing Pseudomonas putida H-2-3 was reported to induce physiological changes on endogenous hormones, antioxidants and ionic balance in abiotic stress-affected soybean plants to improve stress tolerance in plants. Additionally, H-2-3 primed soybean plants showed higher shoot length, plant fresh weight and chlorophyll content as compared to the control plants (Kang et al. 2014). Among the secondary metabolites, biosurfactants are the most potent candidates in enhancing growth of plants, while inhibiting fungal pathogens. Previous research suggests that biosurfactant-producing plant growth-promoting rhizobacteria enhance plant growth significantly, while suppressing the growth of a wide number of phytopathogenic fungi. Sheng et al. (2008) have reported that inoculation of biosurfactant-producing Bacillus sp. J119 significantly enhanced the growth of tomato plants. Moreover, they observed that priming of plants with a biosurfactant-producing bacterial strain enhances root colonization rate, which ultimately promotes growth of plants. Biosurfactants were also reported to enhance bacterial motility, biofilm formation and root colonization, thereby enhancing plant protection against a wide range of phytopathogens, while facilitating growth
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promotion in plants (Kruijt et al. 2009). But further research is essential for understanding the underlying mechanism behind enhanced plant growth promotion in the presence of biosurfactant.
2.6
Effect of Plant Beneficial Rhizosphere Microbes on Soil Fertility
Civilization has developed and flourished in areas where soils were fertile, enabling the human species to meet food needs and other necessities. The fertility of the soil and its balanced ecology is highly crucial for sustainable agriculture. Agriculture has been a crucial part of human civilization for thousands of years and still continues to be an important part of it. Successful agricultural practices result in high yield and for this purpose soil health plays a crucial role. The soil health is the cumulative property, which corresponds to agricultural production along with maintenance of soil native ecosystem. Soil health is reflected in its capability to add to various agricultural interventions (Kibblewhite et al. 2007). This is highly dependent on various aspects of soil ecosystem, which is mediated by carbon sequestration, nutrient cycle of the soil and various management aspects. Various anthropogenic activities have triggered the depletion of soil health, thereby decreasing soil fertility and crop yield. Changes in global climate also have an adverse effect on land quality that results in increased pollution, salinization and desertification of landmasses. Furthermore, long-term usage of chemical fertilizers and pesticides for increasing food production has led to a sharp decline in soil fertility, soil microbial diversity and significant increase in various levels of pollution. Although there have been various efforts globally to increase soil fertility, more emphasis was given on green revolution. The quest for biological mediators has been hailed as an essential part of the revolution. Green revolution aims to enhance soil fertility and restore soil microbial diversity by remediation of degraded soils followed by soil enrichment. The soil fertility and plant health is inter-dependent, which makes plantation an important aspect to maintain soil fertility. A recent study on rhizosphere has brought attention towards the rhizosphere microbes, which are inevitable part of the rhizosphere ecology. In this regard, the plant root ecosystem can be exploited owing to its diverse array of plant beneficial microbes. The rhizosphere is the most diverse and metabolically active ecosystem that influences soil nutrition cycle (Zhang et al. 2010). In this regard, along with various bioremediation techniques, rhizoremediation has also been adapted, which implicates the involvement of various plant beneficial rhizobacteria to enhance soil fertility. Bio-augmentation of plant rhizosphere with various contaminant-degrading bacteria as well as plant-beneficial rhizobacteria is an important criterion for soil decontamination, nutrient solubilization for easy plant uptake and enhancing soil fertility and soil microbial diversity (Divya and Kumar 2011) (Table 2.1).
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Table 2.1 Importance of plant beneficial rhizospheric bacteria in remediating soil contaminants, uplifting soil fertility and plant health Plant-growth-promoting rhizosphere microbes Pseudomonas putida GR12-2
Pseudomonas fluorescens OKC
Test crop Canola
Chickpea
Rhizobium sp. RH4
Pseudomonas BA-8, Bacillus OSU-142 and Bacillus M-3 Pseudomonas fluorescens Pf5
Strawberry
Pseudomonas fluorescens 6-8 Bacillus megaterium, Arthrobacter chlorophenolicus and Enterobacter sp. Klebsiella variicola
Canola
Enterobacter cloacae
Rice
Highbush blueberry
Wheat
Tobacco
Significance of microbeplant interaction Increased P uptake by plants, root and shoot elongation and a significant increase in root and shoot weight Increases germination (87%), root length (108 mm), shoot length (122.5 mm), dry shoot biomass (0.074 g), dry root biomass (0.075 g) and total dry biomass (0.149 g) in comparison to the control plants Germination (86%), root length (76), shoot length (91.5 mm), dry shoot biomass (0.075 g), dry root biomass (0.070 g) and total dry biomass (0.146 g) in comparison to the control plants Significantly increased total soluble solids, total sugar and reduced sugar Increases leaf area (748 cm2), number of leaves (37), increase in system diameter (0.40 mm), dry shoot weight (13 g), dry root weight (12.7 g) Enhances root length and seedling growth Significantly increases crop yield, total weight and micronutrient content in grains Increases plant dry weight and enhances uptake of both K and N by the plant Increases root length, number of roots, tillers, total chlorophyll content and macronutrients in leaf, dry weight of root and shoot
References Lifshitz et al. (1987)
Yadav et al. (2013)
Pırlak and Kose (2009) De Silva et al. (2000)
Pallai et al. (2012) Kumar et al. (2014) Zhang and Kong (2014) Suprapta et al. (2014)
(continued)
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Table 2.1 (continued) Plant-growth-promoting rhizosphere microbes Azotobacter chrocooccum and Bacillus subtilis Bacillus sp. and Pseudomonas sp. Gluconactobacter sp. and Burkholderia sp. Bacillus cereus YL6
Test crop Wheat
Significance of microbeplant interaction Increases crop productivity
Sesame
Increases seed yield
Rice
Increases plant nutrient uptake and yield parameters
Soybean
Increases available P in rhizosphere soil by 120.16% and plant total P content by 198.60% Increases available P in rhizosphere soil by 62.47% and plant total P content by 6.20% Increases available P in rhizosphere soil by 7.21% and plant total P content by 78.89% Significantly increased root and shoot dry weights of tomato plants. M01 and M04 increases shoot dry weight by 30.5% and 32.6% and root dry weight by 27.1% and 33.1%, respectively Increases shoot dry weight by 26.2% and root dry weight by 25.6% Increase in nitrogen fixation along with decreased soil heavy metal contamination of Cu, Cd and Pb Increase in plant biomass Seed treatment with the isolate MKRh3 demonstrated diminished cadmium toxicity along with extensive plant growth and rooting Enhances biomass and vigour index in B. napus Increased uptake of Cd and Zn from heavy-metalcontaminated agricultural
Wheat
Chinese cabbage
Acinetobacter (M01 and M04)
Tomato
Ochrobactrum (M11)
Bradyrhizobium sp., Pseudomonas sp. and Ochrobactrum cytisi
Lupinus luteus
Pseudomonas aeruginosa MKRh3
Black gram
Bacillus sp. SC2b
Brassica napus Sedum plumbizincicola
References Kumar et al. (2014) Jahan et al. (2013) Stephen et al. (2015) Ku et al. (2018)
Zhang et al. (2017)
Dary et al. (2010)
Ganesan (2008)
Ma et al. (2015)
(continued)
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Table 2.1 (continued) Plant-growth-promoting rhizosphere microbes
Test crop
Cupriavidus taiwanensis TJ208
Mimosa pudica
Pantoea sp.
Brassica napus
Sphingobium chlorophenolicum
–
Stenotrophomonas maltophilia MHF ENV 22
Pennisetum pedicellatum
Ralstonia eutropha, Pseudomonas aeruginosa and Enterobacter cloacae
Brassica juncea
Comamonas sp. strain CNB-1
Alfalfa
Rhizobium meliloti
Alfalfa
Significance of microbeplant interaction soil by S. plumbizincicola when inoculated with SC2b The metal absorption efficiency of the nodulated plant increased by 33, 71, 81% for Cd, Pb and Cu, respectively Significant removal of phenol from the soil and enhanced chromium accumulation in the hairy roots of the test crop in presence of Pantoea sp. Enhanced pentacholorophenol (PCP) in loamy sandy soil and decreased PCP phytotoxicity in plants grown in soil artificially contaminated with PCP 100, 50 and 58% cypermethrin degradation was achieved in the rhizosphere of the host at concentration of 25. 50 and 100 mg/kg within 72, 24 and 192 h Biodegradation of phorate by the plant and bacterial consortium individually was found to be 38 4% and 55 4%, respectively. However in association with both consortia and test crop, the biodegradation of phorate was observed to be 64 5% Complete degradation of 4-chloronitrobenzene (4CNB) in 1–2 days along with elimination of 4CNB phytotoxicity to alfalfa Initial concentration of PAH was decreased to 51.4% when alfalfa inoculated with the bacterium was planted in PAH-contaminated soil
References
Chen et al. (2008)
Ontañon et al. (2014)
Dams et al. (2007)
Dubey and Fulekar (2013)
Rani and Juwarkar (2012)
Liu et al. (2007)
Teng et al. (2011)
(continued)
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Table 2.1 (continued) Plant-growth-promoting rhizosphere microbes Pantoea sp. strains ITSI10 and BTRH79 Pseudomonas sp. strains ITRI15 and ITRH76
Test crop Italian ryegrass Birdsfoot trefoil
Rhodoccocus equi, β-Proteobacterium, Enterobacter sp., Acinetobacter calcoaceticus, Comamonas sp., Pseudomonas alcaligenes Psedumonas putida MTCC Rhizobium DPT
High and low erucic acid rapeseed varieties (HEAR and LEAR, respectively)
Microbacterium sp. F10a
Wheat
2.6.1
Cajanus cajan
Significance of microbeplant interaction Efficient hydrocarbon degradation was achieved when the bacterial isolate was used in combination with the test plants Increased biodegradation of diesel from contaminated soil with no impact on photosynthesis of rapeseed
Seeds sowed in 50 ppm toluene-contaminated soil, treated with mixed suspension of both bacteria was found germinated, which was otherwise not observed in seeds sowed in untreated soil Significant increase in growth of wheat along with efficient phenanthrene and pyrene removal from contaminated soil
References Yousaf et al. (2010)
WojteraKwiczor et al. (2014)
Goel et al. (2012)
Sheng et al. (2009)
Carbon Sequestration
The amount of atmospheric carbon has increased in the last few centuries due to various anthropogenic activities. Mitigating this large pool of atmospheric CO2 by terrestrial carbon sequestration is a thoughtful alternative. Soil is an immense reservoir of carbon. The organic components of soil harbour nearly three times the amount of carbon present in the atmosphere (Gougoulias et al. 2014). Soil organic carbon (SOC) is found in the form of structural litter input such as root, shoot detritus and dissolved organic carbon (DOC) such as rhizodeposits and leaf litter leachate (Sokol and Bradford 2019). The terrestrial carbon cycle is regulated by photosynthesis and respiration, where in the former case the atmospheric carbon is fixed by various autotrophs and in the latter, the fixed carbon is released into the atmosphere by various microbial respiration. The reports provided by Lal (2004) have shown that the depletion of soil quality through various anthropogenic activities has resulted in loss of 42 to 78 gigatons of carbon, which accounts for 50 to 66% of historic carbon loss. This loss has been reflected in poor crop yield, which has affected the nourishment of the inevitably growing human population. Thus, it is very essential to maintain the soil carbon level, as with increase in 1 ton of soil
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carbon, there can be a huge increase in the production of wheat by 20 to 40 kg/ha, maize by 10 to 20 kg/ha and cow-peas by 0.5 to 1 kg/ha (Lal 2004). In this regard, rhizosphere microbes can enable carbon sequestration through utilization of DOC, which would enhance soil health. The soil carbon matter depends on the recently fixed carbon and its utilization via microbes. However, the carbon sequestration is not an easy task as it is highly crucial for the microbes to have access to the carbon that is fixed in the soil ecosystem. In a study, during 25-day incubation experiment with root exudate from label wheat and maize plant, approximately 36% of 13C could be retrieved, of which 18.7% and 20.8% of 13C were obtained in the form of CO2, which was respired by microorganisms (Marx et al. 2007). Vidal et al. (2018), in one of the studies, observed that rhizosphere microbes utilize photosynthesisderived 13C as well as natural soil organic 13C. The atmospheric CO2 concentration at sub-ambient and elevated concentration was shown to imply an impact on the colonization of rhizobacteria Pseudomonas simiae WCS417 in Arabidopsis rhizosphere, which was also observed to have an impact on the plant responses towards the rhizobacteria (Williams et al. 2018). Pinus taeda L., when exposed to an elevated concentration of CO2, resulted in increased rates of root exudation, which, in turn, stimulated the microbial metabolism, accelerating the soil organic matter (SOM) turnover (Phillips et al. 2011). Bacterial species of Gammaproteobacteria and Firmicutes groups were found to be dominant in dissolved organic matter (DOM) decomposition in soil obtained from tropical rain forests (Cleveland et al. 2007). The process of carbon sequestration by rhizosphere microbes is still unclear, but various studies support that the soil carbon matter is strongly under the influence of various rhizosphere microbes as they play the role of main decomposers in the soil. It is feared that if the rhizosphere microbial respiration ceases, it would then take 12 years of primary production to exhaust the existing atmospheric CO2 (Gougoulias et al. 2014). Co-inoculation of bacteria and cyanobacteria in soil potted with rice variety Pusa-1460 increased crop yield and organic carbon matter (Prasanna et al. 2012). Bird et al. (2011) reported that rhizosphere-related priming of SOM decomposition is influenced by activities of gram-positive bacteria.
2.6.2
Nutrient Mineralization
The involvement of rhizosphere microbes in the geo-chemical cycling of nutrients such as carbon, nitrogen, phosphorus, potassium and other micronutrients not only increases the availability of nutrients to plants, but also to the soil microbial population. Their capacity to mineralize various elements helps in uplifting soil fertility, which improves plant health in such ecosystem. The appropriate ratio of various elements required for plant growth and crop yield forms a crucial part of soil nutrients. The fixing of atmospheric carbon and nitrogen in the soil is dependent on plant photosynthesis and rhizosphere microbial activity. The soil nutrient cycles are under tremendous influence of rhizosphere microbes. Rhizosphere priming caused by soil micro-organisms influence various nutrient cycling processes in soil, thereby producing fertility effect in the soil. Quantification of microbial-mediated nutrient
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fluxes in rhizosphere for 80-year-old tree species in a deciduous hardwood forest, Indiana, USA, revealed that microbial N cycle may contribute approximately 18% of total N mineralization (Yin et al. 2014). Soil bacteria belonging to genera Pseudomonas, Enterobacter, Bacillus, and fungi Penicillium, Aspergillus solubilize the total soil P via production of organic acids. It is reported that the activity of alkaline phosphatase and acid phosphatase increases from 102 to 325% and 205 to 455%, respectively, in rhizosphere soil (Dotaniya and Meena 2015). Meena et al. (2017) have reported a significant increase in plant nutrient uptake efficiency when mineral fertilizers were added along with rhizosphere microbes. Drastic changes were observed in bacterial communities in desert soil, when long-term farming was commenced on desert area of Sekem Egypt, which also promoted plants grown in those regions (Köberl et al. 2011). Thus, the undeniable beneficial impact of rhizosphere microbes was observed in various soil ecosystems, which not only affects plant growth, but also improves the soil quality by enhancing nutrient composition along with its influence on various geochemical cycles of nutrients.
2.7
Rhizodeposition-Mediated Enhancement of Soil Fertility
Rhizodeposition, apart from remediation, is one of the other factors that mediate soil nutrient cycle (Shimp et al. 1993; Nguyen 2009). The root exudates become important mediator of C cycle in the rhizosphere microbiome, which, in return, shapes the soil biota surrounding the rhizosphere (Terrazas et al. 2016; Hartmann et al. 2008; Paterson et al. 2007). Rhizodeposition varies in various developmental stages in plants, which can vary from 6% to 21% (Bertin et al. 2003; Rohrbacher and St-Arnaud 2016). Rhizodeposition of root exudates and other functional metabolites acts as a source of soil organic carbon (SOC), which helps to maintain soil carbon sequestration and in maintenance of soil structure (Bronick and Lal 2005). The influence of rhizodeposition not only ends with its effectivity in determining rhizosphere microbial niche, but it also has importance in biogeochemical properties of soil (Lambers et al. 2009; Singh et al. 2007). The root exudates are metabolized by the rhizosphere microbial population, thereby enhancing soil nutrients. Root exudates released by plants are also reported to enhance the microbial behaviour to a great extent. It is reported that C-based root exudates can modify the rhizosphere microbes, thereby inducing their capability to transform heavy metal existing in the rhizosphere region of the plant. This transformation further helps in detoxification of heavy-metal-contaminated soil (Seshadri et al. 2015). Degradation of pyrene in contaminated soil was enhanced from 15% in unplanted soil to 65% when the soil was planted with wheat (Shahsavari et al. 2015). The root exudates directly or indirectly affect the biological activity of the rhizosphere microbes facilitating microbes-associated phytoremediation of soil (Vishwakarma et al. 2017). Moreover, plant roots are reported to secrete certain molecules, whose structures are analogous to PAH, thereby facilitating hydrocarbon degradation (Divya and Kumar 2011). Additionally, various secondary metabolites release as root exudate assists hydrocarbon degradation via cometabolism and in stimulating various genes responsible
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for xenobiotics degradation (Singer 2006; Fletcher and Hegde 1995). Rhizodeposition-mediated remediation of pyrene-lead co-contaminated soil (Li et al. 2016), 2,4-dichlorophenoxyacetic acid (Shaw and Burns 2005), phenanthrene in slender oats (Miya and Firestone 2001) are few of the noteworthy studies wherein the rhizodeposits seem to enhance the degradation capacity of the microbial community in the rhizosphere. Various sites of roots are reported to participate in root exudation of various compounds. The immediate region behind the root tips is generally considered to be active site of exudation (Badri and Vivanco 2009). Pearson and Parkinson (1960) reported the secretion of ninhydrin-positive substances from a region behind the root tips in healthy roots. Hence, exudatemediated rhizoremediation is dependent on the sites of active exudation. Biodegradation of phenanthrene was observed to be 86%, 48% and 36%, respectively, at 0–3 mm, 3–6 mm and 6–9 mm distance from the mat of actively exuding roots of Lolium perenne (Corgié et al. 2003). Rhizodeposition of phenolic root exudate activates the biodegradation of trichloroethylene by rhizosphere bacteria (Adriano et al. 2005). Proper knowledge of plant-microbial interaction could trace possible exploitation of rhizosphere interaction, which can assist elevation of soil fertility. The influence of rhizosphere microbes not only ends in soil enrichment but also involves various decontamination processes that help in cleansing various contaminated sites. This involves rhizoremediation of petroleum-contaminated sites, pesticide-contaminated sites and also decontamination of heavy-metalcontaminated sites (Fig. 2.1).
2.8
Rhizoremediation
The association of plant rhizosphere microbes is crucial for plant health. The various plant growth-promoting traits displayed by the associated microbes play an undeniable role in maintaining plant health as well as soil fertility. The rhizosphere is a connecting link between the plant roots and its surrounding soil, which contains various rhizosphere microbes contributing significantly towards plant health (Badri et al. 2009). However, along with the agricultural benefits obtained from plantmicrobe interaction, it has also been found to be an effective medium for soil remediation, which helps in restoring soil fertility. With more emphasis on green initiatives to remediate contaminated sites, phytoremediation has gained attention globally. Although various techniques of phytoremediation, viz. phytoextraction, phytotransformation, phytovolatilization, rhizoremediation are available, microbeassisted remediation is the most effective form of remediation. Rhizoremediation is an imperative part of phytoremediation. It is the remediation technique that involves exploitation of both plants and associated rhizosphere microbes for various remedial strategies. In this regard, plant beneficial rhizosphere microbes play an important role in uplifting soil quality (Gerhardt et al. 2009). 2–5% of rhizosphere bacteria are plant growth promoters that are known for their vital role as biofertilizers, phytostimulators, biopesticides and bioremediators (Antoun and Kloepper 2001; Bishnoi 2015). This strategy of remediation is one of the most effective and
Rhizosphere Microbes for Sustainable Maintenance of Plant Health and Soil. . .
Fig. 2.1 Impact of plant beneficial rhizospheric bacteria in restoring soil fertility and promoting plant growth
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acceptable forms of bioremediation. Owing to a complex signalling method of the plant, the rhizosphere microbes are attracted, forming their own rhizosphere microbiome. The diverse array of microorganisms present in the vicinity of the rhizosphere influences the impact of rhizoremediation. With its effectivity in decreasing soil contamination, this plant-microbe interaction in rhizosphere niche is highly beneficial to the soil as well as towards plant health. Plant-microbe interaction is mediated by various components released by the roots, known as root exudates, and the local microbial community, which includes various soilinhabitant mutualists and parasite. Moreover, the capability of plant roots to penetrate various layers in soil down the earth makes it easier for rhizosphere microbial communities to reach non-penetrable layers of soil, thereby affecting soil conditions considerably (Kuiper et al. 2004). In the process of nutrient acquisition, both soil microorganisms and plants alter soil properties through various metabolic activities and organic litter deposition, respectively (Jacoby et al. 2017). There are various reports wherein rhizosphere microbes assisting soil phytoremediation of a wide range of hydrocarbons and pesticides has been observed. Vetiveria zizanioides along with one of the rhizosphere-colonizing endosulfan-degrading bacteria showed better remediation of endosulfan-contaminated soil (Singh et al. 2016). Similarly, Gordonia sp. S2RP-17 in association with Zea mays was found to remove TPH significantly, almost by 95.8% from diesel-contaminated soil (Hong et al. 2011). Although plants possess bioremediation capability of various contaminants, they lack the metabolic activity that could result in complete degradation of a contaminant. The rhizosphere-associated microbes enhance the process of mineralization of contaminants, which otherwise could not be completely mineralized by plants alone (Vergani et al. 2017). Thus, agriculture practices and the microbial communities in the plant rhizosphere are one of the important factors in uplifting and restoring soil quality. Among all, hydrocarbon poses the biggest threat to soil quality and fertility and is a major type of land pollutant. Previous literature establishes the potency and efficiency of rhizosphere-colonizing microorganisms in hydrocarbon mineralization. Biological remediation not only helps in decreasing phytotoxicity but also in evapotranspiration of hydrocarbon (Khan et al. 2013). Utilizing the plant beneficial microbes to remediate hydrocarbon contamination is the most efficient cleaning procedure as these microbes are capable of degrading hydrocarbon of varying complexity. The hydrocarbon degradation rates and efficiencies vary from strain to strain within the same species as well as within various species. Various enzymatic pathways enable the rhizobacteria to degrade and assimilate the hydrocarbon. The root exudates that help in recruiting beneficial bacteria also play an important role in enhancing microbe-assisted hydrocarbon degradation. Hou et al. (2015) reported significant removal of high-molecular-weight aliphatic (C21–C34) and PAH by Testuca arundinacea L., when inoculated with plant-growth-promoting rhizobacteria. Positive interaction between the hydrocarbon-degrading microbes and tropical grass Brachiaria brizantha was observed in diesel-contaminated soil with significant degradation of the existing contaminants (Mezzari et al. 2011). There are several studies that report the efficiency of rhizosphere colonizing plant-
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beneficial microbes in hydrocarbon decontamination and mineralization in association with crop plants (Kumar et al. 2013; Tara et al. 2014). Pesticide contamination is another inevitable consequence of using pesticides to get rid of various pests and insects from our crops. These pesticides have now entered into the food web resulting in various levels of toxicity in the consumers. There is now a global effort to eliminate the toxic impact of this anthropogenic practice as a result of which various toxic pesticides in many countries around the world have been banned. However, the pesticides, which were used in the past, still persist in the environment, which can still pose threats to the environment as well as its components. PGPR can be a good candidate in this regard as many of the rhizobacteria are investigated for their ability to survive the toxic impact of various pesticides. Enhanced dissipation of lindane was observed in soil planted with Withania somnifera and inoculated with Staphylococcus cohnii subspecies urealyticus (Abhilash et al. 2011). Streptomyces sp. M7 was reported to degrade 68% of lindane in lindane-contaminated soil along with better seedling vigour index of maize plant seeded in same soil (Benimeli et al. 2008). Degradation of herbicides, namely atrazine, metolachlor and trifluralin, was reported to be enhanced in Kochia sp. rhizospheric soil compared to non-rhizospheric soil, thereby emphasizing the potency of rhizosphere microbes in pesticide removal (Anderson et al. 1994). In reference to pesticide contamination, phytostimulation is one of the significantly reported remediation processes for efficient biodegradation of various grades of a pesticide (Velázquez-Fernández et al. 2012). Pisum sativum plants inoculated with endophyte bacteria were found to degrade 2,4-dichlorophenoxyacetic acid with no accumulation of herbicide in the aerial tissues (Germaine et al. 2006). The plant rhizosphere is a huge collection of various plant beneficial microbes, which, in turn, is a large pool of diverse genes. The adaptation of rhizobacteria in root niche is entirely dependent in its genetic manipulations subjected to various biotic and abiotic factors. Molecular studies have revealed that incessant pressure of hydrocarbon contaminants on rhizosphere soil microbiome alters the gene expression pattern that enables significant degradation of hydrocarbon contaminants. Degradation of alkanes is mediated by a number of enzymes coded by a range of genes such as methane monooxygenases (mmo genes), alkane hydroxylases (alkB genes) and cytochrome P450-type alkane hydroxylases (CYP153 genes) (Afzal et al. 2013) produced by different rhizosphere soil microorganisms. Siciliano et al. (2003) reported the expression of three catabolic genes ndoB, alkB and xylE for hydrocarbon degradation and mineralization of hexadecane and phenanthrene in rhizosphere microbes. Expression of alkane monooxygenase (alkB) and naphthalene dioxygenase IndoB) was reported in endophyte and rhizosphere microbes of petroleum-hydrocarbon-contaminated sites (Siciliano et al. 2001). Afzal et al. (2011) reported that there is a positive correlation between the expression of catabolic genes and hydrocarbon degradation. Catabolic genes alkM, alkB and xyle that mediate degradation of alkanes and aromatic petrochemical compounds were reported to be present in various rhizosphere microbes of wild oat (Rajaei et al. 2013). Other than the genomic DNA, extra-chromosomal genes also play an important role. Plasmids often carry genes that provide various conditional advantages to
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the microbes (Divya and Kumar 2011). Various genes contributing to pesticide degradation are often reported to be present in plasmids of rhizosphere microbes. Plasmid of Pseudomonas diminuta was reported to contain parathion-degrading gene (Serdar et al. 1982). Organophosphate-degrading gene OpdA was obtained from plasmid of Agrobacterium radiobacter P230 (Horne et al. 2002). Similarly, parathion-degrading gene degrading gene was also identified in 43-kb plasmid of a Philippine isolate of Flavobacterium sp. (ATCC 27551) (Mulbry et al. 1986). Moreover, root exudates are reported to induce certain genes of rhizosphere microbes, which enable the microbes to cope with contaminant soil, thereby enhancing degradation rates (Segura et al. 2009). Rainey and Preston (2000) have reported the presence of various genes in bacteria with unknown functions. The unveiling of these genes in plant beneficial bacteria through in vivo expression technologies assists further exploration of PGPR. Certain genes are upregulated only in presence of certain types of stress, resulting in non-expression of them in normal in vitro condition. The overall functioning of the important genes can be studied using promoter trap techniques, differential fluorescence induction and in vivo expression technology (IVET) (Rediers et al. 2005). Omics-based study has shaped a better understanding of the effect of rhizobacteria in the remediation of contaminated soil (Reinhold-Hurek et al. 2015). Various pathways involving the degradation of soil contaminants via enzymatic as well as genetic regulations are previously reported. Metagenomics, metatrancrintomics, metaproteomics and genomics are few of the potential tools that have facilitated in-depth study of the various factors that facilitate the impacts of rhizobacteria on soil decontamination (Kotoky et al. 2018). The aforementioned omics-based studies have enabled identification of various genes involved in the degradation of soil contaminants. Moreover, transgenic studies also play a crucial role in understanding the hydrocarbon degradation mechanisms. Plants with various bacterial genes responsible for degradation of various xenobiotics and hydrocarbon have been investigated for their efficiencies. Sylvestre et al. (2009) reported that three components of biphenyl deoxygenase and 2,3 dihydroxybiphenyl dioxygenase are actively produced by transgenic plants, which were critical for bacterial polychlorinated biphenyl (PCB)-degrading pathway. Transfer of NAH7 plasmid in Pseudomonas putida KT2440 strain enabled efficient expression of Nah catabolic pathway in vitro and in situ, leading to complete mineralization of naphthalene (Fernández et al. 2012). Brazil et al. (1995) reported successful expression of bph gene in sugarbeet using recombinant P. fluorescens F113pcb strain. Mueller and Sachs (2015) reported about microbiome engineering, which can be deployed to enhance plant and animal health. Similar approach can be initiated to strengthen the rhizosphere microbes, which, in turn, can strengthen the plants as well as soil health.
2.9
Conclusion
Constant anthropogenic exploration of soil has depleted the global soil fertility to such an extent that there is an urgent requirement to re-establish the soil health. Loss of carbon as well as other nutrients from the soil due to various agricultural practices
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has resulted in decreased soil fertility. Use of various fertilizers and pesticides to increase crop yield has further worsened the condition of soil. Excessive use of fertilizers without considering the rhizosphere microbes has resulted in alteration of nutrient cycles. With advancement in green biotechnology, the beneficial impact of plant beneficial bacteria has attracted various researchers to explore their potentialities in agricultural sector. The plant-growth-promoting rhizobacteria are reported to be associated with various agricultural as well as ornamental plants. These microbes provide enormous benefits to the plants by making various nutrients available to the plants, providing protection from wide range of phytopathogens and secreting various plant beneficial hormones. The beneficial impacts of rhizosphere microbes are not only limited to the plants, but also are extended towards soil health. Various root exudates released by the living plant roots help in developing the rhizosphere microbial ecology, which further increases carbon sequestration in soil and maintains the nitrogen cycle. This ultimately results in a significant increase in soil nutrients. The rhizosphere microbial niche is a rich pool of various genes with high catabolic efficiencies towards various forms of hydrocarbon as well as pesticides. Molecular approaches to identify such genes and their effect have allowed scientists around the globe to understand the benefits rendered by the rhizosphere microbes. Genetic modification of various plants, wherein insertion of microbial catabolic genes has shown a better tolerance to various contaminants. Advancement in omics study has provided information regarding the rhizosphere ecology, which can be further exploited for re-establishing the soil ecology. The rhizosphere is a complex ecology with constant signalling between roots and the rhizosphere microflora. Thorough study of rhizosphere ecology is required to better understand the mutual relation between the microbes and the plant root to utilize it for the betterment of the environment.
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Dissecting Structure and Function of Plant Rhizomicrobiome: A Genomic Approach Hemant Dasila, Samiksha Joshi, and Manvika Sahgal
Abstract
Rhizomicrobiome is the most diverse and highly dynamic environment primarily influenced by root exudates of the host plant. It is a hotspot region for total microbial activities that imparts a beneficial effect on plants by enhancing nutrient availability and suppressing the growth of invading phytopathogens. Numerous efforts have been undertaken to unmask the total microbial diversity and interactive mechanisms occurring at the rhizosphere. Communication within the rhizosphere microbiome via signalling molecules provides a basic model for interactions, but there is a need to explore important events at the molecular level. Dissecting the rhizomicrobiome environment with classical (culture isolation techniques, biochemical characterization, and 16S rRNA gene sequencing) and modern approaches (metagenomics, metatranscriptomics, proteomics, and metabolomics) in combination with bioinformatic tools (BLAST, KEGG, SwissProt, etc.) has unravelled some of the important aspects of microbial interactions at rhizosphere. The role of molecular and bioinformatics tools becomes very important as they cover microbial responses at every stage, e.g. at DNA, RNA, and protein levels. These classical and modern approaches along with bioinformatics tools are a great attempt to unfold hidden secrets in rhizomicrobiome with respect to plant health. Keywords
Rhizomicrobiome · PGP · Bioinformatics · Classical approach · Modern approach
H. Dasila · S. Joshi · M. Sahgal (*) Department of Microbiology, G.B. Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India # Springer Nature Singapore Pte Ltd. 2020 S. K. Sharma et al. (eds.), Rhizosphere Microbes, Microorganisms for Sustainability 23, https://doi.org/10.1007/978-981-15-9154-9_3
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Introduction
Rhizosphere refers to the volume of soil influenced by roots. It is a highly dynamic and complex environment where biogeochemical cycles of elements are affected by an interaction between microorganisms at the root interface (Peterson 2013). Rhizosphere is associated with numerous microbes. Rhizosphere-associated “microbiome” is known as rhizomicrobiome (Berendsen et al. 2012). It is considered as plants’ second genome because it directly influences plant health and agriculture productivity under normal and stressed conditions (Philippot et al. 2013). Rhizomicrobiome is associated with phytohormone production, nitrogen fixation (Kathiravan et al. 2013), and biocontrol activity against phytopathogen (Yin et al. 2013) under abiotic and biotic stress. Soil rhizomicrobiome composition varied in healthy and diseased plants and also acts as an indicator of the future disease outcome in plants. The initial composition of rhizomicrobiome predetermined whether the plants will succumb or survive disease in the future (Wei et al. 2019). The nature of rhizosphere colonizing bacteria, as either attractant or repellent, depends on the plants’ development stage (Peiffer et al. 2013; Chaparro et al. 2014). The dominant and common inhabitants of the rhizomicrobiome include plant growth-promoting rhizobacteria (PGPR) (Ayyadurai et al. 2007; Sekar and Prabavathy 2014). The soil type and microbial community in the rhizospheric region are influenced by plant root exudation profile (De Angelis et al. 2009). Organic carbon released by the plants results in a significant increase in total microbial activity within rhizomicrobiome. Soil microorganisms are chemotactically dragged towards plant root exudates as they provide them a carbon-rich environment (Jones et al. 2009; Mendes et al. 2013). A recent study of total DNA community analysis provides strong evidence that microbial interaction at the rhizosphere is plant species-specific (Rout and Southworth 2013). The rhizosphere microbiome of wheat, rapeseed, and maize each carries different bacterial communities (Bakker et al. 2013). Even within a bacterial group, certain species, for example, fluorescent Pseudomonas spp. is plant species-specific. Biotic and abiotic stresses, anthropogenic effects and climatic variation are key determinants in plant–microbe association and affect the population dynamics of rhizosphere microbes (Bulgarelli et al. 2012; Lundberg et al. 2012). Rhizomicrobiome provides specific nutrition and protection to the plants from invading phytopathogens by producing enzymes or secondary metabolites ( Philippot et al. 2013; Turner et al. 2013).
3.2
Rhizomicrobiome
Rhizomicrobiome comprises of nutrient-rich environment that serves as a junction for nutrient exchange between soil, plants, and microbes. The density of microbial cells in the rhizosphere is much greater as compared to that of plant cells. The constituent microflora of rhizomicrobiome can affect seed vigour, seed germination, nutrition, productivity, plant growth, and development and in disease occurrence (Mendes et al. 2013). It is dynamic and diverse and comprises micro-organisms at
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different domains, viz., fungi, bacteria, algae, archaea, nematodes, protozoa, viruses, and microarthropods (Buée et al. 2009). Amongst these, domain bacteria is the most dominating followed by fungi, actinomycetes and other groups such as Actinobacteria, Acidobacteria, Bacteroidetes, Verrucomicrobia, and Planctomycetes (Buée et al. 2009; Turner et al. 2013; da Rocha et al. 2013).
3.3
Root Exudate–Rhizomicrobiome Relationship
Root–microbe interaction was first reported in the wheat rhizosphere (Foster and Rovira 1976). Root–microbe interaction includes the exchange of signals that initiate all the physiological and metabolic activities in the rhizosphere. Root–microbe interaction is influenced by both root exudates and microbial components. Plant root exudation pattern governs the structure of rhizomicrobiome (Peter 2011). The density and diversity of rhizospheric bacteria vary significantly from that of bulk soil. There is considerable chemical diversity in root exudates which include monosaccharides (glucose, mannose, and fructose) disaccharides (maltose), amino acids (aspartate, glutamate, asparagines, glutamine, arginine, and cysteine), organic acid (benzoic, ascorbic, and acetic acid), and a few high molecular weight compound, such as enzymes, fatty acids, auxins, gibberellins, nucleotides, tannins, terpenoids, alkaloids, polyacetylenes, and vitamins (Gunina and Kuzyakov 2015; Hayat et al. 2017). Although both C and C4 plants release root exudates during photosynthesis, the pattern varies. In C3 plants, dominant sugars are ribose, maltose, and mannose (Vranova et al. 2013), whereas ribitol and inositol in C4 plants (Nabais et al. 2011).
3.3.1
Signal Exchange Between Rhizomicrobiome and Plant Roots
3.3.1.1 Rhizomicrobiome-Mediated Phytohormone Production Phytohormones are one of the key players in plant growth and development. The phytohormones act as molecular signals in response to environmental stress that otherwise becomes lethal or limits plant growth (Fahad et al. 2015). Important phytohormones are gibberellins, cytokinins, and ethylene. Rhizosphere-colonizing bacteria such as Azotobacter sp., Bacillus subtilis, Pantoea agglomerans, Pseudomonas fluorescens, Paenibacillus polymyxa, Rhizobium sp., and Rhodospirillum rubrum produce gibberellins or cytokinins, whereas Achromobacter, Acinetobacter, Agrobacterium, Alcaligenes, Azospirillum, Bacillus, Burkholderia, Enterobacter, Pseudomonas, Ralstonia, Rhizobium, and Serratia produce ACC deaminase (Kang et al. 2010). The enzyme ACC deaminase regulates the rhizosphere ethylene level. Phytohormone ethylene affects plant growth and development in various ways which include root initiation, promoting fruit ripening, promoting leaf abscission, inhibiting root elongation, stimulating seed germination, promoting lower wilting, and initiating the synthesis of inducible factors that regulate other plant hormones. Lower the ethylene level, more the plant growth. It has been reported that
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co-inoculation of ACC deaminase positive Pseudomonas sp. and R. leguminosarum resulted in improved nodule dry weight, nodule number, grain yield, straw yield, fresh biomass, and nitrogen content in grains of lentil (Iqbal et al. 2012).
3.3.2
Signalling: Microbe to Plant
Rhizomicrobiome comprises bacterial strains that produced secondary metabolites and volatile organic compounds (VOCs). Priming of VOC producing bacterial strains can improve stress tolerance and promotes plant growth development. For example, polyamines play important physiological roles in plants. Polyamine helps in higher biomass production, elevated photosynthetic capacity, and altered root architecture in Arabidopsis (Zhou et al. 2016). Bacillus megaterium strain BOFC15 is reported to secrete a spermidine that in turn induces polyamine production in Arabidopsis.
3.3.3
Signalling: Plants to Rhizomicrobiome
Plants harbour the mutualistic, parasitic, and commensal microorganisms. Legumes are the best-studied examples of signalling from the plant to a microorganism. The exchange of signals between plant and rhizobia gives rise to nodule formation (Oldroyd 2013). Flavonoids (2-phenyl-1,4-benzopyrone derivatives) are the first plant signals exchanged with its rhizobial symbionts which further induced nod genes in rhizobia (Redmond et al. 1986) to secrete lipochitooligosaccharides (LCOs) molecules known as Nod factors. The nod factors are central signalling molecules that initiate the nodulation process in plants (Lerouge et al. 1990). Plant perceives these LCOs signal via its tyrosine kinase receptor present at the root epidermis. Tyrosine kinase initiates signalling cascade which finally leads to nodule development (Limpens et al. 2015).
3.4
Communication in the Rhizomicrobiome
3.4.1
Signal Molecules
Quorum sensing (QS) is the dominant mechanism through which rhizobacteria detect and respond to within the rhizosphere environment (García-Contreras et al. 2015). QS signals belong to different classes of chemical, viz., fatty acids, N-acyl homoserine lactones, and alcohol (Venturi and Keel 2016). A few gram-negative bacteria like Burkholderia spp. and Stenotrophomonas maltophilia reportedly produce diffusible signal factor (DSF) which is chemically cis-2-unsaturated fatty acids (Ryan et al. 2015) whereas rhizosphere-associated proteobacterial strains such as Erwinia, Pseudomonas putida, Pseudomonas chlororaphis, Pseudomonas syringae, Serratia, and Ralstonia produce and respond to the N-acyl homoserine lactone
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(AHL) type of QS signal (Ferluga et al. 2008). However, ascomycetes mostly secrete alcoholic QS signals (Benocci et al. 2017).
3.4.2
Communication Within Rhizomicrobiome: Operational Molecular Machinery
A communication event within the rhizosphere microbiome involves activation and inactivation of genes, induction, and repression of genes to the various signals. Various signals involved in rhizosphere communication include pattern recognition receptors (PRRs), legume-rhizobia system, induced systemic resistance (ISR), ABC (ATP-binding cassette), and multidrug and toxic compounds extrusion (MATE) transporters. Pattern recognition receptors (PRRs) are microbe-specific receptors that recognize different molecular signals. PRRs further bind to microbe-associated molecular patterns (MAMPS). PRRs induce responses in the form of plant elicitors’ peptides when encountered with non-beneficial bacteria (Lee et al. 2018; Ruiz et al. 2018). These responses trigger a signalling cascade that activates certain transcription factors, defense-related genes, reactive oxygen, and nitrogen species (Ipcho et al. 2016). The legume-rhizobia system has been extensively used to uncover molecular determinants for symbiosis (McCormick 2018; Wood and Stinchcombe 2017). In rhizobia, nod transcription factors (NF), i.e. lipochitooligosaccharides (LCOs), are activated via release of flavonoids from legumes. These nod factors are responsible for rhizobial host specificity (Behm et al. 2014). The LCOs activated via rhizobia–legume interaction promote plant growth and health. Jasmonic acid released by plants trigger induced systemic resistance (ISR) to counter pathogenesis (Zamioudis and Pieterse 2012). The connection between transporter proteins and soil phytopathogens has not been extensively studied, but in a few studies, the presence of MATE transporters is detected in rice roots. MATE transporter proteins promote the release of phenolic compounds into the xylem (Baetz and Martinoia 2014). In Arabidopsis (Garcia et al. 2004) out of 129 genes encoding ABC transport proteins, 25 were involved in root secretions. The expression level of these genes in root cells were higher (Badri et al. 2008). Both ABC and MATE transporter proteins are capable of releasing root phytochemicals into the rhizosphere. MATE transporter proteins are also connected with the release of citrate that confers aluminium resistance in plants (Stukkens et al. 2005). Overexpression studies involving genes responsible for the synthesis of SA (salicylic acid) and camalexin (provides disease resistance against nematodes) in Arabidopsis (Youssef et al. 2013) reveal that knockout of the above genes results in low accumulation of camalexin which later results in increased probability of nematode attacks (Iven et al. 2012). PsoR protein from Pseudomonads plays an important role in the regulation of antimicrobial genes that are responsible for biocontrol. PsoR proteins are regarded as a subfamily of LuxR proteins (Gonzalez and Venturi 2013).
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The Direct Role of Rhizomicrobiome in Plant Growth Promotion
Rhizomicrobiome promotes direct plant growth via the production of plant hormones and solubilization of mineral phosphates and essential nutrients. Most of the organic nitrogen and other essential nutrients retained by the PGPRs result in reduced dependence on fertilizers.
3.5.1
Phosphate Solubilization
After nitrogen (N), phosphorus (P) is the second-largest nutrient that is crucial for plant growth and development. It plays a key role in major metabolic pathways such as macromolecular biosynthesis, photosynthesis, respiration, and energy transfer mechanism (Li et al. 2017). This leads to increased demand for phosphate fertilizer. However, the use of phosphate fertilizer is not only expensive but also damaging to soil micro-environment. Phosphorus can cause eutrophication of lakes resulting in reduced soil fertility. To meet the high demand for phosphorus in an eco-friendly way, phosphorus-solubilizing bacteria (PSB) are now becoming a central point of the research. About 95–99% of phosphate present in the soil is insoluble, precipitated, and is in an immobilized form (Ahemad and Kibret 2014). Different rhizosphere-associated microbes such as bacteria and fungi have phosphorus solubilization potential. PSB constitutes 1–50% of the whole microbial component of rhizosphere followed by fungi which constitute only 0.1–0.5% (Satyaprakash et al. 2017). Rhizosphere-associated bacterial genera Arthrobacter, Bacillus, Beijerinckia, Burkholderia, Enterobacter, Erwinia, Pseudomonas, Rhizobium, Rhodococcus, and Serratia are known phosphate solubilizers. Phosphate solubilizing fungi isolated from the rhizosphere of haricot bean, faba bean, cabbage, tomato, and sugarcane belong to genera Aspergillus, Penicillium, and Fusarium. Amongst them, Aspergillus and Penicillium solubilized 728.77 μg mL1 and 514.44 μg mL1 phosphorus, respectively (Elias et al. 2016).
3.5.2
Nitrogen Fixation
Nitrogen-based fertilizers are being widely used to fulfil crop nitrogen requirements (Santi et al. 2013). An alternative environment-friendly approach is crop inoculation with potential biological nitrogen-fixing plant growth-promoting rhizobacteria (Gaby and Buckley 2012). Nitrogen-fixing rhizobacteria include Azoarcus, Acetobacter, Azospirillum, Burkholderia, Azotobacter, Cyanobacteria, Enterobacter, Pseudomonas, and Gluconacetobacter (Bhattacharyya and Jha 2012).
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Potassium Solubilization
Potassium (K) is the third major essential macronutrient for plant growth and development. Soil usually contains a low amount of potassium and most of the potassium present in the soil are found as silicate minerals and insoluble rock (Parmar and Sindhu 2013). Nowadays, potassium deficiency has become a major constraint in crop production. Potassium deficiency symptoms include low yield, poorly developed roots accompanied by slow seed growth rate and small seed size. Several species present in the rhizosphere microbiome have the potential to solubilize potassium rock by the production of organic acid, and it provides an alternative source of potassium for plant uptake (Kumar and Dubey 2012). Bacterial strains Acidothiobacillus ferrooxidans, Bacillus edaphicus, Burkholderia, Paenibacillus sp., Pseudomonas, and Bacillus mucilaginosus (Liu et al. 2012) are responsible for potassium solubilization.
3.5.4
Siderophore Production
Iron is one of the most important micronutrients for almost all organisms of the biosphere. In soil, iron is present as a ferric ion (Fe+3) that is sparingly soluble and not easily assimilated either by plants or bacteria (Ma 2005). Rhizobacterial strains have evolved specialized mechanisms for iron assimilation, i.e., production of low molecular weight iron-chelating compounds referred to as siderophores (Arora et al. 2012). Depending upon functional groups, siderophores are divided into three main families, namely catecholate, hydroxamate, and carboxylate. To date, 500 different types of siderophores are known, out of which 270 have been structurally characterized (Cornelis 2010). The study of radiolabeled ferric siderophores as a sole iron source confirmed that plants can assimilate labelled iron by several rhizobacterial strains, i.e., Aeromonas, Azotobacter, Bacillus, Burkholderia, Pseudomonas, Rhizobium, Serratia, and Streptomyces sp. (Sujatha and Ammani 2013).
3.6
Indirect Plant Growth Promotion
Phytopathogenic microorganisms are a major threat to sustainable agriculture. The phytopathogens deplete soil fertility, disturb soil ecology, damage groundwater quality, and directly influence crop yield. Bacteria constituting rhizomicrobiome contribute to soil fertility and promote plant growth indirectly by suppressing the phytopathogens (Tariq et al. 2014).
3.6.1
Antibiosis
Antibiotic production is one of the most powerful weapons that microorganisms use to eliminate phytopathogens. It is one of the most studied biocontrol mechanisms
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(Shilev 2013). Majority of rhizobacteria produce antibiotics. Pseudomonads have been reported to produce numerous antibiotics, for example, 2,4-diacetylphloroglucinol (DAPG), amphisin, phenazine, oomycin A, pyoluteorin, kanosamine, oligomycin A, pyrrolnitrin, tropolone and cyclic lipo-peptides (Loper and Gross 2007). Bacillus, Streptomyces, and Stenotrophomonas sp. produce antibiotic compounds xanthobaccin and zwittermicin A (Compant et al. 2005). Antibiotic compounds, such as polyketide and lipopeptide, produced by Bacillus amyloliquefaciens seem to elucidate biocontrol activity against soil-borne pathogens (Ongena and Jacques 2008). At times, a few phytopathogens might develop resistance against antibiotics. Thus, it becomes very difficult to implement these rhizobacteria as biocontrol agents in the field. The problem is overcome by the use of microbial strains producing more than one antibiotic (Glick 2012). There are various examples for use of antibiotic-producing strains as biocontrol agents, for example, 2, 4- DAPG (2, 4-diacetylphloroglucinol) positive strain is used in soil treatment for biocontrol of wheat disease caused by fungus Gaeumannomyces graminis var. tritici (de Souza et al. 2003). Bacterization of wheat seeds with P. fluorescens prevents it from phytopathogen attack due to the production of antibiotic, phenazine-1-carboxylic acid (PCA) (Weller 2007). In addition to the antibiotic production, some rhizobacterial strains are also capable of producing a volatile compound, HCN (Hydrogen cyanide) to suppress phytopathogenic invasion, e.g. HCN- mediated biocontrol of tobacco black rot disease was done by Pseudomonas fluorescens CHAO strain (Sacherer et al. 1994). HCN along with DAPG released by Pseudomonas fluorescens LBUM 223 strain promotes the biocontrol of tomato Canker disease caused by Clavibacter michiganensis (Lanteigne et al. 2012).
3.6.2
Lytic Enzymes
Enzymatic activity is another important mechanism adopted by rhizobacterial biocontrol agents. The enzymes involved in biocontrol activity include dehydrogenases, chitinases, lipases, β-glucanase, phosphatases, and proteases (Joshi et al. 2012: Hayat et al. 2012). These enzymes attack pathogens by excreting cell wall hydrolysing enzymes. These enzymes play a very important role in protecting the plant from a biotic stress. The important phytopathogenic fungi that are suppressed through the action of hydrolytic enzymes include Botrytis cinerea, Fusarium oxysporum, Rhizoctonia solani, Phytophthora sp., and Pythium ultimum (Nadeem et al. 2013).
3.6.3
Induced Systemic Resistance (ISR)
ISR is a physiological state of an enhanced defensive property that is elicited in response to specific stimuli and boosts plant innate defenses against biotic factors (Avis et al. 2008). Rhizobacteria play an important role in providing systemic
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resistance to plants against a broad spectrum of phytopathogens. Jasmonic and ethylene signalling within plants is a classic example of induced systemic resistance that elevates the host immune system in response to a vast variety of pathogens (Glick 2012). Bacterial components that can stimulate induced systemic responses in host include flagella, siderophores, homoserine lactone, lipopolysaccharides, DAPG along with volatile compound, 2, 3-butanediol, and acetoin (Doornbos et al. 2012).
3.7
Endophytic Root Microbiome
Endophytes are those microbes (bacteria or fungi) residing inside plant tissues that do not cause negative effects on plant growth (Coombs and Franco 2003). Distribution of endophytes throughout the plant is based on several factors, such as their colonization ability and allocation of plant resources. Based on their plant-inhabiting lifestyle, endophytes are classified into three main categories: (a) Obligate endophytes: derived from seeds and unable to survive in soils (b) Facultative endophytes: widely exist in soil, which can colonize and infect plant in favourable situations, and (c) Passive endophytes: lack colonization ability and can only infect via wounds or cracks on the plant (Fig. 3.1) (Hardoim et al. 2008). Most of the endophytes with plant growth promotion traits belong to a facultative group. Root endophytes often colonize and penetrate the epidermis at sites of lateral root emergence, below the root hair zone and in root cracks (Zakria et al. 2007). Structure and composition of root endosphere microbiome is found to be less diverse as compared Endodermis Endosphere/Endophyte
Root Cracks
Epidermis
Root Hair Rhizosplane Microbiome Phloem Xylem
Rhizosphere Microbiome
Colonization Types Passive
Soil Bacteria
Facultative
Obligate
Fig. 3.1 Bacterial distribution and colonization patterns of endophytes in the plant root
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to rhizosphere or bulk soil microbiomes (Liu et al. 2017) which indicate roots as effective habitat filters, restricting community membership to progressively and more narrowly defined lineages as environments deviate from soil to roots (Bulgarelli et al. 2012). The dominant endophytic bacterial communities in plant roots mainly belong to phyla Proteobacteria followed by Actinobacteria, Firmicutes, and Bacteroidetes. Other bacterial phyla commonly found in the root endosphere, but in fewer fractions, are Armatimonadetes, Cyanobacteria, Chloroflexi, Verrucomicrobia, Nitrospirae, and Planctomycetes (Edwards et al. 2015). Members from Archaea, Acidobacteria, and Gemmatimonadetes are either absent or rarely present in the root endosphere (Sessitsch et al. 2012). The dominance of phyla was plant-specific, whereas the abundance is influenced by soil cultivation history. Proteobacteria, Actinobacteria, Firmicutes, Bacteroidetes, Verrucomicrobia, Planctomycetes, and Chloroflexi were the most abundant phyla associated with grapevine roots (Samad et al. 2017). Correa-Galeote et al. (2018) demonstrated Proteobacteria, Firmicutes, and Bacteroidetes as predominant phyla inside the maize roots. On exploring the rice root microbiome, members from Rhizobiaceae, Bradyrhizobiaceae, Streptomycetaceae, and Comamonadaceae family were found in abundance (Edwards et al. 2015). Fungal endophytic communities in roots are mainly dominated by Polyporales, Russulales, and Agaricales (Sokolski et al. 2007).A few endophytes may form mycorrhiza-like structures. For example, Leptodontidium formed peloton-like structures on roots of Dendrobium nobile, an orchid, and induced positive effect on various plant growth parameters (Hou and Guo 2009). Some common root endophytes are DSEs (dark septate endophytes), hyaline hyphal endophytes, or hyphomycetes endophytes. DSEs occur in roots of Rosmarinus officinalis along with arbuscular mycorrhizal fungi (AMF) and in Pinus halapensis, with ectomycorrhizal fungi (Girlanda et al. 2002). Similarly DSEs occur with AMF in Pedicularis roots (Li and Guan 2007). In a mutualistic association between Heteroconium chaetospira (DSE) and Brassica campestris, endophytic fungi received carbon from the plant and supplied nitrogen to it (Usuki and Narisawa 2007). Aquatic hyphomycetes are commonly found in riparian and coastal ecosystems. For example, multiple species of aquatic hyphomycetes were isolated from roots of riparian plants including grasses (Cupressaceae) and Pteridophytic trees (Sridhar and Bärlocher 1992). Endophytes exert various beneficial effects on plant via plant growth hormones, nitrogen fixation, increased nutrient uptake, and inhibition of phytopathogens. In addition, they provide diverse bioactive secondary metabolites (Santoyo et al. 2016), and therefore are used as bio inoculants. Several factors influence the structure and diversity of the endophytic community. These include plant species and genotype, agricultural practices, environmental conditions, seasonal variation, geographical location, soil type, and host plant nutrient status (Hardoim et al. 2015). Spatiotemporal patterns have been documented in endophyte communities of certain plant species. With the availability of new molecular approaches, such as high throughput sequencing (e.g., 454-pyrosequencing) (Lundberg et al. 2012), microarray multiplex
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technology (Gao and Tao 2012), and nucleic acid-based stable isotope probing (Radajewski et al. 2000), discovering and characterizing the endophyte community structure and dynamics has become a reality. A study of potato root extracts by pyrosequencing showed that five of the 10 most common genera were reported for the first time as potato endophytes (Manter et al. 2010). With the help of SIP-rRNA analysis, the diversity within primary bacterial consumers of plant-derived carbon has been explored, and new endophytic phylotypes have be en identified (Vandenkoornhuyse et al. 2007). Although endophytes have been detected in all plant parts, roots are the first to the recruit them.
3.8
Classical Approach to Study the Microbiome
Classical approach to get insight into microbial community associated with rhizosphere involves isolating and culturing microbes using specific nutrient media and growth conditions depending on the target organisms and host environment. Obtaining a pure culture of an organism is required for detailed studies of its genetics and physiology. Moreover, it will give actual microbial composition and its functional implications on performance of host plant.
3.8.1
Culture-Dependent Methods
These are the methods used for isolation and morphological, physiological, and functional characterization of microbes from an environmental sample.
3.8.1.1 Isolation and Culturing Classically, the microbial community analysis has relied on culturing techniques which include isolation of microbes through enrichment or serial dilution methods followed by spread or pour plating on specific medium and subsequent determination of viable counts (Fig. 3.2). Variety of selective (e.g., the bile salts in MacConkey agar) or non-selective (e.g., nutrient agar or plate count agar, etc.) media are available for maximum recovery of different microbial species. The specific growth media for all the three domains, i.e., archaea (standard growth media, chemically defined medium, and halophilic medium), bacteria (Kings’ B agar, ammonium mineral salt, Antarctic bacterial medium, Jensen N2-free agar, T3 agar, R2 agar, tryptic soya agar, and yeast mannitol agar), and eukarya (fungus) (Czapek Dox agar, Rose Bengal agar, Sabouraud dextrose agar, and potato dextrose agar) have been described (Yadav et al 2008). The culturable approach has revealed a diversity of microorganisms associated with various soil quality parameters, such as organic matter decomposition and disease suppression. Through this approach, analysing large number of highly diverse samples is very time consuming. Considering the ‘great plate count anomaly’ which states that microscopic bacterial counts are considerably higher than the equivalent total viable counts (Torsvik and Ovreas
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Fig. 3.2 Different culturable and unculturable approaches for characterization of microorganisms
2002), it has been estimated that only 1% of the total bacteria can be readily cultivated in vitro. Significant efforts have been made in past years to advance culturing methods for unculturable species which accounts for 99% of the actual bacteria present. Certain bacteria have fastidious growth requirements, for example, N-acetyl muramic acid for Tannerella forsythia; Pyridoxal or L-cysteine for Abiotrophia spp.; and Granulicatella spp. (Vartoukian et al. 2010).Whereas others require specific oxygen concentration, nutrient level, a humic acids, and signalling molecules in growth medium (Stevenson et al. 2004). It has been observed that addition of signalling molecules, for example, cyclic AMP (cAMP), 5-amino-acid peptide, or acyl homoserine lactone, improves the cultivability of unculturable soil bacteria (Janssen 2008). Use of Gellan gum instead of agar resulted in enhanced bacterial growth and 10-fold higher Colony-forming unit (CFU) counts (Kamagata and Tamaki 2005). Furthermore, beneficial bacterial interactions are also found to be useful in in vitro cultivation of unculturable bacteria only when these bacteria are co-cultivated with helper strains (Nichols et al. 2008). When the cell free extract or spent culture supernatant obtained from helper strain was added to culture media growth of species, such as Sphingomonas spp., Psychrobacter spp., Catellibacterium spp., and Symbiobacterium spp. was stimulated (Nichols et al. 2008). Recently a novel strategy, SMART (selective medium design algorithm restricted by two constraints),
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was developed to design selective media using non-natural material and containing two selective agents: a carbon source and an antimicrobial agent. This strategy has been used for designing selective media for culturing Acidovorax avenae, Pectobacterium carotovorum, Burkholderia glumae, Xanthomonas campestris, and Ralstonia solanacearum (Kawanishi et al. 2011).
3.8.1.2 Functional Characterization One of the most widely used method for assessing gross functional diversity is community-level physiological profiles (CLPP) (Konopka et al. 1998). This approach is facilitated by the use of a commercial taxonomic system, known as the BIOLOG® system that is based on utilization of different carbon sources (Garland 1996). Utilization of each substrate is detected by the reduction of a tetrazolium dye, which results in a colour change that can be quantified with spectrophotometer. Advantages of CLPP include ability to differentiate between microbial communities, relative ease of use, reproducibility and production of large amount of data describing metabolic characteristics of the communities. Prior to BIOLOG, several commercial kits utilizing phenotypes for determination of biochemical properties of microbes were also available (Busse et al. 1996). Furthermore, microbes can be checked for various functional traits (Fig. 3.2) like nitrogen fixation (Boddey et al. 1995); phytohormones production (Bric et al. 1991), zinc solubilization (Fasim et al. 2002), ammonia production (Cappuccino and Sherman 1992), siderophore production (Schwyn and Neilands 1987), HCN production (Bakker and Schippers 1987), and phosphate solubilization (Pikovskaya 1948) both qualitatively and quantitatively. Although many new molecular approaches have been applied for studying the biodiversity and role of microorganisms in the environment, classical approach is still useful to assess metabolic potential of diverse microbial communities and provide detailed understanding of their metabolism and functions. 3.8.1.3 16S rRNA Gene Sequencing 16S rRNA molecule is the most common house-keeping genetic marker used for studying bacterial phylogeny and taxonomy. It is 1500 bp in length. Its function has not changed over the time, hence random sequence changes in 16S rRNA are accurate measure of the evolution (Christensen et al. 2001). 16S rRNA genes may not be identical in all organisms and comprised of both variable and conserved regions (Tortoli 2003). The presence of variable regions does not affect the use of 16S rRNA for bacterial identification and in finding the close relationship at the genus or species level (Garrity and Holt 2001). Universal primers usually complementary to the conserved regions present at the beginning of the gene and at either of 540bp region or at the end of the whole sequence (1550bp) are used for amplification and sequencing. The sequence of the variable region in between is used for the comparative taxonomy (Relman 1999). Sometimes sequencing of entire 1500bp region is required to distinguish between particular taxa or strain (Sacchi et al. 2002). Since initial 500bp region is slightly more diverse, it provides adequate
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differentiation for identification and also provides bigger percent difference between strains. The applications of 16S rRNA gene sequence are as follows:
Identification of Novel Pathogen In every publication regarding description of new prokaryote, 16S rRNA gene sequence is important. 16S rRNA gene sequence analysis provides accurate identification at the species level and can also clarify their clinical importance (Clarridge et al. 1999). Other techniques for the identification include the most common DNA– DNA hybridization technique which is considered as standard for proposing new species. Depending upon DNA–DNA hybridization, which provides reassociation kinetics, the genetic definition of a species is quantifiable, i.e., (1) 70% DNA– DNA relatedness and (2) 5 C or less ΔTm for the stability of heteroduplex molecules.
Identification of Unculturable Bacteria Universal primers against 16S rRNA gene region are used to derive a sequence for uncultured bacterium.
3.9
Modern Approach
3.9.1
Functional Genomics
Functional genomics is the study of how genes, genomes, proteins, and metabolites contribute to particular phenotype. Functional genomics comprise the study at DNA (genomics), gene (transcriptomics), protein (proteomics), and metabolite (metabolomics) level. Functional genomics unfolds the interaction between genes and proteins. It combines data derived from various molecular process related to DNA sequence, gene expression, and protein function. Further analysis requires proper modeling for molecular dynamics and interactive study that regulate gene expression, cell cycle progression, and cell differentiation. Various tools used for functional genomics are as follows:
3.9.2
DNA Microarray
It is a molecular technique that comprises thousands of microscopic DNA probes (spots) attached to solid surface, such as silicon chip or glass. Labelled ssDNA or RNA fragment from a sample of interest are hybridized under stringent conditions. The amount of nucleic acid content extracted from an original sample is directly proportional to the amount of hybridization detected in microscopic probes spots.
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Next-Generation Sequencing
In next-generation sequencing (NGS), DNA template is fragmented, attached to adaptors followed by amplification in PCR, and then immobilized on beads where identical cluster of DNA are formed. These cluster DNA fragments are ready for nucleotide incorporation followed by washing and detection, where the read length is directly proportional to the number of cycles. Prominent and widely used nextgeneration sequencing (NGS) platforms are Roche 454 platform (Roche Life Science), Illumina and Applied Biosystem SOLiD platform (Shendure et al. 2005).
3.9.4
Mass Spectrometry
Mass spectrometry analyses the samples through generation of multiple ions which separate according to charge-to-mass ratio. Three main components of mass spectroscopy include an ion source (convert gas phase into simple ions), mass analyser (separates sample ions under influence of electromagnetic field), and a detector. Most recent and advanced mass spectrometer available nowadays is Orbitrap, is versatile, dynamic in range, has high accuracy and high resolution which enable its use in proteomics and metabolomics application. In Orbitrap, ions are trapped in an orbital motion around the spindle, and the image obtained from these trapped ions are detected which are further converted into mass spectrum by using Fourier transform. Orbitrap provides tandem mass spectra of compounds which help in elucidation of analyte structure thus resulting in identification of trace-level components from the complex mixture (Makarov and Scigelova 2010).
3.9.5
Transcriptomics
Transcriptomics is profiling the abundance of transcript under various conditions in different cell types. These RNA sequences (Transcript) also enable to analyse exon/ intron and transcript boundaries which result in some novel transcript discovery. In addition, transcriptomics can also be used for profiling noncoding RNA, ribosomeassociated mRNA, and has potential to unfold the regulation at transcription and post-transcriptional level. The advantage of RNA-Seq over DNA microarray is that it is independent of species of interest and thus can be implemented for all.
3.9.5.1 Transcriptomics and Agriculture Transcriptomics approach provides a feasible tool to study microbial community associated with different plants (Molina et al. 2012; Sheibani-Tezerji et al. 2015). Metagenome and genomic analysis enumerate presence or absence of genes, but transcriptomics provides expression level of specific genes under different microenvironment conditions. Thus, it became an important key to understand the microrhizobiome association with host plants. Profound analysis of differentially expressed genes in host plants helps in elucidating mechanism of association
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between plants and rhizomicrobiome. Dual RNA sequence profiling provides a better resolution of expressed genes in both partners (in symbiosis) at the same time. Symbiotic association between Azospirillum brasilense and wheat plants has been monitored through study of upregulation of genes associated with the cell cycle progression and nutrient acquisition (Camilios-Neto et al. 2014).
3.9.6
Proteomics
Proteins are considered to be most important functional unit of cell. Sometimes transcript level does not necessarily correlate with the quantity of protein then, proteomics is used. Proteomics also unravel the mechanism of complex post translational modifications. Different techniques are used to study the protein content of the cell. The 2D-gel electrophoresis is used to evaluate the protein content. The technique involves the separation of protein first by mass then by the charge present on polypeptide. Another relatively most used proteomics approach is GeLC-MS, in which one-dimensional gel electrophoresis (SDS-PAGE) proteins are first separated and then each gel lane is divided into equally sized section from which proteins are digested and separated by liquid chromatography and finally analysed by mass spectroscopy (MS). More recently, a high-throughput technology, e.g. multidimensional protein identification technology (MudPIT), has been developed. It provides an efficient way to identify large number of proteins from complex ones. In MudPIT, proteins are digested into peptides followed by separation through two-dimensional chromatography based on hydrophobicity and charge and are subsequently analysed by MS.
3.9.6.1 Proteomics and Agriculture Proteomics analysis emphasized identification of novel physiological stress-related proteins that are expressed in most complex environments of rhizomicrobiome. Total protein can be extracted from the rhizomicrobiome either by direct or indirect lysis method (Maron et al. 2007). Direct lysis method involves total protein isolation from rhizomicrobiome that are expressed under natural and stress conditions. The protein fingerprints thus obtained are further subjected to production and analysis of those metabolites which are necessary for the plant protection. Indirect method includes isolation of total proteins from cultured rhizosphere endophytes that are expressed under stress condition. The protein fingerprint thus obtained was further subjected to 2D-gel electrophoresis (Bhuyan et al. 2015).
3.9.7
Metabolomics
Metabolomics deals with the detection and characterization of exudates that are released by microorganisms in the rhizomicrobiome. Tracing of metabolite directly correlates with cellular phenotype rather than genes or proteins. Metabolomics targets the complex cellular metabolism and characterization of new cellular
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pathways that can later be used for drug delivery system like in cancer. The most widely used tools in metabolomics involve liquid chromatography coupled with mass spectroscopy (MS) and NMR (Nuclear magnetic resonance). The main advantage of NMR is easy sample preparation and high reproducibility.
3.9.7.1 Metabolomics and Agriculture Metabolomics is an emerging field and its application in agriculture field is still under progression. Several factors are limiting the study of root exudates. These include limitation in tracing specific exudates; sensitivity error in current metabolomics platforms; and difficulties in tracking the temporal and spatial dynamics of exudates at relevant scales (Van Dam and Bouwmeester 2016). But question remains the same that how metabolomics help in analysing a complex system such as rhizomicrobiome? GC-MS and LC-MS along with NMR (Nuclear magnetic resonance) spectroscopy are most widely used technologies for analysing metabolites in the biological samples (Dunn and Ellis 2005). At present, extraction and identification of root exudates is still the major challenge in rhizosphere metabolomics (Pandey and Mann 2000). It requires separate processing of microbe’ and plant fractions. The final product is formed upon their interactions, and use of final metabolites allows to evaluate the functional community present in soil.
3.9.8
Interactomics
It is the study of networking and interaction at molecular and physiological level. It involves protein–protein interaction, e.g., functional interaction found in signal transduction, metabolic pathways and transcriptional regulation and many important biological functions. Dissecting these interactions plays a vital role in understanding the interactive pathways that forms the basis of many cellular processes. Recent interactomics’ techniques involve tandem affinity purification (TAP) which involves two steps of high specificity affinity purification. In combination with other tools, such as phage display and protein microarray, these technologies help in understanding the interactive protein networking.
3.9.9
Metagenomics
Metagenomics is defined as an analysis of the complete microbial genome from any environmental niche (Zeyaullah et al. 2009). It gives a comprehensive view of the species composition, genetic diversity, evolution, and interactions of microbial communities with its natural environment (Simon and Daniel 2011). The metagenomic approach can either be functional (Rabausch et al. 2013) or sequence-based (Soni et al. 2012), which can be used for targeting different aspects of a microbial community. The sequence-based approach is a reliable tool to study the structure of the uncultivated microbial population through 16S rDNA based analysis, whereas the metabolic or functional potential of a microbial community can
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be analysed by using functional metagenomics. Thus, functional metagenomics can be considered as a major tool for identifying and characterising novel gene families from rhizosphere metagenome. Metagenomics is not only helpful in determining bacterial diversity but also useful in exploring the fungal population in the rhizosphere (LeBlanc et al. 2015). Many large-scale metagenomics projects have been undertaken to investigate various aspects of the microbial composition, e.g. Human Microbiome Project, International Census of Marine Microbes, and Earth Microbiome Project. Bioinformatic software are required to handle a large amount of data generated from different next-generation sequencing platforms, such as 454 pyrosequencing and illumina-based sequencing. Some important and widely used software available for such metagenomic analysis include Quantitative Insights into Microbial Ecology (QIIME), mothur, CARMA, and MEGAN (Escobar-Zepeda et al. 2015). Software namely Illumina reads and PacBio reads have been recently developed for short and very long sequence analysis, respectively. Moreover, a connection between taxonomic classification from meta-profiling and metabolic information is established through PICRUSt software (Langille et al. 2013). Despite the immense importance of microbes in the rhizosphere, very little information is available about their diversity and functions at a community level. Metagenomics has an advantage over culture-dependent approaches to investigate the community structure and exploit the functionalities of microbiome as all of them are life-forms based on DNA as a carrier of genetic information. Furthermore, sequence-based metagenomic studies reported that rice rhizosphere has the abundance of Actinobacteria, Firmicutes, Acidobacteria, Planctomycetes, and Proteobacteria (Bhattacharyya et al. 2016), whereas rhizosphere of wheat mainly showed association with phyla Chloroflexi and Planctomycetes (Naz et al. 2014) and Actinobacteria, Firmicutes, Archaea, Proteobacteria, virus, fungi, and unclassified taxa (Hernandez-Leon et al. 2012). The soybean rhizosphere was colonized by γ-Proteobacteria, Actinobacteria, and Ascomycetes (Bresolin et al. 2010). Similarly, in the sugarcane rhizosphere, Proteobacteria, was dominant followed by Acidobacteria, Bacteroidetes, Firmicutes, and Actinobacteria (Pisa et al. 2011). Comparative assessment of bacterial communities associated with shisham rhizosphere through Illumina sequencing showed a dominance of Proteobacteria and Firmicutes at Lachhiwala and Tanakpur (healthy forest stands), whereas Acidobacteria at Pantnagar forest (diseased stand) (Joshi 2018). Different management practices, for example, conventional tillage and no-tillage, affected the functional potential of soil microbial communities of soybean and wheat fields (Souza et al. 2013). Chhabra et al. (2013) used a functional metagenomic approach to study mineral phosphate solubilization genes in the rhizosphere of barley, which had not received phosphate fertilizer for the last 15 years. Metagenomic approach was used to investigate microbiome of tap root of sugar beet for various plant-growth-promoting traits. A high number of genes coding for ACC deaminase, ß-1,3-glucanases, siderophore production, and phosphate solubilization were detected, whereas genes involved in IAA production or nitrogen-fixation were rare or not found at all (Tsurumaru et al. 2015). Metagenomic technology has been successful at all scales; it has been used to study single genes, pathways, organisms, and communities.
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Approaches that involve massive sequencing to capture entire communities will likely become more common with further advances in sequencing technology.
3.9.9.1 Metagenomics and Agriculture Metagenome study provides an excellent idea about how different microbial community present in rhizomicrobiome help in degradation of toxic compounds that are accumulated in soil. The abundance of Bacteroidetes, Firmicutes, Cyanobacteria, and Actinobacteria in wheat rhizosphere was found to be associated with the degradation of organic soil pollutant, e.g., benzoates, naphthalene, carbazoles, phenols, xenobiotics, and biphenyls (Singh et al. 2018).
3.9.10 Metatranscriptomics Messenger RNA (mRNA) is a short-lived intermediate between DNA and protein. Transcription of mRNA is a highly regulated and energy-expensive process, but mRNA is the most powerful weapon to study cellular responses with respect to change in environmental conditions (Moran et al. 2013). Using high-throughput sequencing techniques such as Illumina, metatranscriptomics offers a non-PCR-based method for looking at transcriptional activity occurring within a complex and diverse microbial population at a specific point in time. However, curation and annotation of these complex data has emerged as a major challenge. Metatranscriptomics uses short sequence reads. The short sequence reads can be either individually aligned directly to external reference databases (hereafter “assembly-free”) or assembled into longer contiguous fragments (contigs) for alignment (hereafter “assembly-based”). Poulsen et al. (2013) used an assembly-based approach to analyse gut microbiome. Whereas, the assembly-free approach has been used in analysis of lactic acid bacterial strains (Jung et al. 2013), aligning short reads to reference genomes. An open source pipeline developed by Martinez et al. (2016) to analyse metatranscriptomics datasets that align short reads directly to a protein database before annotation.
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Sample collection
RNA extraction
cDNA libarary preparation
Assigning transcript to gene
de-novo assembly
Absolute versus relative abundance-normalization Metatranscriptomics Workflow
3.9.10.1 Metatranscriptomics and Agriculture Metatranscriptomics plays an important role dissecting the microbial community and their functional aspects. It also plays an essential role in evaluating rhizobacteriainduced systemic resistance in plants (De Vleesschauwer and Hofte 2009). For example, Pseudomonas fluorescens strains promote resistance in tomato leaf curl virus (Sangeetha et al. 2010). Metatranscriptomics study allows researcher to compare and modulate bacterial gene expression profiles of samples treated with signalling molecules, e.g. ethylene, jasmonic acid, salicylic acid and abscisic acid, and control plants from the rhizosphere to monitor defense response. The expression analysis of coi1, npr1, cpr5, pad4, eds5, jin1, jar1, and etr1 genes help in evaluating the responses that arise during signalling cascade (Jones and Dangl 2006; Kazan and Schenk 2007). Metatranscriptomics analysis of microbial communities associated with rhizosphere help in evaluating the responses that arise during signalling cascade. 3.9.10.2 Metatranscriptomics Tools Compared to other omics approaches, metatranscriptomics is less common. Metatranscriptomics reads are generally analysed and mapped to specialized databases (NCBI) by using specialized alignment tools such as, Bowtie 2, BLAST, and BWA. Results are then annotated using Swiss-Prot, KEGG, GO, and COG. The most recent technique used in the metatranscriptomics analysis is stable isotope probing (SIP) which targets specific transcriptomes of aerobic microorganism. Second strategy is to assemble the small reads of transcriptomes into longer fragments called contigs (Celaj et al. 2014). Several software packages such as Trinity (Grabherr et al. 2011), Oases (Schulz et al. 2012), AbySS, Trans-Abyss,
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MetaVelvet (Namiki et al. 2012), Scriptures, and Cufflinks (Guttman et al., 2010; Trapnell et al. 2010) are used to analyse contigs. Amongst these, Trinity is sensitive across broadest range of gene expression levels. Li and Dewey (2011) developed RNA-Seq by Expectation Maximization (RSEM), a quantitative approach for transcriptome analysis. In RSEM, inputs are taken from reference or standard transcriptome or assembly (analysed from Trinity) along with RNA-Seq reads that are generated from the samples which result in normalizing transcriptomics abundance.
3.9.10.3 Factors Affecting Metatranscriptomic Analysis The parameters that affect the analysis of data generated through metatranscriptomic analysis are as follows Read length: Normalization of gene length during retrieving of data from a shotgun sequencing because sequencing data reads will be directly proportional to the length of the gene. RPKM/FPKM (reads per fragment per kilo base per millions reads) This can be calculated by RPKM ¼
ðcDNA reads obseved per geneÞ 10 ðgene lengthÞ ðtotal number of reads in cDNA libraryÞ
cDNA/ DNA ratio: It is used to measure the number of transcript present in each gene copies.
3.9.10.4 Computational Analysis of Metatranscriptomic Data Dataset of metatranscriptome contains millions of RNA sequenced reads. To analyse such a high informative data, a special tool is required, and several comprehensive tools have also been developed in last few years, e.g. HUMAnN51 and MG-RAST52. These tools along with specialized bioinformatic tools, e.g.GEM54 and BOWTIE53, are used for mapping; Trimmomatic 55 tool is used for quality filtering and Cuff Duff56 tool is to analyse differential gene expression.
3.9.11 Comparative Metatranscriptomics Comparative metatranscriptomics deals with the comparative study of the rhizosphere microbial communities associated with different plant types in the same or different set of environments. It measures community-wide comparative gene transcriptional behaviours, an overview of total metabolic potential, microbial community composition, and transcriptionally active taxa. It plays a very important role in the analysis of different mutants growing under the same set of condition, e.g., comparative study of rhizosphere, microbiome of an avenacin-deficient mutant, and wild type oat sad1 under same field conditions (Haralampidis et al. 2001). Comparative metatranscriptomics is very useful in determining rhizosphere microbial communities that are expressed under seasonal variation and stress condition, e.g. differential gene expression of day/night pattern of microbial assemblage
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(