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- Herausgeber: John Wiley & Sons
- Kategorie: Wissenschaft und neue Technologien
- Sprache: Englisch
A guide to the role microbes play in the enhanced production and productivity of agriculture to feed our growing population Phytomicrobiome Interactions and Sustainable Agriculture offers an essential guide to the importance of 'Phytomicrobiome' and explores its various components. The authors - noted experts on the topic - explore the key benefits of plant development such as nutrient availability, amelioration of stress and defense to plant disease. Throughout the book, the authors introduce and classify the corresponding Phytomicrobiome components and then present a detailed discussion related to its effect on plant development: controlling factors of this biome, its behaviour under the prevailing climate change condition and beneficial effects. The book covers the newly emerging technical concept of Phytomicrobiome engineering, which is an advanced concept to sustain agricultural productivity in recent climatic scenario. The text is filled with comprehensive, cutting edge data, making it possible to access this ever-growing wealth of information. This important book: * Offers a one-stop resource on phytomicrobiome concepts * Provides a better understanding of the topic and how it can be employed for understanding plant development * Contains a guide to sustaining agriculture using phytomicrobiome engineering * Presents information that can lead to enhanced production and productivity to feed our growing population Written for students, researchers and policy makers of plant biology, Phytomicrobiome Interactions and Sustainable Agriculture offers a clear understanding of the importance of microbes in overall plant growth and development.
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Table of Contents
Cover
Title Page
Copyright Page
Dedication Page
List of Contributors
Preface
About the Editors
1 Plant Root Exudate Analysis
1.1 Introduction
1.2 Root Exudates Composition: Collection and Analysis
1.3 Role of Root Exudates in Shaping Rhizospheric Microbiomes
1.4 Applications of Root Exudation
1.5 Conclusion and Future Prospects
References
2 Phytoproteomics
2.1 Introduction
2.2 Phytomicrobiome
2.3 Phytomicrobiome: The Communication via Signaling
2.4 Proteomics
2.5 Analysis of Phytomicrobial Interactions Using Proteomics Approaches
2.6 Conclusion and Future Prospects
References
3 Metagenomics
3.1 Introduction
3.2 Metagenomics
3.3 Metagenomics of Plant Rhizosphere
3.4 Metagenomics of Plant Phyllosphere
3.5 Metagenomics of Plant Endosphere
3.6
In‐silico
Tools for Metagenome Analysis
3.7 Recent Progress in Metagenomic Studies of Plant Microbiome
3.8 Conclusion and Future Prospects
References
4 Combating the Abiotic Stress Through Phytomicrobiome Studies
4.1 Introduction
4.2 Phytomicrobiome Signaling Compounds
4.3 Mechanisms of Phytomicrobiome Associated with Abiotic Stress Tolerance
4.4 Importance of Phytomicrobiome Engineering for Crop Stress Alleviation
4.5 Omics Strategies in Phytomicrobiome Studies
4.6 Conclusion and Future Prospects
Acknowledgments
References
5 Microbial Diversity of Phyllosphere
5.1 Introduction
5.2 Origin of Phyllosphere Microflora
5.3 Tools to Study Phyllomicrobiome
5.4 Biodiversity of Phyllosphere
5.5 Microbial Adaptation to Phyllosphere
5.6 Interaction of Phyllomicrobiota with Plants
5.7 Significance of Phyllomicrobiome Studies
5.8 Conclusion and Future Prospects
References
6 Rhizosphere Engineering
6.1 Introduction
6.2 Natural Plant–Microbe Interactions in Rhizosphere
6.3 Molecular Mechanisms in Plant–Microbe Interactions in Rhizosphere
6.4 Biochemical Components in Rhizosphere Signaling
6.5 Tools and Techniques in Rhizosphere Engineering
6.6 Rhizosphere Components Amenable to Engineering
6.7 Conclusion and Future Prospects
Acknowledgment
References
7 Plant Communication with Associated
7.1 Introduction
7.2 Biofilm and Rhizospheric Interactions
7.3 Biofilm Formation at the Root Rhizosphere
7.4 Genetic Features Responsible for Bacterial Cell Adhesion to Plant System
7.5 Nutrient Interactions
7.6 Biotic Interaction
7.7 Conclusion and Future Prospects
References
8 Phytomicrobiome
8.1 Introduction
8.2 Phytoremediation
8.3 Phytomicrobe Interactions and Rhizomediation
8.4 Conclusion and Future Prospects
References
9 Rhizospheric Biology
9.1 Introduction
9.2 Engineering the Rhizosphere
9.3 Engineering Soil Microbial Populations and Plant–Microbe Interactions
9.4 Plant Growth‐Promoting Rhizobacteria: Mechanisms, Potential, and Usages
9.5 Plant–Microbe Interaction
9.6 Biofertilizers and its Applications
9.7 Plant Genetic Engineering
9.8 Conclusion and Future Prospects
Acknowledgments
References
10 Application of Inorganic Amendments to Improve Soil Fertility
10.1 Introduction
10.2 Impact of Bhoochetna Movement in Southern India
10.3 Sustainable Agriculture
10.4 Factors to Be Considered While Selecting a Soil Amendment
10.5 Advantages of Soil Amendments
10.6 Land Modeling
10.7 Major Applications of Soil Amendments
10.8 Combination Strategy for Soil Quality Improvement
10.9 Conclusion and Future Prospects
References
11 Improved Plant Resistance by Phytomicrobiome Community Towards Biotic and Abiotic Stresses
11.1 Introduction
11.2 Microbes and Plants
11.3 Response of Abiotic Response on Plant
11.4 Role of Phytohormones in Increasing Abiotic and Biotic Stress Tolerance
11.5 Gene Transfer in Plants
11.6 Conclusion and Future Prospects
References
12 Bioprospecting
12.1 Introduction
12.2 Plant‐Associated Microbial Communities
12.3 Beneficial Effects of Plant‐Associated Microbial Communities
12.4 Role of Microbial Processing (Signals) in Facilitating Plant Growth
12.5 Conclusion and Future Prospects
Acknowledgments
References
13 Advances in Omics and Bioinformatics Tools for Phyllosphere Studies
13.1 Introduction
13.2 Recent Trends and Approaches
13.3 Computing for Biology
13.4 Bioinformatics in Microbial Research
13.5 Phyllosphere Microbiome Studies Based on Genome‐Wide Association
13.6 Omics Strategies and Their Integration
13.7 Conclusion and Future Prospects
References
14 Microbial Mediated Zinc Solubilization in Legumes for Sustainable Agriculture
14.1 Introduction
14.2 Chronological Events of Zinc Biology
14.3 Role of Zinc in Living System
14.4 Zinc Deficiency vs. Zinc Toxicity in Crop Plants
14.5 Availability of Zinc in Soil Environment
14.6 Factors Affecting Zinc Availability to Plants
14.7 Response of Legume Crops to Zinc
14.8 Microbial Mediated Zinc Solubilization in Legume Crops
14.9 Conclusion and Future Prospects
References
15 Composition and Interconnections in Phyllomicrobiome
15.1 Introduction
15.2 Significance of Phyllospheremicrobiota
15.3 Phyllosphere Microorganisms as Plant Growth Regulator
15.4 Plant–Pathogen Interactions Mediated by Phyllosphere Microbiome
15.5 Conclusion and Future Prospects
References
Index
End User License Agreement
List of Tables
Chapter 1
Table 1.1 Root exudation of different plants: biochemical nature of root exud...
Table 1.2 Developments in root exudate studies and their action mechanism.
Chapter 2
Table 2.1 Proteomic approaches available for detection of plant and microbes ...
Table 2.2 Examples of phytomicrobiome interactions.
Chapter 3
Table 3.1 Advance molecular techniques used for the characterization of vario...
Chapter 4
Table 4.1 Role of phytomicrobiome in abiotic stresses studied recently.
Chapter 5
Table 5.1 Major findings obtained from the study of the phyllomicrobiome of d...
Table 5.2 Microbial diversity in the phyllosphere of various crop plants.
Chapter 6
Table 6.1 Signaling molecules secreted by plants for establishing plant–micro...
Table 6.2 Signaling molecules secreted by microbes for establishing plant‐mic...
Table 6.3 Rhizobacteria used for alleviation of heavy metal stress in plants.
Chapter 7
Table 7.1 List of microorganism forming biofilm and their mode of attachment.
Table 7.2 List of endophytic bacterial mutant having genetic alteration and r...
Chapter 8
Table 8.1 Composition of root exudates.
Table 8.2 List of crop plants used in phytoremediation of heavy metals from s...
Table 8.3 Potential microorganisms for biodegradation of different organic po...
Chapter 9
Table 9.1 Various compounds in root exudates of different plant species.
Table 9.2 Mechanisms of PGPR.
Table 9.3 Nitrogen‐fixing bacteria with their relationship to host plants.
Chapter 10
Table 10.1 Differences between organic and inorganic amendments.
Chapter 15
Table 15.1 Phyllosphere microorganisms as biocontrol agents.
Table 15.2 Plant–pathogen interaction by phyllosphere microorganisms.
List of Illustrations
Chapter 1
Figure 1.1 Classification of root exudates compounds: various compounds are ...
Chapter 2
Figure 2.1 A schematic flowchart of proteomic approaches for phytomicrobiome...
Chapter 3
Figure 3.1 Metagenomic approach to reveal the structure and function of a pl...
Chapter 4
Figure 4.1 Schematic diagram representing the interplay of phytomicrobiome a...
Chapter 5
Figure 5.1 Different parts of phyllosphere and the multipartite interactions...
Figure 5.2 Classification of root exudates compounds: various compounds are ...
Chapter 6
Figure 6.1 Techniques used for rhizosphere engineering.
Figure 6.2 Approaches to engineer rhizosphere for sustainable agriculture.
Chapter 7
Figure 7.1 Phyto‐rhizospheric microbial interaction.
Figure 7.2 Formation of biofilm at the root rhizosphere.
Figure 7.3 Quorum sensing at the root rhizosphere.
Figure 7.4 PGPR‐dependent nitrogen fixation.
Chapter 8
Figure 8.1 Schematic diagram representing degradation of Inorganic and organ...
Chapter 9
Figure 9.1 Overview of PGPR mechanisms.
Sources:
Pankaj et al. 2013; Bhatt a...
Chapter 10
Figure 10.1 Physical, chemical, and biological indicators of soil quality. K...
Figure 10.2 Permeability and water retention ability of different types of s...
Chapter 11
Figure 11.1 Plant response to different forms of biotic and abiotic stresses...
Chapter 12
Figure 12.1 Plant microbiota: promoting plant growth and health, suppressing...
Figure 12.2 Role of endophytes in the process of phytoremediation: endophyte...
Chapter 13
Figure 13.1 Schematic representation of central dogma with biological tasks....
Figure 13.2 Structural organization of information extraction in bioinformat...
Figure 13.3 Various tasks that can be done through bioinformatics in microbi...
Chapter 14
Figure 14.1 Role of zinc in plants.
Figure 14.2 Causes of zinc deficiency in crops.
Chapter 15
Figure 15.1 The significance of phyllosphere microbiota in agriculture.
Figure 15.2 Importance of phyllosphere microbiota.
Figure 15.3 Frost injury on leaf surface due to ice nucleation activity.
Guide
Cover Page
Phytomicrobiome Interactions and Sustainable Agriculture
Copyright
Dedication
List of Contributors
Preface
About the Editors
Table of Contents
Begin Reading
Index
WILEY END USER LICENSE AGREEMENT
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Phytomicrobiome Interactions and Sustainable Agriculture
Edited by
Amit Verma
S. D. Agricultural University
Palanpur, Gujarat, India
Jitendra Kumar Saini
Central University of Haryana
Mahendergarh, Haryana, India
Abd El‐Latif Hesham
Beni‐Suef University
Beni‐Suef, Egypt
Harikesh Bahadur Singh
GLA University
Mathura, Uttar Pradesh, India
This edition first published 2021© 2021 John Wiley & Sons Ltd
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The right of Amit Verma, Jitendra Kumar Saini, Abd El‐Latif Hesham and Harikesh Bahadur Singh to be identified as the authors of the editorial material in this work has been asserted in accordance with law.
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Library of Congress Cataloging‐in‐Publication DataNames: Verma, Amit, 1983‐ editor. Title: Phytomicrobiome interactions and sustainable agriculture / edited by Amit Verma, S.D. Agricultural University, Gujarat, India, Jitendra Kumar Saini, Central University of Haryana, Mahendergarh, India, Abd El‐Latif Hesham, Beni‐Suef University, Egypt, Harikesh Bahadur Singh, GLA University, Mathura, India. Description: First edition. | Hoboken, NJ : Wiley‐Blackwell, 2021. | Includes bibliographical references and index. Identifiers: LCCN 2020051129 (print) | LCCN 2020051130 (ebook) | ISBN 9781119644620 (hardback) | ISBN 9781119644811 (adobe pdf) | ISBN 9781119644828 (epub) Subjects: LCSH: Plant‐microbe relationships. | Agricultural microbiology. | Plants–Microbiology. | Plants–Effect of stress on. | Sustainable agriculture. Classification: LCC QR351 .P525 2021 (print) | LCC QR351 (ebook) | DDC 579/.178–dc23 LC record available at https://lccn.loc.gov/2020051129LC ebook record available at https://lccn.loc.gov/2020051130
Cover Design: WileyCover Image: © Catherine MacBride/Getty Images
To my father and mother
List of Contributors
Richa AgnihotriICAR‐Indian Institute of Soybean ResearchIndoreMadhya PradeshIndia
Hina BansalAmity Institute of BiotechnologyAmity UniversityNoidaUttar PradeshIndia
Abhishek BhartiICAR‐Indian Institute of Soybean ResearchIndoreMadhya PradeshIndia
Kalpana BhattGurukula Kangri VishwavidhyalayaHaridwarUttarakhandIndia
Pankaj BhattIntegrative Microbiology Research CentreSouth China Agricultural UniversityGuangzhouP.R. China
Sunita ChauhanAmity Institute of BiotechnologyAmity UniversityKantRajasthanIndia
Rakhi DhankharMaharshi Dayanand UniversityRohtakHaryanaIndia
Ajinath DukareICAR‐Central Institute of Post‐Harvest Engineering and Technology (CIPHET)LudhianaPunjabIndia
Bandita DuttaMaulana Abul Kalam Azad University of TechnologyKolkataWest BengalIndia
Saurabh GangolaGraphic Era Hill UniversityBhimtalUttarakhandIndia
Mudasir GaniFaculty of AgricultureSher‐e‐Kashmir University of Agricultural Sciences and Technology Kashmir (SKUAST‐K)Wadura, Sopore, KashmirJammu‐Kashmir (UT)India
Sayantani GaraiUniversity of Engineering and ManagementKolkataWest BengalIndia
Tripti GroverGargi CollegeUniversity of DelhiNew DelhiIndia
Pooja GulatiMaharshi Dayanand UniversityRohtakHaryanaIndia
Aparna GunjalDr. D.Y. PatilArts, Commerce and Science CollegePuneMaharashtraIndia
Shweta KulshreshthaDepartment of Biotechnology, Kumarappa National Handmade Paper InstituteJaipurRajasthanIndia
Arun KumarDepartment of AgronomyPunjab Agricultural University (PAU)LudhianaPunjabIndia
Kapila KumarManav Rachna International Institute of Research and StudiesFaridabadHaryanaIndia
Sanjeev KumarDepartment of Basic Science, College of Horticulture and Forestry Dr. YSP University of Horticulture and ForestryHamirpurHimachal PradeshIndia
Reena KumariDepartment of Biotechnology, College of Horticulture and Forestry Dr. YSP University of Horticulture and ForestryHamirpurHimachal PradeshIndia
Rekha KushwahaUniversity of MissouriColumbiaMO, USA
Dibyajit LahiriUniversity of Engineering and ManagementKolkataWest BengalIndia
Hemant S. MaheshwariEcophysiology of Plants, Faculty of Science and EngineeringGELIFES‐Groningen Institute for Evolutionary Life SciencesGroningenThe Netherlands
and
ICAR‐Indian Institute of Soybean ResearchIndoreMadhya PradeshIndia
Reema MishraGargi CollegeUniversity of DelhiNew DelhiIndia
Aparajita MohantyGargi CollegeUniversity of DelhiNew DelhiIndia
Moupriya NagUniversity of Engineering and ManagementKolkataWest BengalIndia
Sharon NagpalDepartment of MicrobiologyPunjab Agricultural University (PAU)LudhianaPunjabIndia
Neha PatilPDEA’s Annasaheb Magar MahavidyalayaPuneMaharashtraIndia
Suresh Chandra PhularaDepartment of Biotechnology Koneru Lakshmaiah Education FoundationGunturAndhra PradeshIndia
B. Jeberlin PrabinaTamilnadu Agriculture UniversityCoimbatoreTamilnaduIndia
Varsha RaniDepartment of Biotechnology Shoolini UniversitySolanHimachal PradeshIndia
Rina Rani RayMaulana Abul Kalam Azad University of TechnologyKolkataWest BengalIndia
Balram SahuDepartment of Agricultural MicrobiologyIndira Gandhi Krishi VishwavidhyalayaRaipurChhattisgarhIndia
Pawan SainiDepartment of Plant Breeding and GeneticsPunjab Agricultural University (PAU)LudhianaPunjabIndia
and
CSB‐Central Sericultural Research & Training Institute (CSR&TI)PamporeJammu‐Kashmir (UT)India
Pooja SainiDepartment of Plant Breeding, Genetics and Biotechnology, Dr. Khem Singh Gill College of AgricultureEternal University (EU)Baru SahibHimachal PradeshIndia
Deepka SharmaDepartment of Biotechnology, College of Horticulture and Forestry Dr. YSP University of Horticulture and ForestryHamirpurHimachal PradeshIndia
Mahaveer P. SharmaICAR‐Indian Institute of Soybean ResearchIndoreMadhya PradeshIndia
Prachie SharmaManav Rachna International Institute of Research and StudiesFaridabadHaryanaIndia
Sonali ShindeMES Abasaheb Garware CollegePuneMaharashtraIndia
Ravindra SoniDepartment of Agricultural MicrobiologyIndira Gandhi Krishi VishwavidhyalayaRaipurChhattisgarhIndia
Nimmy SrivastavaAmity Institute of BiotechnologyAmity UniversityRanchiJharkhandIndia
Deep Chandra SuyalDepartment of Microbiology, Akal College of Basic SciencesEternal UniversityBaru SahibSirmourHimachal PradeshIndia
Neha TrivediIndian Agricultural Research InstituteNew DelhiIndia
Amit VermaS.D. Agricultural UniversityPalanpurGujaratIndia
Madan L. VermaDepartment of Biotechnology, Indian Institute of Information TechnologyUnaHimachal PradeshIndia
Shulbhi VermaS.D. Agricultural UniversityPalanpurGujaratIndia
Meghmala WaghmodePDEA’s Annasaheb Magar MahavidyalayaPuneMaharashtraIndia
Preface
The microorganisms are of utmost importance to the survival of plants, animals, and humans. Microorganisms interact with their hosts in both positive and negative manners. Therefore, the microorganisms and the technologies based on the microbial processes find many useful applications in the sustainable development of environment, energy, health, and agriculture. The improvements in crop productivity and management of plant diseases require a good understanding of the interactions between microorganisms with different parts of the plants. The plant–microbiome interaction denotes the genome of all the microorganisms, including bacteria, viruses, and fungi, living in and on various parts of plants. In recent times, significant technological progress has been made to improve our understanding of the plant‐microbiome or phytomicrobiome interactions. In order to make agriculture sustainable, it is indeed necessary to learn about various concepts and advances in this field.
This book includes a discussion on some basic concepts, including rhizosphere and phyllospheremicrobiome, analysis of root exudates, role of phytomicrobiome in biotic and abiotic stress management, etc. The book also covers advanced information about metagenomics and proteomics studies in relation to plant microbial community analysis. Modern sustainable practices, including rhizosphere engineering, have also been touched upon.
After numerous deliberations, we came up with the idea to explore the possibility of developing a book on phytomicrobiome interactions and sustainable agriculture. We had in our mind to develop a book that will be beneficial for teachers and students, as well as researchers. Therefore, we invited a variety of researchers and convinced them to contribute the chapters for this book.
We are thankful to our family, friends, students, teachers, and mentors who acted as a source of inspiration to us. At this point we must appreciate the kind gesture of the entire Wiley team, especially Rebecca Ralf (Commissioning Editor), Athira Menon (Project Editor), and Kerry Powell (Managing Editor) who gave us support and showed trust in our capabilities. They generously extended the book timelines in the hard times of the COVID‐19 pandemic and kept supporting us continuously, and as a result, we were able to complete this book in its present form.
This has been our maiden effort to produce a book on phytomicrobiome interactions for the sustainable development of agriculture to help students, teachers, and researchers. We hope that we will get support from the readers of the book. We are always open for criticism, suggestions, and recommendations that can help us to explore other aspects of phytomicrobiome interactions for improving crop productivity.
We dedicate this book to all the persons who are directly or indirectly serving the people affected by COVID‐19.
Amit Verma
Jitendra Kumar Saini
Abd El‐Latif Hesham
Harikesh Bahadur Singh
India, July 2020
About the Editors
Dr. Amit Verma is currently working as Assistant Professor in the Department of Biochemistry, S D Agricultural University, India. He worked under Dr. D.N. Kamra, National Professor, ICAR, India as Research Associate in the Department of Animal Nutrition, IVRI, Bareilly India and studied different aspects of Rumen enzymology. He received his doctorate from G. B. Pant University of Agriculture and Technology, Pantnagar, and investigated the different industrial applications of the Keratinase enzyme. He was awarded with the University Merit Scholarship and CSIR‐JRF, CSIR, India during his doctorate. He qualified for examinations, such as GATE, ICMR JRF, ICAR SRF and ASRB NET. He has keen interest in the field of microbial biotechnology and plant–microbe interactions. His current work is focused on the rhizosphere metabolite investigation of arid plants and phytomicrobiome composition of castor crops under biotic stress. He is a member of many national and international professional bodies. He has written more than 25 research and review articles in reputed peer‐reviewed journals along with 3 books, 15 book chapters, and more than 15 conference proceedings. He also received a Young Scientist Award from the VIRA foundation, India. He also serves as regular reviewer for international reputed journals with high‐impact factors such as (i) Scientific Reports (Impact factor 4.122); (ii) Frontiers in Microbiology (Impact factor 4.019); (iii) Frontiers in Plant Science (Impact factor 3.678); (iv) PLOS ONE (Impact factor 2.77); (v) Protoplasma (Impact factor 2.8).
Dr. Jitendra Kumar Saini received his BSc (Industrial Microbiology) and MSc (Microbiology) degrees from Gurukula Kangri University, Haridwar. He obtained his PhD in Microbiology from Gobind Ballabh Pant University of Agriculture and Technology, Pantnagar in 2010 after which he worked as a postdoctoral associate at GADVASU, Ludhiana in a World Bank–funded NAIP project on Rumen microbiology. Later he joined the DBT‐IOC Centre for Advanced Bioenergy Research, Indian Oil Corporation Ltd., Research and Development Centre, Faridabad as a scientific officer, where he led a team on enzyme development for advanced biofuels. Dr. Saini's work on cellulosic bioethanol production employing thermotolerant yeast won the best poster award at the “International Conference on Emerging Trends in Biotechnology‐2014” held at JNU, New Delhi. He joined the Department of Microbiology, Central University of Haryana, Mahendergarh, in 2016 as an Assistant Professor. His current research focuses on enzyme and microbial technologies for sustainable development of energy and environment. Dr. Saini is a recipient of the Early Carrier Research grant from the Science and Engineering Research Board, Department of Science and Technology, Government of India, and a twinning grant from the Department of Biotechnology, Government of India. He is currently supervising two doctoral and 4 postgrad dissertation students, and has supervised 11 postgrad dissertations in the past, besides co‐supervising a postdoc. He has filed one US patent, is an author of 23 articles, and is an active reviewer for many reputed journals in biofuel and bioenergy research. Dr. Saini conducted a one‐week Global Initiative of Academic Networks course on “Integrated Lignocellulosic Biorefineries for Sustainable Development.” Recently, he organized an International Conference AMI‐2019 entitled “Microbial Technologies in Sustainable Development of Energy, Environment, Agriculture & Health” as an organizing secretary. He is the review editor for the journal, Frontiers in Energy Research. Dr. Saini is a life member of the Association of Microbiologists of India (AMI) and the Asian Federation of Biotechnology (AFOB).
Abd El‐Latif Hesham is the Professor of Microbial Genetics and Environmental Meta‐Genome Biotechnology, Genetics Department, Faculty of Agriculture, Beni‐Suef University, Egypt. He also served as the Professor of Microbial Genetics and Environmental Meta‐Genome Biotechnology in the Genetics Department, Faculty of Agriculture, Assiut University, Egypt. He graduated and got his M.Sc. from the Genetics Department, Faculty of Agriculture, Assiut University, Egypt, and his PhD degree from the Chinese Academy of Sciences in Microbial Genetics and Environmental Meta‐Genome Biotechnology. He has been awarded postdoctoral studies from CAS‐TWAS. He is an expert in microbial genetics and biotechnology, biodegradation, bioremediation and phytoremediation, microbial community structure, soil microbiology and enzyme activities, biological control, antimicrobial activates, biofertilizer, biofuels, and environmental meta‐genome biotechnology. He has authored more than 80 peer‐reviewed publications in reputed Thomson Reuters high‐impact factor journals and one book and seven book chapters in internationally reputed publishers like Elsevier, Springer‐Nature, Taylor & Francis, and John Wiley & Sons. He is a key person in many national and international research projects related to field of microbial genetics and applied biotechnology. He has been a scientific and organizing committee member and invited speaker in various international conferences. He is also a recipient of several prestigious national and international awards including most recently, being named a member of the Egyptian National Biotechnology Network of Expertise (NBNE) and Academy of Scientific Research & Technology (ASRT), and has been appointed as the Country Representative for Egypt and the Arab Counties by the International Biodeterioration & Biodegradation Society (IBBS) UK, which belongs to the Federation of European Microbiological Societies (FEMS). He is an associate editor and editorial board member for journals, such as (i) Scientific Reports, (ii) Frontiers in Microbiology, (iii) Current Bioinformatics, (iv) PeerJ, (v) All Life Journal, (vi) International Journal of Agriculture & Biology, (vii) Journal of Environmental Biology, and (viii) Biocatalysis and Agricultural Biotechnology.
Dr. Harikesh Bahadur Singh is a Professor in the Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, India. Over the past 35 years, Professor Singh has served Central Universities and CSIR Institutes with his teaching and research skills. Professor Singh has been decorated with several prestigious awards, including the CSIR Technology Award by the Honorable Prime Minister of India, the Vigan Bharati award, the Mundukar memorial award, the BRSI Industrial Medal, the Vigyan Ratna by CSTUP, the Panchanan Meheshwari Medal, and many more, for his key role in translating agriculturally important microorganisms from lab to land. To his credit, he has 20 US patents, 350 research papers, 17 edited books, 70 book chapters, and 55 review articles. Professor Singh is also a Fellow of the National Academy of Agricultural Sciences. Professor Singh is serving as an associate/academic/board editor with journals of international repute.
1Plant Root Exudate Analysis: Recent Advances and Applications
Shulbhi Verma and Amit Verma
S.D. Agricultural University, Palanpur, Gujarat, India
1.1 Introduction
Root exudates are a group of chemical compounds released from plant roots, which contains the ability to alter the activity of soil and microbes below the ground. These chemical compounds are the basis of interaction among root, soil, and microbes in the rhizosphere and also assist in root colonization. Such interaction assists in development‐ and defense‐related activity in plants through enhancing the nutritional availability and suppressing disease occurrences by the alleviation of various stress factors. Root exudates pave the way for communication within the rhizosphere around plant roots, play a pivotal role in the soil system, and create phytomicrobiomes. Generally, plant root exudate consists of 10–40% carbon, primary and secondary metabolites, mucilage, protein, strigolactones, phytohormone, steroids, terpenoids, fatty acids, and nucleotide derivatives, which act as modifiers of rhizospheric soil (Figure 1.1).
Moreover, different parts of the root release different chemical compounds into the soil, such as meristem, the root elongation zone exudes asparagine and threonine, the root hair zone releases various hydrophobic and hydrophilic amino acids, including phenylalanine, leucine, valine, and glutamic acid, aspartic acid excretes from all parts of the root zone, and the root tip secretes mucilage (Badri and Vivanco 2009). Root exudates characteristics and amounts get changed according to plant genotype, age, biotic, and abiotic stress state, health and disease conditions of the plant, the surface area of the root system, and root architecture (Badri and Vivanco 2009). Apart from the plant characteristics, the environmental factors also show an impact on the root exudation mechanism and exudate constituents (Canarini et al. 2019). Thus, understanding the mechanism of root exudation, and factors affecting it, is of prime importance to support environmentally sustainable agriculture and to alleviate the large use of agricultural chemicals that create biosphere contaminations.
Interaction of root exudates and microbes can change the face of the soil, and plants flourish under such conditions, which combats the ill effects of various environmental factors. Thus, root exudation directly effects plant development, which is beneficial to humans and the environment. It is well established that these interactions can promote the growth and productivity of plants, suppress plant disease, increase immunity and the defense of plants, increase nutrient availability and utilization of plants, and enable better coping mechanisms in stress conditions (Bais et al. 2006). Exudation and its interaction with microbes produces a great impact on soil fertility, which may replace the chemical fertilizer applications and pave a way toward eco‐friendly cultivation traditions. It is a well‐established fact that a link exists between the root exudate metabolites and the rhizosphere recruitment of different microbial communities (Schulz‐Bohm et al. 2018; Sugiyama 2019). Apart from interaction studies, root exudates research is at a culminating point with the development of aptamers specifically for root exudates, which can be utilized for development in a fertilizer system (Emily et al. 2013).
Figure 1.1 Classification of root exudates compounds: various compounds are found in the root exudation, which belongs to wide array of biochemical classes.
Root exudates exploration revealed the high diversity of chemicals in plant root exudates. Exudation profiling revealed the presence of chemical compounds, and explains the function of concerning chemical in the soil ecosystem and their effects on plant systems. Few technologies, such as NMR and MS, narrate the structural characters of exudate compounds for clearer observations and assist in unravelling the properties of these compounds that are present in root exudates (Verma et al. 2018). Thus, these studies are directed to the chemical synthesis of those compounds, which can be further utilized for conditioning the soil for particular crop cultivation and for paving a way toward “rhizosphere engineering” (Bais et al. 2006). Root exudates profiling may prove to be the strongest technique for elaborating on the root role and overcomes the plant‐ and soil‐ related issues that hinders crop productivity and sustainable agriculture.
1.2 Root Exudates Composition: Collection and Analysis
Root exudates chemicals secreted through plant roots are necessary for the soil environment as well as for the plant. Root exudates analysis is quite essential in order to know the function of chemicals present in the exudates. There were several procedures to know the compounds present in the root exudates, such as high performance liquid chromatography (HPLC), UV, visible absorption, transcriptome analysis, metabolomics, proteomics, and gas chromatography–mass spectrometry (GS/MS) utilized to determine various compound present in exudates (Table 1.1).
There are several methods of root exudate collection from mature trees. The characterization of its composition has revealed the hidden capacity of root exudates in stimulating microbial activity and decomposition activity of organic soil matter (Phillips et al. 2008). However, the method depends on a realistic architecture to resemble the natural rhizosphere and doesn't accompany an accumulation of other compounds usually not present in exudate. Root secretion possesses several biological active compounds that reduce the dependency on chemicals in the soil and is safe for environment (Carlsen et al. 2012). To avoid the impact of microbes on root exudates profiles, sterilized water cultivation systems were adopted (Badri et al. 2008; Oburger et al. 2013; Strehmel et al. 2014). Furthermore, hydroponics strategy permits exudate sampling with minimum root damage. Root exudates collected in nutrition solution at three and seven days from model organism Arabidopsis thaliana for analysis by LC–MS revealed the difference in wild and mutant root exudates composition (Badri et al. 2008). As days increase, root exudates secretion increases, as shown in the seven‐day root exudates collection period in a nutrient solution that it is quite sufficient for analysis of chemical composition through ultraperformance liquid chromatographic–electrospray‐ionization technique–time of‐flight mass spectrometry (UPLC/ESI‐QTOFMS). This estimated 103 compounds includes different classes of biological compounds related to nucleic acids, secondary metabolites, amino acids, and defense molecules (Strehmel et al. 2014). In contrast, six hours of exudate of Zea mays exposed to different nutrient deficiencies were analyzed through HPLC and statistics were used to reveal the strong influence of a nutritional status of a plant to cope with a limiting nutrient supply (Carvalhais et al. 2010). The limitation of such hydroponic medium collection of exudates is a very different type of plant development as compared to a natural solid substratum growth of a plant. Therefore, a solid medium for exudate collection is designed utilizing vermiculite, sand, perlite, etc., which mimics the rhizospheric conditions more closely. Transcriptome and other omic technologies involved in the analysis of exudate from different microbes reveals the gene and protein involved in the plant microbe's interaction. However, root exudate collection from the natural rhizospheric region is still one of the best methods to collect and analyze root exudate of plants under different conditions. Apart from this, there is a requirement of keeping the physical parameter near to the natural conditions, especially pH and temperature conditions, during the collection of root exudate. Through root exudation analysis we came to know about the impact on microbes and function in rhizosphere, however, its collection is a major constraint during its analysis, due to a lower concentration and presence of many compounds in several times a higher concentration, which is irrelevant to root exudation. So, there is a requirement of using a combination of collection methods to analyze the root components with high accuracy in order to assign the function imparted by the respective component in the growth and development of plants.
Table 1.1 Root exudation of different plants: biochemical nature of root exudate components and techniques involved in characterization.
Plant System
Exudate Profile
Technique
References
Maize (
Zea mays
)
Wide variety of fatty acids, nitrogenous compounds, organic acids, steroids, and terpenoid derivatives
GC–MS and
1
H NMR
Lima et al. (
2014
)
Lettuce (
Lactuca sativa
)
Exudate comprises amino acids, amides, sugars, sugar alcohols, organic acids
GC–MS
Neumann et al. (
2014
)
Arabidopsis
Varied composition of sugars, sugar alcohols, amino acids and phenolics at different developmental stages
GC–MS
Chaparro et al. (
2013
)
Tall fescue (
Lolium arundinaceum
)
Sugars, polyols, growth factors and vitamins, lipids, amines, phenolics, carboxylic acids, nucleosides and others
GC‐(TOF) MS (gas chromatography –time of flight–mass spectrometry)
Guo et al. (
2015
)
Taro plants (
Colocasia esculenta
)
Organic acids like lactic acid, benzoic acid,
m
‐hydroxybenzoic acid,
p
‐hydroxybenzoic acid, vanillic acid, succinic acid and adipic acid.
GC–MS
Asao et al. (
2003
)
Potato (
Solanum tuberosum
L.)
Sugar quantification
Colorimetric estimation using glucose and fructose assay kits
Hoysted et al. (
2018
)
Maize (
Zea mays
)
Benzoxazinoids compounds
HPLC‐DAD
Neal et al. (
2012
)
Beech forest (
Fagus sylvatica
L.)
Low‐molecular organic acids
Ion chromatography
Shen et al. (
1996
)
Sugar Maple (
Acer saccharum
Marsh.)
Organic acids, carbohydrates, amino acids and amides
Thin‐layer chromatography
Smith (
1970
)
Betula alleghaniensis
,
Fagus grandifolia
, and
Acer saccharum
Carbohydrates, amino acids/amides, organic acids, and 9 inorganic ions
–
Smith (
1976
)
Fagopyrum esculentum
L‐tryptophan, fructose‐leucine or fructose‐isoleucine, fructose‐phenylalanine,
N
‐acetyl glutamic acid methyl ester
UHPLC‐HRMS
Gfeller et al. (
2018
)
Buckwheat (
Fagopyrumesculentum
)
Caprolactam, an inhibitory allelochemical
1H and 13C NMR spectra
Tin et al. (
2009
)
Mesocosms having different plants
organic carbon
HPLC‐IRMS system
Karlowsky et al. (
2018
)
Datiscaglomerata
Flavonoids with abundant aglycones
HPLC, UV absorption and LC–MS
Gifford et al. (
2018
)
Medicago
spp.
Flavonoids exclusively isoflavonoids
HPLC, UV absorption and LC–MS
Gifford et al. (
2018
)
1.3 Role of Root Exudates in Shaping Rhizospheric Microbiomes
Root exudate composition resembles the plant constitution and its release of the organic compounds from the root zone allows it to participate in the rhizodeposition process (Jones and Darrah 1995). Root exudation is composed of a tremendous range of chemical compounds, including primary as well as secondary metabolites, ions, mucilage, reactive oxygen molecules, water molecules, amino acids, enzymes, peptides, sugars, vitamins, nucleotides, organic acids, plant inhibitors, growth regulators, sterols, fatty acids, phenolic compounds, flavonoids, and other miscellaneous chemicals (Bais et al. 2006; Huang et al. 2014; Tsuno et al. 2019). Root exudates contain the capacity to modulate the plant microbe interaction in the rhizosphere (De Weert et al. 2002; Zwetsloot et al. 2019). Moreover, these chemical compounds help microbes in the activity in the soil around the root, which is beneficial to plant development as well as to regain soil fertility.
Legume plants are considered an excellent example of shaping rhizospheric microbes through nitrogen assimilation through symbiotic associations of rhizobacteria. The key factor of plant rhizobia interaction in shaping rhizosphere is that flavonoid composition exists in the root exudates of legumes (Abdel Lateif et al. 2012; Weston and Mathesius 2013). Recently, researchers focused on microorganisms other than rhizobiums, which have the capacity of nitrogen fixation, such as cyanobacteria, Frankia, diazotrophsbacteria, etc. Several non‐leguminous plants have rhizobia for nitrogen fixation, such as in Parasponiasp. (family Cannabaceae), which may assist in the shaping of rhizospheric microbes.
Altering the behavioral changes in microorganisms through the effect of root exudates is proven and has been recently termed as “rhizosphere engineering”. In A. thaliana, root secretion possesses antimicrobial compounds that are responsible for its resistance to many non‐host pathogens that are present in the rhizosphere. Phenolic compounds and antimicrobial protein of root exudates may help in guarding the roots against potential pathogens (Bais et al. 2005). In experimental research, evidence shows that root exudate diversity is a crucial link between plant diversity and soil microorganisms (Steinauer et al. 2016). For better dynamic in‐depth interaction knowledge apart from phenolic compounds, flavonoid molecules and several biomolecules possess the capacity to increase favor around the rhizosphere. There are enormous biological molecules in root exudates, such as rosmarinic acid, jasmonic acid, and napthoquinones, which direct microbes toward plants for mutual benefit (Brigham et al. 1999; Bais et al. 2002; Carvalhais et al. 2015). Furthermore, there are few biomolecules, such as flavonoid, strigolactones, and terpenoids, which assist plants in specifically attracting the beneficial counter‐partner through root signals (Vranova et al. 2013; Lareen et al. 2016; Massalha et al. 2017). Mutualistic interactions, nodulation and mycorrhizal interactions, signal perception and transduction such as receptor‐like kinases (RLKs) are the signal‐based interaction of plant and microbes (Lagunas et al. 2015).
In the consecutive discussion, root excaudate’s role as a messenger that communicates within rhizosphere is examined. This perspective is well defined in root–root communication involved in an allelopathy phenomenon in the rhizosphere, which contributes in agricultural growth, because rhizospheric allelochemicals are protective in nature for plants. Root microbe communication in the rhizosphere may enhance the plant biomass through an increase in nutrition uptake, secretion of phytohormones, and helps in defense of the plant (Robin et al. 2008).
1.4 Applications of Root Exudation
Root exudate varies across the plant genotype and changes in root exudates of plant can be utilized in the breeding program for the enhancement of nutritional interaction among plants and microbes. For targeted breeding, perspective profiling of root exudates is essential for sustainable agriculture (Kuijken et al. 2015). This phenomenon is well‐known through exudate profiles among 19 natural Arabidopsis accessions, which shows a high variation in glycosylated and sulfated metabolites, plant hormones, salicylic acid catabolites, phenylpropanoids, coumarin scopoletin, and polyamine derivatives (Monchgesang et al. 2016). Similar studies were done and demonstrated about the rhizobacterial community composition influenced by varying exudation profiles (Micallef et al. 2009). Root exudate chemical composition changes in the condition of nutrient deprivation, which can further assist said breeding program. Few studies represent the effect of nutrient deficiency in the exudates, and the effect of phosphate limitation investigated in Arabidopsis results in the high abundance of oligolignols, which is responsible for lignifications and coumarins in low quantity (Ziegler et al. 2016). Particularly Fe‐deficient strawberry root exudates show a high content of dehydroascorbic acid, trans ferulic acid, galactonic acid, sucrose, and thymidine, whereas P‐deficient strawberry root exudates show higher concentration of malic acid, lysine, galactaricacid, butylamine, and simultaneously show a low concentration of ribonic acid, sorbitol 6 phosphate, and proline (Valentinuzzi et al. 2015).
In the environment, plants are exposed to all kinds of friendly and unfriendly microbes with several stresses in the ground. Plant secretion called root exudate has a lot of potential from the perspective of defense. Root exudates possess antimicrobial chemicals, such as phytoanticipins, diterpene rhizathalene A, phytoalexins, phenylpropanoids, t‐cinnamic acids, momilacton A, rosmarinic acids, terpenoids, benzoxazinoids, and the defense signaling molecules, salicylic acid, nitric oxide, and methyl jasmonate, which assist in the defense mechanisms of the plant. In addition, these chemical phenolics and terpenoids act as an antimicrobial apart from defense root exudates, which support the stress condition of plants due to their primary and secondary metabolite present in root exudates (Table 1.2).
Plant root exudation indirectly controls resource competition by altering soil chemistry, soil process, and microbial populations, and thus has an important function in plant development. Root exudation possesses the capacity to alter the soil nutrient availability by changing the soil property in the aspect of its chemistry and biology. Root exudate releases mucilaginous substance from root tip of the plant and is a part of exudation quite essential to maintain the water potential (Susan 2018). Root exudate releases plant carbon compounds (border cells and exudates) and primary metabolites into the rhizospheric soil (Canarini et al. 2019). It is important to understand root‐mediated communication between plants and other organisms, which assists in the enhancement of agricultural production and can be useful in reduction in the demand for chemical fertilizer, such as in legume plants.
1.5 Conclusion and Future Prospects
Today's main concern of agriculture is the quality of productivity in order to feed the world population. For more production and protection of crops, farmers use chemicals that directly or indirectly effects the fertility of the soil as well as the consumers of the crop. To alleviate the chemical inputs in the agriculture requires detailed information about root exudation and its influence on plant development through soil condition modulation in terms of both biotic as well as abiotic components. Production of the crop depends on plant genotype and soil ecosystem. Root exudate is the key factor in the rhizospheric interaction due to nutrient assets. Researchers should emphasize root exudates, through profiling and their impact on microbes and soil in the rhizosphere for more exploration of root exudate. Still there are several unexplored chemicals of root exudates that can create magnificent changes in the soil and plants in terms of fertility, defense, growth, and yield. A few relevant and essential components of root exudates can be used for developing variety through genetic engineering and breeding, which assists in a sustainable agriculture system. Several chemical inducers should be explored, which increases the quantity of root exudates for better performance of the rhizosphere. In conclusional, in revealing root exudation secrets, we can support economical agricultural productivity through achievement of environmental sustainability.
Table 1.2 Developments in root exudate studies and their action mechanism.
S. No.
Root exudate component(s)
Plant system under study
Mechanism
References
1
Terpenoid class of compound: strigolactone
—
Recruitment of fungal species and establishment of Arbuscular mycorrhiza
Parniske (
2008
)
2
The isoflavones like daidzein, genistein, and coumestrol
Tribe Phaseoleae plants
Induces the nod gene expression in their rhizobial partners
Dakora (
2000
)
3
Sugars, sugar acids, amino acids and organic acids
Maize root
Effect of exudate components on the chemosensory systems of
Pseudomonas putida
KT2440
Lopez‐Farfan et al. (
2019
)
4
A class of indole‐derived plant chemical, benzoxazinoids
Cereal crops
Antifeedant, insecticidal, antimicrobial, and allelopathic activities are related with this exudate component
Wouters et al. (
2016
)
5
A phenolic compound luteolin
‐‐
Acts as a potent and specific inducer of
nodABC
gene expression in
Rhizobium meliloti
.
Caetano‐Anolles et al. (
1988
)
6
Catechol and flavonoids catechin, and quercetin
Maize (
Zea mays
L.)
Silicon‐induced amelioration of aluminum toxicity
Kidd et al. (
2001
)
7
Benzoxazinoids, secondary metabolites in grasses
Maize (
Zea mays
L.)
Effects the interaction between maize and
Pseudomonas putida
KT2440.
Neal et al. (
2012
)
8
Cyclic hydroxamates
Maize (
Zea mays
L.)
Mediate aluminum toxicity resistance in plant
Poschenrieder et al. (
2005
)
9
Benzoxazinoids, secondary metabolites in grasses
Maize (
Zea mays
L.)
Regulator of innate immunity against aphids and fungi
Ahmad et al. (
2005
)
10
Carotenoid‐derived strigolactones
Pea &
Arabidopsis
Involved in inhibition of shoot branching in plants
Gomez‐Roldan et al. (
2008
)
11
Soyasaponins
Soybean (
Glycine max
)
Regulates communication with beneficial microorganisms in soil
Tsuno et al. (
2018
)
12
Phytoestrogens
Clover legume
Male‐biased sex ratios and accelerates male metamorphic timing in wood frogs
Lambert (
2015
)
13
Phenol glycoside: rutin
Eucalyptus globulus ssp. bicostata
r
Regulate orientation of hyphal elongation toward the root tip, thereby favoring mycorrhizal infection
Lagrange et al. (
2001
)
14
Artificial root exudate having glucose, organic acids, and serine
—
These components of root exudate accelerate the degradation of pyrene in soil, especially glucose
Lu et al. (
2017
)
15
Organic acids
Legumes
Lotus corniculatus
L. and
Trifoliumarvense
L. and the grass
Calamagrostis epigeios
(L.)
Influence of these exudation components on plant nutrient acquisition
Boldt‐Burisch et al. (
2019
)
16
Root exudate components: proline and phytohormones
Citrus plants
Alleviation of abiotic stress conditions.
Vives‐Peris et al. (
2017
)
17
Root exudate components: proline and salicylates
Citrus plants
Recruitment of rhizobacteria and alleviation of abiotic stress conditions.
Vives‐Peris et al. (
2018
)
18
1‐alanine, 1‐proline and oxalic acid of root exudate
Sedum alfredii
Phytoremediation of lead contaminated soils
Luo et al. (
2017
)
19
Organic acids like malic, lactic, acetic, succinic, citric, and maleic acids in root exudates
Corn hybrids (
Zea mays
L.)
These exudate components might contribute to drought tolerance in corn hybrids
Song et al. (
2012
)
20
Organic acid exudates
White spruce (
Picea glauca
) and subalpine Fir (
Abieslasiocarpa
)
Significant role of exudate organic acids in the transformation of mica and chlorite into smectite in rhizospheric soils
Tuason and Arocena (
2009
)
21
Root exudate metabolome: primary and secondary metabolites
Quercus ilex
(holm oak)
Exudate components were changed irreversibly by the lack of water under extreme drought conditions
Gargallo‐Garriga et al. (
2018
)
22
Seed exudate: carbon and nitrogen contents
Chia (
Salvia hispanica
)
Plant exudates greatly affect the physical behavior of soil
Oleghe et al. (
2017
)
23
Exudate components like total free amino acids, proline, potassium, and some phytohormones
Barley (
Hordeum vulgare
L.)
Root exudate is an important factor in the context of crop performance and carbon balance under conditions of climate change
Olga et al. (
2017
)
24
Sakuranetin and sorgoleone of root exudate
Sorghum (
Sorghum bicolor
L.)
Biological nitrification inhibition activity
Subbarao et al. (
2013
)
25
1,9‐decanediol
Rice (
Oryza sativa
)
Blocks the ammonia monooxygenase pathway of ammonia oxidation and effects nitrogen use efficiency
Sun et al. (
2016
)
References
Abdel Lateif, K., Bogus, D., and Hocher, V. (2012). The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria.
Plant Signal. Behav.
7 (6): 636–641.
Ahmad, S., Veyrat, N., Gordon Weeks, R. et al. (2005). Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize.
Plant Physiol.
157 (1): 317–327.
https://doi.org/10.1104/pp.111.180224
.
Asao, T., Hasegawa, K., Sueda, Y. et al. (2003). Autotoxicity of root exudates from taro.
Sci. Hortic.
97: 389–396.
https://doi.org/10.1016/S0304‐4238(02)00197‐8
.
Badri, D.V. and Vivanco, J.M. (2009). Regulation and function of root excudates.
Plant Cell Environ.
32: 666–681.
Badri, D.V., Loyola‐Vargas, V.M., Broeckling, C.D. et al. (2008). Altered profile of secondary metabolites in the root exudates of
Arabidopsis
.
Plant Physiol.
146 (2): 762–771.
Bais, H.P., Walker, T.S., Schweizer, H.P., and Vivanco, J.M. (2002). Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of sweet basil (
Ocimumbasilicum
L.).
Plant Physiol. Biochem.
40: 983–995.
Bais, H.P., Prithiviraj, B., Jha, A.K. et al. (2005). Mediation of pathogen resistance by exudation of antimicrobials from roots.
Nature
434: 217–221.
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57: 233–266.
Boldt‐Burisch, K., Bernd, U., Annenaeth, M., and Fhüttl, R. (2019). Root exudation of organic acids of herbaceous pioneer plants and their growth in sterile and non‐sterile nutrient‐poor, sandy soils from post‐mining sites.
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Brigham, L.A., Michaels, P.J., and Flores, H.E. (1999). Cell‐specific production and antimicrobial activity of naphthoquinones in roots of
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.
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Caetano‐Anolles, G., Crist‐Estes, D.K., and Bauer, D.W. (1988). Chemotaxis of
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J. Bacteriol.
170: 3164–3169.
Canarini, A., Kaiser, C., Merchant, A. et al. (2019). Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli.
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.
Carlsen, S.C.K., Pedersen, H.A., Spliid, N.H., and Fomsgaard, I.S. (2012). Fate in soil of flavonoids released from white clover (
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Appl. Environ. Soil Sci.
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