Rhizosphere Biology: Interactions Between Microbes and Plants PDF

Rhizosphere Biology Vadakattu V. S. R. Gupta Anil K. Sharma Editors Rhizosphere Biology: Interactions Between Microbes and Plants Rhizosphere Biology Series Editor Anil K. Sharma Biological Sciences, CBSH, G. B. Pant University of Agriculture & Technology, Pantnagar, Uttarakhand, India The Series Rhizosphere Biology, emphasizes on the different aspects of Rhizo- sphere. Major increase in agricultural productivity, to meet growing food demands of human population is imperative, to survive in the future. Along with methods of crop improvement, an understanding of the rhizosphere biology, and the ways to manipulate it, could be an innovative strategy to deal with this demand of increasing productivity. This Series would provide comprehensive information for researchers, and encompass all aspects in ﬁeld of rhizosphere biology. It would comprise of topics ranging from the classical studies to the most advanced application being done in the ﬁeld. Rhizoshpere is a dynamic environment, and a series of processes take place to create a congenial environment for plant to grow and survive. There are factors which might hamper the growth of plants, resulting in productivity loss, but, the mechanisms are not very clear. Understanding the rhizosphere is needed, in order to create opportunities for researchers to come up with robust strategies to exploit the rhizosphere for sustainable agriculture. There are titles already available in the market in the broad area of rhizosphere biology, but there is a major lack of information as to the functions and future applications of this ﬁeld. These titles have not given all the up-to-date information required by the today’s researchers and therefore, this Series aims to ﬁll out those gaps. More information about this series at http://www.springer.com/series/15861 Vadakattu V. S. R. Gupta Anil K. Sharma Editors Rhizosphere Biology: Interactions Between Microbes and Plants Editors Vadakattu V. S. R. Gupta Anil K. Sharma Agriculture and Food, CSIRO Department of Biological Sciences Urrbrae, Australia CBSH, G.B. Pant University of Agriculture & Technology Pantnagar, Uttarakhand, India ISSN 2523-8442 ISSN 2523-8450 (electronic) Rhizosphere Biology ISBN 978-981-15-6124-5 ISBN 978-981-15-6125-2 (eBook) https://doi.org/10.1007/978-981-15-6125-2 # Springer Nature Singapore Pte Ltd. 2021 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 Rhizosphere plant–microbe interactions are diverse, spatially and temporally dynamic, inﬂuenced by plant, soil biophysical environment, and are critical to plant health and crop productivity. It is well established that bacteria and fungi around a plant's root in the rhizosphere, the miniature ecosystem around the root, can inﬂuence both the root's form and its physiology. The rhizosphere concept, coined in 1904 by Lorenz Hiltner about the roles of soil microorganisms in plant nutrition and health, has initiated a century-long research and discussion about organismic interactions between plants and microbes. More than 50 years ago, Dr Ralph Foster’s (CSIRO, Adelaide) electron micrographs revealed the intricate structure of rhizo- sphere, rhizoplane, and endosphere environments and the interplay between plant root, microﬂora, and protozoa. Rhizosphere microbiota provides a valuable potential resource of plant probiotic and growth-promoting functions capable of conjugating crop productivity within sustainable agricultural systems. It is, therefore, important to understand the dynamics of rhizosphere interactions in order to develop practical strategies that would help improving yield and maintain ecosystem health. During the last decade, there has been a renewed interest in exploring the dynamics of the rhizosphere, using omics tools, for its composition and organismal interactions occurring in the complex spatial structuring at the root–soil interface and their key drivers during the crop growth. Recent research has shown structural and functional diversiﬁcation of root-associated microbial communities of crop varieties, wild and domesticated accessions of barley, maize, canola, peas, and various Arabidopsis accessions, etc. Some of these ﬁndings also identiﬁed bacterial taxa which were positively correlated with crop performance or yield. This led to an intense effort to identify the plant-based traits that modulate the genetic structure and diversity, gene expression, and functional proﬁle from the outer realms of rhizo- sphere to inside the root. This new understanding has highlighted an attractive avenue that would help to better harness beneﬁcial outcomes from plant– microbiome interactions. This book is a compilation of the latest knowledge on plant and microbial aspects of rhizosphere biology covering different ecological, molecular, and biochemical characteristics of rhizosphere and endosphere interactions. It contains 15 chapters, each prepared by authors who are internationally recognized for their knowledge and v vi Preface expertise in a particular area of rhizosphere interactions. Additionally, it covers the cross-talk between plants and microbes including quorum-sensing signal molecules, plant interactions with abiotic factors, and potential ways rhizosphere microbial composition and functionality could be manipulated for enhanced and efﬁcient beneﬁts. The different chapters cover key areas such as (1) factors driving rhizo- sphere biology and interactions, (2) diversity of phenotypic and functional groups, (3) functional signiﬁcances of rhizosphere interactions, and (4) how best to manipu- late rhizosphere interactions. A special feature of the papers is that they highlight the beneﬁts of using the latest omics (metagenomics, transcriptomics, and proteomics) and isotopic tools in dissecting the plethora of mechanisms, genes, and metabolites involved in the multitrophic interactions. Endophytic bacteria, those that colonize the internal tissue of the plant showing no external sign of infection or negative effect on their host, have been found in all plants and form a range of relationships including symbiotic, mutualistic, commensalistic, and trophobiotic interactions. This type of plant microbiome is now considered as the second genome of the host plant and concepts such as “holobiont” comprising the plant with its endophytic microbiome as an extended phenotype and a uniﬁed system. In the chapter on bacterial endophytes, Tosi et al. (Chap. 1) present a comprehensive summary of the latest knowledge about the diversity and functions of bacterial (including actinobacteria) endophytes, their inﬂuence on plant ﬁtness, and the potential to manipulate their functions in agroecosystems. The presence of a taxonomic overlap between endophytic and rhizospheric communities and clear community shifts between these compartments conﬁrms the idea that rhizosphere is a key habitat regulating endophytic communities. Although soil type can have a major inﬂuence, strong and signiﬁcant host genotype effects on the diversity resulting in distinct taxonomic composition of endophytic bacteria have been shown with a variety of plants. However, the obser- vation of differential abundance, core microbiomes, new knowledge on the herita- bility of the speciﬁc taxa and their links to plant genotype through genome-wide association studies is needed in order to develop designer plant–microbiome combinations that maximize beneﬁcial functions. The involvement of root exudates as carbon and nutrient sources in modifying the rhizosphere microbial communities, as proposed by Albert Rovira more than 50 years ago, is now extended to include signal molecules and root architecture inﬂuencing the microbiome composition. In Chap. 9, Haichar and Achouak describe how newly introduced and modiﬁed genes in plants inﬂuence the quality and quantity of root exudates and in turn rhizosphere microbiome. It is increasingly becoming clear that the ability of soil microbes to colonize a particular plant species is fuelled and modulated by the release of signals by either or both partners and are only recognized by the right partner. Taking the knowledge from legume–rhizobia and plant–mycorrhizal symbioses, Antar et al. summarize (Chap. 13) the latest knowledge about the signals involved in other beneﬁcial plant–microbe interactions and microbe–microbe signal interactions. In spite of recent ﬁndings about the intricacies of rhizosphere interactions, the exact molecular mechanisms governing the complex root–soil–microbe interactions remain largely unknown. Balasubramanian et al. present (Chap. 14) a review of Preface vii what is known about the strategies for manipulating the rhizosphere region with a focus on engineering the root H+ efﬂux and organic anions, secondary metabolite composition of root exudates, alterations in root biomass accumulation, and below- ground carbon allocations for improved plant performance. The carbon inputs by plant roots not only provide the primary source of organic C into the soil modifying rhizosphere microbiome, but the chemical composition of exudates also strongly inﬂuences the metabolic potential of rhizosphere-enriched microbes along with mediating nutrient ﬂuxes in the rhizosphere. In Chap. 2, Pett- Ridge et al. provide evidence showing the downstream effects of rhizosphere dynamics on the colonization of nearby soil minerals, degradation of prior season’s root litter, and the balance of stabilized versus lost soil carbon. Furthermore, this study provides an excellent example illustrating the beneﬁts of using the latest genomic and isotopic techniques to unravel the mechanisms of C ﬂow between growing plant roots, soil microbial communities, and the surrounding mineral matrix. The beneﬁcial effects of these rhizosphere interactions on nutrient ﬂuxes and availabilities could also improve plant nutrition through increased nutrient use efﬁciency and, as discussed by Paterson and Mwafulirwa (Chap. 3), provide a realistic means of improving plant health and productivity while potentially also mitigating environmental impacts. Also, recent ﬁndings about the diazotrophic communities in the rhizosphere and endosphere in terms of their diversity and functional capacity have rejuvenated the old idea of harnessing the biological N ﬁxation in nonleguminous crops through manipulation of this speciﬁc functional group; the chapter by Roley (Chap. 4) presents the latest knowledge on this topic. The rhizobia-legume and mycorrhizae–plant interactions are two well-established examples of plant–microbe symbiosis with extensive research and knowledge about the mechanistic aspects of the beneﬁcial interactions. Recent research has shown that the interactions of “Arbuscular Mycorrhizal Fungi” (AMF), the obligate biotrophs, in the rhizosphere are not just restricted to host plant but involve bacteria in the rhizosphere and hyphosphere; Wang and Feng discussed (Chap. 11) new insights into interactions between AM fungi and other organisms in the rhizosphere. Plant health status affected by the presence of pathogens and root disease incidence could be a driver for change in the root microbiome as discussed in the chapter by Barnett (Chap. 8) and it was proposed that microsite-based variation between healthy and diseased niches in the root system could ultimately lead to the development of disease suppressive microbiomes; however, the exact mechanisms for such community changes remain elusive at present. Alternatively, plant–microbe interactions in the rhizosphere can have a signiﬁcant impact on plant health acting as the ﬁrst line of defense in the rhizosphere. Therefore, identiﬁcation of plant genetic traits involved in the recruitment of beneﬁcial microorganisms, i.e. promoting pro- biotic microbial community, would help improve plant defenses against biotic stresses; the chapter by Chiaramonte et al. (Chap. 7) discusses strategies and potential to explore this option through plant breeding programs. Plant root–biota associations in the rhizosphere involve complex networks and interactions between micro- and macroorganisms across multiple microsites and in intricate spatial structuring that can vary temporally during crop growth from viii Preface seedling to maturity. Recent evidence from genomic and transcriptomic studies clearly indicates that there is a strong association between rhizosphere development and taxonomic makeup including the succession in bacterial community in ﬁeld environments. This has been demonstrated for several crops including cereals, canola, cotton, and other crops (Richardson et al., Chap. 5). The major predators of microorganisms such as protists, faunal nematodes, and microarthropods can modulate the composition of rhizosphere microbiome through preferential feeding, with functional consequences in plant performance by affecting nutrient cycling, pathogen density, etc. (Geisen and Quest, Chap. 12). As rhizosphere food webs are not universally identical, the functional importance of microbial–faunal interactions is modulated by the soil habitat structure and management. The concept of succession in rhizosphere microbiome dynamics also leads to the idea of “legacy” in that the rhizosphere of crop leaves a footprint in the soil systems affecting the following crops. Since rhizosphere interactions involve modiﬁcations in soil physicochemical and biological components, the legacy effects should incor- porate physical, chemical, and biological effects that potentially endure beyond the root that created it. In the chapter by Oliver et al. (Chap. 6), they suggest that constraints of destructive sampling can be overcome from the recent advances in micro X-ray computed tomography, but it still requires other complementary techniques to determine the extent of the rhizosphere legacy. It was considered that the most effective form of manipulation of rhizosphere and endosphere microbiomes is through the use of beneﬁcial microorganisms, “bio- inoculants” either singly or as consortia for biocontrol to reduce or eliminate plant disease effects or effects of abiotic stresses such as from drought/water-stress or salinity effects. Through the use of latest omics tools (metagenomic, transcriptomics, and metabolomics), it is now possible to describe in-depth the networks of members of rhizosphere microbiomes including the effects of introducing inoculants as well as identifying mechanisms to manipulate and engineer microbiomes (Franco, Chap. 15). For example, recent evidence suggests that rhizobacteria with the capac- ity to produce ACC deaminase can initiate a cascade of changes in plant physiologi- cal and biochemical responses resulting in increased tolerance to abiotic stresses in a broad range of plant species (Sharma et al., Chap. 10). As a result of fast-changing global climate scenario with predictions for reduced rainfall and increased effects of other abiotic stresses across many agricultural regions worldwide, exploitation of such beneﬁcial plant–microbe interactions to alleviate abiotic stress effects in crops should be one of the key approaches to promote resilience and improve global food production. A majority of the recent research on the makeup and dynamics of rhizosphere microbiome until now has concentrated on taxonomic/phylogenetic makeup of the microbiome mainly about who is present and variations with plant type, management, and soil environment. In view of the extensive diversity and the dynamic spatial and temporal structure of the microbiome, interpretation and extrapolation of variations in phylogenetic makeup in terms of their functional potential and resilience have been found to be not straightforward. Hence future research on plant-trait based microbiome interactions requires investigations targeting speciﬁc functional groups associated with key Preface ix plant traits to help with the development of management interventions that can improve productivity in agricultural systems. Through a combination of genomic, transcriptomic, and isotopic tools, it should be possible to directly follow the dynamics of speciﬁc microbial functional group and link it with associated func- tional ﬂuxes. Such research would facilitate the identiﬁcation of key drivers from plant, microbial, and process perspectives, thereby assisting in the development of new designer plant holobionts that utilize native soil microbiome through next- generation crop breeding, “syncoms” or synthetic communities and management practices for sustainable and resilient food production systems. Urrbrae, Australia Vadakattu V. S. R. Gupta Pantnagar, Uttarakhand, India Anil K. Sharma Acknowledgements With its complexity and diversity of life it hosts, the topic of rhizosphere attracts the interest of many disciplines. As the co-editors of this book, we acknowledge all the authors for preparing excellent summaries with thought provoking discussions on the various topics of rhizosphere interactions. We extend our sincere appreciation to the various reviewers of the manuscripts for their diligence in helping to improve the contributions. Ms. Ranjita Vadakattu provided invaluable help by providing logisti- cal support through the compilation and revision process keeping track of all the contributions. We also thank our parent organizations CSIRO Agriculture and Food in Australia and G.B. Pant University of Agriculture & Technology in India for their support to our participation in preparing this publication. xi Contents 1 Bacterial Endophytes: Diversity, Functional Importance, and Potential for Manipulation............................ 1 Micaela Tosi, Jonathan Gaiero, Nicola Linton, Tolulope Mafa-Attoye, Anibal Castillo, and Kari Dunﬁeld 2 Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant Interactions.............................. 51 Jennifer Pett-Ridge, Shengjing Shi, Katerina Estera-Molina, Erin Nuccio, Mengting Yuan, Ruud Rijkers, Tami Swenson, Kateryna Zhalnina, Trent Northen, Jizhong Zhou, and Mary K. Firestone 3 Root–Soil–Microbe Interactions Mediating Nutrient Fluxes in the Rhizosphere.......................................... 75 Eric Paterson and Lumbani Mwafulirwa 4 Diazotrophic Nitrogen Fixation in the Rhizosphere and Endosphere....................................... 93 Sarah S. Roley 5 Root Microbiome Structure and Microbial Succession in the Rhizosphere.......................................... 109 Alan E. Richardson, Akitomo Kawasaki, Leo M. Condron, Peter R. Ryan, and Vadakattu V. S. R. Gupta 6 Rhizosphere Legacy: Plant Root Interactions with the Soil and Its Biome............................................... 129 Ivanah C. Oliver, Oliver G. G. Knox, Richard J. Flavel, and Brian R. Wilson 7 Rhizosphere Microbiome and Soil-Borne Diseases............. 155 Josiane Barros Chiaramonte, Lucas William Mendes, and Rodrigo Mendes 8 Root Disease Impacts on Root-Rhizosphere Microbial Communities......................................... 169 Stephen Barnett xiii xiv Contents 9 Newly Introduced or Modiﬁed Genes in Plants Potentially Modulate the Host Microbiome........................... 185 Feth el Zahar Haichar and Wafa Achouak 10 Rhizosphere Plant–Microbe Interactions Under Abiotic Stress.... 195 Suvigya Sharma, Dinesh Chandra, and Anil K. Sharma 11 Arbuscular Mycorrhizal Fungi Interactions in the Rhizosphere... 217 Fei Wang and Gu Feng 12 Microbial–Faunal Interactions in the Rhizosphere............. 237 Stefan Geisen and Casper W. Quist 13 Inter-Organismal Signaling in the Rhizosphere............... 255 Mohammed Antar, Parghat Gopal, Levini Andrew Msimbira, Judith Naamala, Mahtab Nazari, William Overbeek, Rachel Backer, and Donald L. Smith 14 Molecular Mechanisms of Plant–Microbe Interactions in the Rhizosphere as Targets for Improving Plant Productivity....... 295 Vimal Kumar Balasubramanian, Christer Jansson, Scott E. Baker, and Amir H. Ahkami 15 Inoculation Effects in the Rhizosphere: Diversity and Function... 339 Christopher M. M. Franco Editors and Contributors About the Editors Vadakattu V. S. R. Gupta is a Senior Principal Research Scientist at the CSIRO Agriculture and Food unit at the Waite campus in Adelaide, South Australia. He has more than 20 years of experience in fundamental and applied, ﬁeld-based functional microbial ecology research in soil and water ecosystems in Australia, Canada, and India. His research interests include unraveling the complexities of microbial diver- sity, functional capability, and resilience of microbe–soil–plant interactions for disease suppression and plant nutrition as a key for developing sustainable agricul- tural systems. His research has identiﬁed changes in soil biology in genetically modiﬁed crop systems and the impacts of herbicides on soil biological functions. He has published over 100 refereed articles in scientiﬁc journals and books and developed soil biology research investment priorities for government and industry funding bodies in Australia. He was awarded the 2015 Prescott Medal by the Soil Science Society of Australia for his outstanding contribution to Soil Science. Anil K. Sharma is a Professor at the Department of Biological Sciences, CBSH G.B. Pant University of Agriculture & Technology, Pantnagar. He was a Visiting Scientist at the University of Basel, Switzerland from July 2003 to November, 2003, and at the University of Helsinki, Finland in 2013. He completed his postdoctoral studies at GSU, Louisiana, USA, and he has extensive research and teaching experience. He is a reviewer for DBT, DST, and MOEF projects and for journals such as the Biocontrol Journal, International Journal of Agriculture, and Microbiol- ogy. He holds three patents in the ﬁeld of plant biology and microbiology and has received a number of prestigious grants. His laboratory is involved in various international collaborations, and he has published more than 84 research articles, 32 review articles, and two books with renowned publishers. He has presented his research on several internationally acclaimed platforms. xv xvi Editors and Contributors Contributors Wafa Achouak Aix Marseille Univ, CNRS, CEA, UMR 7265 BVME, LEMIRE, ECCOREV FR 3098, Saint-Paul-lez-Durance, France Amir H. Ahkami Environmental Molecular Sciences Laboratory (EMSL), Paciﬁc Northwest National Laboratory (PNNL), Richland, WA, USA Scott E. Baker Environmental Molecular Sciences Laboratory (EMSL), Paciﬁc Northwest National Laboratory (PNNL), Richland, WA, USA Vimal Kumar Balasubramanyam Environmental Molecular Sciences Laboratory (EMSL), Paciﬁc Northwest National Laboratory (PNNL), Richland, WA, USA Stephen Barnett Medical Biotechnology, Flinders University, Bedford Park, SA, Australia South Australian Research and Development Institute, Hartley Grove, Urrbrae, SA, Australia Anibal Castillo Environmental Microbiology of Agro-Ecosystems, School of Environmental Sciences, Guelph, ON, Canada Josiane Barros Chiaramonte Embrapa Meio Ambiente, Jaguariúna, SP, Brazil Leo Condron Faculty of Agriculture and Life Sciences, Lincoln University, Christchurch, New Zealand Kari Dunﬁeld Environmental Microbiology of Agro-Ecosystems, School of Envi- ronmental Sciences, Guelph, ON, Canada Feth el Zahar Haichar Univ Lyon, Université Claude Bernard Lyon 1, UMR CNRS 5557, Laboratoire d’Ecologie Microbienne, UMR INRA 1418, Villeurbanne Cedex, France Katerina Estera-Molina Department of Environmental Science, Policy and Man- agement, University of California, Berkeley, CA, USA Gu Feng College of Resources and Environmental Sciences, China Agricultural University, Beijing, People’s Republic of China Mary K. Firestone Department of Environmental Science, Policy and Manage- ment, University of California, Berkeley, CA, USA Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Livermore, CA, USA Richard J. Flavel Faculty of Science, Agriculture, Business and Law, School of Environmental and Rural Science, The University of New England, Armidale, NSW, Australia Chris Franco Medical Biotechnology, College of Medicine and Public Health, Flinders University, Bedford Park, SA, Australia Editors and Contributors xvii Jonathan Gaiero Environmental Microbiology of Agro-Ecosystems, School of Environmental Sciences, Guelph, ON, Canada Stefan Giesen Department of Terrestrial Ecology, Netherland Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands Christer Jansson Environmental Molecular Sciences Laboratory (EMSL), Paciﬁc Northwest National Laboratory (PNNL), Richland, WA, USA Akitomo Kawasaki CSIRO Agriculture and Food, Canberra, ACT, Australia Oliver G. G. Knox Faculty of Science, Agriculture, Business and Law, School of Environmental and Rural Science, The University of New England, Armidale, NSW, Australia Nicola Linton Environmental Microbiology of Agro-Ecosystems, School of Envi- ronmental Sciences, Guelph, ON, Canada Tolulope Mafa-Attoye Environmental Microbiology of Agro-Ecosystems, School of Environmental Sciences, Guelph, ON, Canada Lucas William Mendes Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, SP, Brazil Rodrigo Mendes Embrapa Meio Ambiente, Jaguariúna, SP, Brazil Lumbani Mwafulirwa The James Hutton Institute, Aberdeen, UK Global Academy of Agriculture and Food Security, University of Edinburgh, Midlothian, UK Department of Animal and Plant Sciences, University of Shefﬁeld, Shefﬁeld, UK Trent Northen Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA Erin Nuccio Physical and Life Sciences, Lawrence Livermore National Labora- tory, Livermore, CA, USA Ivanah C. Oliver Faculty of Science, Agriculture, Business and Law, School of Environmental and Rural Science, The University of New England, Armidale, NSW, Australia Eric Paterson The James Hutton Institute, Craigiebuckler, Aberdeen, UK Jennifer Pett-Ridge Physical and Life Sciences, Lawrence Livermore National Laboratory, Livermore, CA, USA Casper W. Quist Department of Terrestrial Ecology, Netherland Institute of Ecol- ogy (NIOO-KNAW) and Laboratory of Nematology, Wageningen University and Research Centre (WUR), Wageningen, The Netherlands Alan E. Richardson CSIRO Agriculture and Food, Canberra, ACT, Australia xviii Editors and Contributors Ruud Rijkers Systems Ecology, Department of Ecological Science, VU Univer- sity, Amsterdam, Netherlands Sarah S. Roley School of the Environment, Washington State University, Richland, WA, USA Peter R. Ryan CSIRO Agriculture and Food, Canberra, ACT, Australia Dinesh Sharma Department of Biological Sciences, CBSH, G.B. Pant University of Agriculture & Technology, Pantnagar, India Suvigya Sharma Department of Biological Sciences, CBSH, G.B. Pant University of Agriculture & Technology, Pantnagar, India Shengjing Shi Science Center, AgResearch Ltd., Christchurch, New Zealand Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA Tami Swenson Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA Micaela Tosi Environmental Microbiology of Agro-Ecosystems, School of Envi- ronmental Sciences, Guelph, ON, Canada Fei Wang School of Resource and Environmental Sciences, Henan Institute of Science and Technology, Xinxiang, People’s Republic of China Brian R. Wilson Faculty of Science, Agriculture, Business and Law, School of Environmental and Rural Science, The University of New England, Armidale, NSW, Australia NSW Ofﬁce of Environment and Heritage, University of New England, Armidale, NSW, Australia Mengting Yuan Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA Kateryna Zhalnina Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Livermore, CA, USA Jizhong Zhou Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Livermore, CA, USA Institute for Environmental Genomics, Department of Microbiology and Plant Science, University of Oklahoma, Norman, OK, USA Bacterial Endophytes: Diversity, Functional Importance, and Potential for Manipulation 1 Micaela Tosi, Jonathan Gaiero, Nicola Linton, Tolulope Mafa-Attoye, Anibal Castillo, and Kari Dunfield Abstract Even though beneﬁcial plant–microbe relationships have been studied for over one century, the recognition of a complex microbiome inhabiting the plant is relatively recent and reveals new opportunities for manipulating plant growth and health. Endophytes, commonly deﬁned as non-pathogenic microorganisms inhabiting the plant interior, constitute an important component of the plant microbiome. Speciﬁcally, bacterial endophytes gained research interest only in the past decades, due to their role in plant-growth promotion and their potential use in agriculture. New research is continuously published in this topic, with increasing sophistication provided by new technologies such as omics. For this reason, this chapter aimed to summarize current knowledge on bacterial endophytes focusing on three major aspects: (1) current knowledge on their bacterial endophytic diversity and regulation by plant and soil factors, (2) func- tional aspects of bacterial endophytes and available tools to study them, and (3) role of bacterial endophytes on plant ﬁtness and potential manipulation tools in agroecosystems. To ﬁt the scope of this book, which is the rhizosphere, the chapter focused on soil-borne facultative endophytes, even though we acknowl- edge the relevance of obligate vertically transmitted endophytes. M. Tosi · J. Gaiero · N. Linton · T. Mafa-Attoye · A. Castillo · K. Dunﬁeld (*) Environmental Microbiology of Agro-Ecosystems, School of Environmental Sciences, Alexander Hall, Guelph, ON, Canada e-mail: dunﬁ[email protected] # Springer Nature Singapore Pte Ltd. 2021 1 V. V. S. R. Gupta, A. K. Sharma (eds.), Rhizosphere Biology: Interactions Between Microbes and Plants, Rhizosphere Biology, https://doi.org/10.1007/978-981-15-6125-2_1 2 M. Tosi et al. 1.1 Bacterial Endophytes: Definition, Classification, and Scope of this Chapter Research on bacterial endophytes began growing exponentially in the late twentieth century, mostly fueled by an interest on their role in plant-growth promotion and potential application in agriculture (Turner et al. 1993; Hallmann et al. 1997; Sturz et al. 2000). The term endophytic was applied to microorganisms that could colonize internal tissues of a plant locally or systemically, residing there latently or actively for at least part of their lifetime without causing damage (i.e., commensal or mutualistic relationships) (Wilson 1995; Hallmann et al. 1997). Later ﬁndings reported microbial species with both a pathogenic and a beneﬁcial life form in the plant (Kogel et al. 2006), making this deﬁnition controversial and giving birth to a new notion where these categories are extremes in an operational continuum instead of two deﬁned groups (Schulz and Boyle 2005; Partida-Martínez and Heil 2011). To what extent this versatility is widespread is still uncertain, therefore, here we exclusively refer to endophytes as those non-pathogenic microorganisms inhabiting the plant interior. Isolating organisms from the plant interior from those inhabiting plant surfaces, such as the rhizoplane or the phyllosphere, is a challenging step. Typically, plant tissues are surface-sterilized before isolation or nucleic acid extrac- tion but, to date, no standardized methods have been deﬁned for different plant species or tissue types, despite the fact that the chosen methodology can strongly affect the results (Reinhold-Hurek and Hurek 2011) (See Box 1.1). Some beneﬁcial plant–microbe relationships have been studied for more than a century, as is the case for mycorrhizal fungi (Frank 1885), rhizobia–legumes (Beijerinck 1888), and Frankia–actinorhizal plants (Bottomley 1911). However, these studies were focused on just those few known associations, and they were mostly approached as one-to-one interactions between a microorganism and a host plant. It was in the last decades that most endophyte research switched to a community approach, acknowledging the different microorganisms that co-exist, as well as the interactions that occur between them and with the host plant (Andreote et al. 2009; Bulgarelli et al. 2013; Gaiero et al. 2013). New technologies like DNA proﬁling and sequencing became key in unraveling the complexity of endophytic microbial communities and, nowadays, the increasing number of beneﬁcial traits found suggests that a microbe-free plant would hardly survive under natural conditions (Partida-Martínez and Heil 2011). Endophytic communities are such an essential piece of plant ﬁtness that some authors are considering them the second genome of a plant host, where plant and microbiome work as a meta-organism (Lakshmanan et al. 2014). Similar concepts are now widespread in the literature, like “extended phenotype” (Partida-Martínez and Heil 2011) or “holobiont,” comprising the host organism with its symbiotic microbiome (Vandenkoornhuyse et al. 2015). This change of perspective is in synchrony with animal health, where researchers are also recognizing the host and its microbiome as a uniﬁed system (Ramírez-Puebla et al. 2013). Bacterial endophytes are usually classiﬁed based on their life strategies: while some of them are considered obligate, which means they need the host plant to fulﬁll 1 Bacterial Endophytes: Diversity, Functional Importance, and Potential for... 3 their life cycle, others are known as facultative for having a free-living phase in the soil (Hardoim et al. 2008, 2015). These authors also introduced the categories of opportunistic endophytes, as those who thrive as epiphytic but sporadically enter the plant, and passenger or passive endophytes, who enter and inhabit the plant without actively seeking to colonize it (Hardoim et al. 2015). Different life strategies are usually associated with different degrees of dependency with the host plant. Facul- tative endophytes must colonize the plant from the rhizosphere, for which they will probably go through a mutual signaling phase to then enter through root cracks or wounds, germinating radicles, emerging root hairs, among others (Reinhold-Hurek and Hurek 2011; Santoyo et al. 2016). Obligate endophytes, on the other hand, are thought to be transmitted vertically, via seed (Hardoim et al. 2008; Truyens et al. 2015). Bacterial endophytes can inhabit multiple tissues (e.g., roots, stems, leaves, ﬂowers, fruits, seeds, vascular tissues), their communities ﬂuctuate with plant development, and they carry out many functions that could potentially regulate growth and development of the host plant during its whole lifecycle. These effects could begin as early as seed establishment, as was shown by their indispensable role in primary colonization and rock-dwelling by some cacti species (Puente et al. 2009). Continually, more and more complex interactions are being unmasked, from non-rhizobia bacteria inhabiting legume nodules with the potential for hori- zontal gene transfer (HGT) (Li et al. 2008) to endophytic fungi hosting symbiotic bacteria (Lackner et al. 2009; Desirò et al. 2015). There is much we do not know about their assembly rules, distribution in the bulk soil-rhizosphere-endosphere continuum, or effects on plant ﬁtness, but past research on widely studied endosymbionts and phytopathogens can act as a useful reference for future studies (Sasse et al. 2018). According to the review by Partida-Martínez and Heil (2011), a key question is how endophytes affect plant physiology, ecology, and, in the long term, evolution. If endophytes can shape the plant’s response to multiple biotic and abiotic factors, and if they can be transmitted from generation to generation, they will most probably affect population dynamics and ecological interactions such as competition, herbiv- ory, or pollination (Friesen et al. 2011). In fact, Friesen et al. (2011) stated that the large populations and short generation times of microorganisms would allow trait mediation to evolve on an ecological time scale. Although the effects of bacterial endophytes at the plant community and ecosystem level are still understudied, with most studies carried out on single plants or monocultures, there is increasing interest in their impact beyond the individual plant level (van der Heijden et al. 2016). For instance, synergistic effects on plant biomass and diversity could be expected from the interaction between different groups of symbionts, likely with outcomes affect- ing ecosystem functioning (van der Heijden et al. 2008, 2016). Most certainly, these complex communities inhabiting plants have major implications in agroecosystems, as they are widespread in grain, pasture, horticultural, ﬂoral, and forestry crops (Baldan et al. 2014). It is also possible that plant breeding has inadvertently modiﬁed the microbiome of wild ancestors, which was probably more adapted to marginal soils (Wissuwa et al. 2009; Bulgarelli et al. 2013). But bacterial endophytes are not only important for their impact on plant and ecosystem functioning; they also 4 M. Tosi et al. constitute a source of novel metabolites to be applied in medicine or industry (Strobel 2003; Smith et al. 2008). A promising aspect for bioengineering is in their capacity to synthesize, at a higher rate, biologically active substances analogous to those synthesized by the host plant (Gunatilaka 2006; Wang and Dai 2011). Box 1.1 Methodological Constraints in DNA Analyses of Bacterial Endophytes Despite great improvements in the last decades, the study of bacterial endophytes still faces many methodological challenges and inconsistencies that need to be solved to validate and consolidate different ﬁndings. Many reviews are discussing the potential and the ﬂaws of studying and manipulating bacterial endophytes, but we still lack standardized methodologies to unify these research efforts. During our literature review, we could identify different areas in need of a critical methodological revision, testing, and development of a standardized protocol. The work by Richter- Heitmann et al. (2016) constitutes a useful approach to understanding the effectivity and risks attached to different endosphere isolation methods, while it evidences the variability resulting from root morphology traits. Surface-sterilization. Sodium hypochlorite (NaClO) is the most commonly used agent. Usually, a pre- or post-NaClO treatment with ethanol (70 or 95%) is done to improve penetration and sterilization, although it was suggested it could lead to contraction of the plant tissues (Sieber 2002). For optimal results, concentration, exposure time, and agitation should be tested for different plant species and growth stages (Hallmann et al. 2006). Underexposure to NaClO leads to contamination with surface-dwelling microbes and ampliﬁable DNA (Reinhold-Hurek and Hurek 2011), but overexposure can damage endophytes (Lundberg et al. 2012). Since residual NaClO can cause DNA mutations and artifacts, we must rinse several times with sterile water, and some authors also included a sodium thiosulfate rinse (Rosenblueth and Martínez-Romero 2004; Pereira et al. 2011). Alternative sterilizing agents, like propylene oxide vapor, hydrogen peroxide, or formaldehyde, are less commonly used (Hallmann et al. 2006; Nassar et al. 2005). Prior to chemical treatment, shaking with sterile glass beads (McClung et al. 1983; Reinhold et al. 1986; Sessitsch et al. 2012) or sonication can be used to physically remove microbes attached to the plant surface. Sonication has been used both complementary to surface disinfection (Conn and Franco 2004) or as the main removal procedure (Lundberg et al. 2012; Bulgarelli et al. 2012). Microscopy studies have shown that physical removal was less efﬁcient to remove rhizoplane microorganisms than NaClO (Richter-Heitmann et al. 2016; Reinhold-Hurek et al. 2015), while sonication in particular could cause root tissue damage (Richter-Heitmann et al. 2016). (continued) 1 Bacterial Endophytes: Diversity, Functional Importance, and Potential for... 5 Box 1.1 (continued) Sterilization control. Usually an aliquot of the last water rinse (or an imprint of the sterilized tissue) is incubated in a general culture medium (e.g., TSA or LB), either liquid or solid. Microbial growth (turbidity or colony growth) indicates incomplete removal of surface bacteria (Hallmann et al. 2006). Culture-dependent techniques might not be suitable if the study has a culture-independent approach, and alternative methods should be examined, like microscopy (Turner et al. 2013), PCR (Wemheuer et al. 2017), or sequencing DNA from the last water rinse, similarly to the “kitome” analysis carried out to check for contamination from DNA extraction kits (Kim et al. 2017; Salter et al. 2014). DNA extraction. Generally carried out directly from plant tissues, whole or ground in liquid nitrogen. On pre-extracted endophytic bacteria, it may over- come some issues of target speciﬁcity due to the large amount of plant material (Sessitsch et al. 2012). Extraction methods differ in cell lysis efﬁciency and removal of PCR inhibitors, biasing downstream analyses, and diversity estimations. Hence, when comparing endophytic and soil microbial communities, there is a compromise between optimizing the procedure for each sample type or treating all samples equally, for example, by using only soil DNA extraction kits (Bulgarelli et al. 2012). Finally, there may exist a trade-off between increased reproducibility and total yield of endophytic diversity, as found when comparing commercial kits and SDS- or CTAB- based DNA extraction tests (Maropola et al. 2015). Downstream target speciﬁcity. Ideally, PCR primers would cover all target taxa but, as we know, modiﬁcations and optimizations are continually made even for the highly conserved bacterial 16S rRNA gene (Caporaso et al. 2012). Another common issue is the co-ampliﬁcation of non-target DNA (e.g., chloroplasts, mitochondria), since samples will have a high ratio of plant DNA relative to bacterial DNA. Several studies have compared the utility of many bacterial 16S primers for use in endosphere microbiome research (Beckers et al. 2016; Dorn-In et al. 2015; Thijs et al. 2017; Klindworth et al. 2013); 799F-1391R, 335F-769R, and 341F-785R have been suggested due to their high coverage of the domain Bacteria. Relic DNA is often discussed as a potential source of variation in soil microbial diversity analyses, since it may persist for months or years (Carini et al. 2017), but its impact is still contro- versial (Lennon et al. 2018) and, to our knowledge, it has not been explored in the endosphere. However, propidium monoazide may be used to remove contaminating DNA on the root surface, such as from dead microbial cells (Leff et al. 2017). Understanding the limitations. Even though bacterial endophytes were initially deﬁned as those who could be isolated from surface-sterilized plant tissues, complete removal of surface microbes is challenging. Ideally, (continued) 6 M. Tosi et al. Box 1.1 (continued) improved and standardized surface-sterilization alternatives should be devel- oped. But when sterilization is not feasible, and depending on the purposes of the study, less rigid concepts might be more suitable, like root-associated or tightly bound bacteria (Lundberg et al. 2012; Donn et al. 2015). In this chapter, we will discuss current knowledge and prospects on the diversity and function of bacterial endophytes, their inﬂuence on plant ﬁtness, and their potential to be manipulated in agroecosystems. The unique symbiotic relationship between legumes and nodulating N-ﬁxing rhizobia, sometimes excluded from the group of endophytic bacteria (Partida-Martínez and Heil 2011), will be mentioned in some examples but detailed information can be found within the large body of published literature (e.g., Poole et al. 2018; Wang et al. 2018). Since this book is mostly dedicated to rhizospheric processes, we emphasize soil-borne facultative endophytes. Obligate endophytes may have a strong inﬂuence on plant functioning due to their dependency on their host for survival and reproduction, and that they represent an interesting tool for manipulation, since they are transferred between plant generations via seed (Sachs et al. 2004; Friesen et al. 2011). However, for their distinct behavior and the need to ﬁt the scope of this book, we considered that they deserved a separate analysis. We will also purposely overlook bacteria inhabiting plant surfaces, like the phyllosphere and the rhizoplane, although their inﬂuence should not be neglected. Surface-inhabiting communities were shown to affect plant functioning (Oh et al. 2012; Vorholt 2012) and they might be intimately related to the endosphere (Hardoim et al. 2008). 1.2 Diversity of Bacterial Endophytes: What Do We Know? Studies of bacterial endophytes began with simple systems of one-to-one microbe– host interactions, mostly using traditional techniques like isolation, culturing in synthetic media, and in vitro testing of morphological and physiological features. Many bacterial species have been isolated from different plant tissues and species, as reviewed previously (Hallmann et al. 1997; Sturz et al. 2000; Rosenblueth and Martínez-Romero 2006). Although culturing techniques provide some advantages, like working with isolated strains or working in a controlled environment, they are not amenable to studying the large diversity present in natural environments. In fact, many studies were able to capture more diversity with culture-independent than culture-dependent methods (Araújo et al. 2002; Conn and Franco 2004; Pereira et al. 2011; Qin et al. 2012). While for soils it is estimated that only about 0.001–1% of the microorganisms can be grown in synthetic media (Torsvik and Øvreås 2002), this percentage is unknown for endophytes. Yet, the review by Finkel et al. (2017) stated that the endophytic community encompasses a relatively higher percentage of culturable microorganisms. Supporting this idea, Le Cocq et al. (2017) established 1 Bacterial Endophytes: Diversity, Functional Importance, and Potential for... 7 that, compared to soil microorganisms, most endophytes are fast-growing, with a rapid response to nutrient and carbon substrate availability, thus amenable to culture- based work. So far, a complementary application of culture-dependent and -inde- pendent methods, together with an improvement of culturing techniques to capture a higher proportion of the actual diversity (Alain and Querellou 2009; Fierer 2017), seems to be a promising approach for exploring endophytic communities. High-throughput culture-independent methods improved data acquisition, boosting our knowledge of endophytic communities and their ubiquity. First attempts to characterize endophytic bacterial diversity with culture-independent methods were carried out with proﬁling techniques such as terminal restriction fragment length polymorphism analysis (T-RFLP) and denaturing gradient gel electrophoresis (DGGE) (e.g., Conn and Franco 2004; Seghers et al. 2004; Andreote et al. 2009). More advanced technologies like next-generation sequencing (NGS) allowed more insight into the composition of endophytic communities. For instance, bacteria seem to be the dominant and most ubiquitous taxonomic group in the endosphere, followed by fungi and then, if present, archaea (Hardoim et al. 2015; Krishnaraj and Pasha 2017; Kroll et al. 2017). Studies show that only a few bacterial phyla are consistently dominant (Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes), with higher variability at lower taxonomic resolution levels (Bai et al. 2015; Santoyo et al. 2016; Kroll et al. 2017; Liu et al. 2017a). According to a curated database analyzed by Hardoim et al. (2015), these four phyla comprised ~96% of the total prokaryotic sequences consisting of 21 bacterial and 2 archaeal phyla. These authors reported that Proteobacteria was the most dominant group (54%, and Gammaproteobacteria being the most dominant class), followed by Actinobacteria (20%), Firmicutes (16%), and Bacteroidetes (6%). Bacterial phyla found to have a low abundance in the endosphere are Acidobacteria, Planctomycetes, Verrucomicrobia, and Gemmatimonadetes (Hardoim et al. 2015; Santoyo et al. 2016; Liu et al. 2017a). Several research papers whereby endophytic bacterial communities were analyzed using DNA sequencing studies are listed in the reviews by Bulgarelli et al. (2013) and Liu et al. (2017a). Archaeal phyla have also been detected in plant tissues (Euryarchaeota, Crenarchaeota, and Thaumarchaeota), although they are usually present in low abundance (e.g., 1.96 indicate signiﬁcant phylogenetic clustering) (Vamosi et al. 2009) Catenulispora appeared to prefer the rhizosphere to background soil. Overall, positive and negative responses to the root were phylogenetically clustered based on the net relatedness index (NRI) and nearest taxon index (NTI) (Webb et al. 2002), which likely reﬂect the phylogenetic evenness and clustering within community data. In this study, both indices were signiﬁcantly positive at all time points (NRI, NTI 1.96), indicating clustering within both deep (NRI) and shallow (NTI) 2 Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant... 59 Fig. 2.4 The diversity in bulk soil and rhizosphere microbial community associated with A. fatua are indicated by (a) OTU richness and (b) phylogenetic diversity (a measure of biodiversity which incorporates the phylogenetic differences between species) in rhizosphere and bulk soils across the stages of plant growth. Data are presented as mean standard errors (n ¼ 16). The P values calculated using ANOVA are shown in each ﬁgure. Data based on the large phylogenetic tree (Fig. 2.3) were used to calculate phylogenetic diversity (Faith’s PD) using the generalized time reversible model in FastTree with a gamma branch-length correction (Price et al. 2010). The tree topology was constrained using a smaller tree composed of representatives for each family, where an OTU with a closely related full-length 16S sequence (97% similar) was selected for each family in the dataset (Nuccio et al. 2016). Faith’s PD was calculated using alpha_diversity.py (QIIME 1.5dev) for the rhizosphere and bulk soils at weeks 0 (bulk only), 3, 6, 9, and 12 branches of the phylogenetic tree (Vamosi et al. 2009). Both the Shi et al. (2015) study and the Nuccio et al. (2016) study suggest that this phylogenetic coherence between the net positive and net negative root responses indicates an evolutionary adaptation of soil bacteria and the development of traits in individual populations that confer rhizosphere competence. Community ecological factors, such as community assembly, diversity, and interactions, may also be affected by the growth of plant roots. In our studies of Avena spp., we have found that rhizosphere bacterial community assembly coincides with increases in network size and complexity, and a concurrent decrease in richness and diversity (Shi et al. 2016). The positive change in bacterial co-occurrence network complexity indicates that root growth may progressively stimulate interactions within microbial communities or induce the development of shared niches as a plant matures (Shi et al. 2016). We saw some evidence for such interactions in our early Avena spp. studies, which suggest that co-occurring groups (modules) of Alphaproteobacteria interact via quorum signaling with homoserine lactone compounds near mature (12-week-old) roots (DeAngelis et al. 2007). Decreasing bacterial diversity over time with root growth is not surprising; if certain members of an assemblage increase in dominance and a constant mass of DNA is sampled, then the traditional richness (and diversity indices) will decline (Fig. 2.4). Overall, our research using the Avena spp. “wild model” system indicates that rhizosphere microbiomes change in composition, function, and responses to plant exudates as plants mature (Bird et al. 2011; Shi et al. 2015; Zhalnina et al. 2018), 60 J. Pett-Ridge et al. with increasing microbial network complexity, altered functional potential, and shifting viral–host linkages over time (DeAngelis et al. 2008; Shi et al. 2016; Nuccio et al. 2020; Starr et al. 2019). Together, these results imply that temporal changes in rhizosphere microbial composition and function may impact not only plant–microbe interactions but also the broader soil C cycle. 2.5 Role of Rhizosphere Communities in the Soil Carbon Cycle It is generally accepted that decomposition of plant litter is mediated by a succession of soil microbial populations (Sylvia et al. 2004); however, the mechanisms under- lying rhizosphere community succession and assembly, and their subsequent impact on C cycling are just beginning to be explored and connected. DeAngelis et al. (2009) showed that in the presence of Avena spp. roots, microbial community composition and C utilization patterns are signiﬁcantly different from those in bulk soil. Subsequent studies assessing the microbial capability to breakdown complex C and N sources (using chitinases and proteases) have demonstrated enhanced activity in the rhizosphere and spatial differences within root zones (DeAngelis et al. 2009; Shi et al. 2015, 2016). An analysis of homoserine lactone signals suggests that density-dependent regulation is partially responsible for the enhanced capacity of the Avena rhizosphere community to break down macromo- lecular compounds (DeAngelis et al. 2008). Proteomics analyses indicate that rhizosphere bacteria actively synthesize proteins associated with sugar transport and utilization (Pett-Ridge and Firestone 2017), while research on speciﬁc root exudates, such as oxalic acid, suggests that some exudates may promote carbon loss by liberating organic compounds from protective mineral associations (Clarholm et al. 2015; Keiluweit et al. 2015). Metatranscriptomic analyses of soil from the A. fatua rhizosphere and near decaying roots indicate the development of distinct carbohydrate depolymerization microbial guilds based on shared gene expression over time, and suggest that a succession of microbial functions occurs as individual roots are colonized, age, and decay (Nuccio et al. 2020). Finally, although little is known about the ecology of bacteriophages or viruses of fungi and other eukaryotes in soil, Starr et al. (2019) found signiﬁcant composition differences and temporal changes in both hosts and RNA viruses in a comparison of rhizosphere, decaying root and bulk soil habitats. Since viral replication can lead to host cell death and release of soluble carbon, virus-mediated lysis of bacterial and fungal cells may play a role in the redistribution of cellular debris and the ultimate fate of root-derived C. Taken together, these studies provide evidence that plant roots alter both resource availability and the ecology of soil microbial decomposers, and shape how plant C is processed. Several of our studies with Avena spp. speciﬁcally address how rhizosphere microbial communities mediate the conversion of plant root litter to either SOM or CO2. Using a broad-brush community characterization approach (13C PLFA- phospholipid fatty acid analysis), Bird et al. (2011) followed the decomposition of intact 13C-labeled Avena spp. roots for two subsequent growing periods after plant senescence. The 13C (originating as root carbon) was observed in a succession of 2 Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant... 61 microbial community components, and with time, different groups of soil organisms acted as the primary decomposers of the decaying root debris. The presence of actively growing root systems stimulated the movement of 13C into Gram-positive and Actinobacteria groups, which are known for their oxidative enzyme capacities (Waldrop and Firestone 2004). In a more recent study, Shi et al. (2018) followed the decomposition of 13C root litter in the presence of an active A. fatua rhizosphere over two growing seasons. In this study, growing roots suppressed the rate of root litter decomposition and signiﬁcantly affected the bacterial, archaeal, and fungal community composition. Ribosomal RNA gene copy numbers of these microbes were on average 20% higher in the presence of growing roots, affecting the relative abundance of at least nine bacterial phyla. Genetic potential measurements made with GeoChip functional gene arrays (He et al. 2007) showed that microbes living near plant roots had relatively more genes coding for low molecular weight compound degradation enzymes, whereas those from unplanted soil had relatively more macromolecular degradation genes (Shi et al. 2018). To evaluate how community structure, genetic potential, and environmental variables all interacted to control root litter decomposition, Shi et al. (2018) used a Mantel analysis to test for pair-wise correlations. The resulting model suggests that the primary impact of live roots on decomposition appears to result from an alteration of soil microbial functional gene proﬁles. In a third study on the interaction between growing roots, decaying roots, and soil microbial communities, Nuccio et al. (2020) extracted gene transcripts (metatranscriptomes) from soil near live and decaying roots in microcosms containing A. fatua. Focusing on Carbohydrate-Active Enzymes (CAZyme) func- tional domains and enzymes involved in the degradation of macromolecular plant compounds, Nuccio et al. used a genome-centric approach to show that carbohydrate depolymerization was carried out by a series of microbial guilds with distinct spatial and temporal response patterns in different soil habitats (rhizosphere and detritusphere). These microbial guilds appear to specialize in their use of the different substrates made available by roots of different ages and decomposition stages. While these root substrates—exudates, mucilage, root hairs, and root bio- mass—are the initial sources of C that enter belowground food webs, the microbial transformation of this C is what determines whether it is retained as SOM or is returned back to the atmosphere. 2.6 Role of Root Exudates About 30–60% of C assimilated by plants is transferred to roots (Lynch and Whipps 1990), and up to 50% is exuded into the rhizosphere in a range of forms (Table 2.1; van Dam and Bouwmeester (2016)). Many of the interactions between roots and the surrounding microbial community are accomplished through chemical communica- tion driven by root exudates. These interactions have been implicated in plant defense (Baetz and Martinoia 2014), nutrient acquisition (Khorassani et al. 2011), and the regulation of soil bacterial and fungal community composition (Broeckling et al. 2008; Haichar et al. 2008; Shi et al. 2011). However, the mechanisms that 62 J. Pett-Ridge et al. Table 2.1 Commonly detected exudates of A. barbata and A. fatua measured from hydroponically grown plants, seedlings, and rhizosphere soil Class Compound Source Sugars and derivatives α-D-glucosamine phosphate, arabinose, arbutin, E, S, (n ¼ 24) cellotetraose, D-threitol, fructose, galactonic acid, Zb galactose, glucose, inositol, lyxose, maltose, myoinositol, N-acetyl-D-mannosamine, neohesperidin, rhamnose, ribitol, ribose, sorbitol, sorbose, sucrose, threonic acid, xylitol, xylosea Carboxylic acids and 2-Hydroxybutyric acid, 3-hydroxy-3-methylglutaric acid, E, S, Z derivatives (n ¼ 12) α-ketoglutaric acid, cis-aconitic acid, fumaric acid, lactic acid, maleic acid, malic acid, malonic acid, oxalic acid, pyruvic acid, succinic acid Amino acids and 2-Aminoisobutyric acid, 5-aminovaleric acid, alanine, E, S, Z derivatives (n ¼ 30) arginine, asparagine, aspartic acid, cysteine, gamma- amino-n-butyric acid, glutamic acid, glycine, histidine, homoserine, isoleucine, L-citrulline, L-homoserine, L- hydroxyproline, L-pyroglutamic acid, leucine, lysine, methionine, N-acetylaspartic acid, ornithine, phenylalanine, proline, serine, threonine, tryptophan, tyrosine, valine Aromatic acids and 2,3-Dihydroxybenzoic acid, 3-dehydroshikimic acid, E, S, I, derivatives (n ¼ 15) 4-hydroxybenzoic acid, 4-hydroxyphenylpyruvic acid, Z benzoic acid, caffeic acid, cinnamic acid, ferulic acid, nicotinic acid, p-coumaric acid, phthalic acid, quinic acid, shikimic acid, syringic acid, vanillic acid Fatty acids and Adipic acid, arachidic acid, elaidic acid, lauric acid, E, S, Z derivatives (n ¼ 12) lignoceric acid, linoleic acid, methylhexadecanoic acid, oleic acid, palmitic acid, palmitoleic acid, pelargonic acid, stearic acid Sterols Cholesterol S Glycerol and derivatives Glycerol, glycerol-α-phosphate, glycerol-β-phosphate S (n ¼ 3) Nucleosides and Adenine, adenosine, cytidine, deoxyguanosine, guanine, E, S, Z nucleotides (n ¼ 12) guanosine, hypoxanthine, inosine, thymidine, uracil, uridine, xanthine Plant hormones (n ¼ 4) Abscisic acid, indole-3-acetic acid, jasmonic acid, Z salicylic acid Betaines (n ¼ 6) Betonicine, carnitine, choline, glycine betaine, Z stachydrine, trigonelline Miscellaneous (n ¼ 14) 1,2,4-Benzenetriol, acetol, biotin, butyrolactam, D- E, S, I, lyxosylamine, dehydroabietic acid, pantothenic acid, Z riboﬂavin, sinapyl alcohol, syringylaldehyde, taurine, thiamine, urea, vanillin a Exudates were measured by GC–MS, LC–MS, and/or high-performance liquid chromatography (HPLC) b E—Estera (2017); S—Shi (unpublished); I—Iannucci et al. (2012); Z—Zhalnina et al. (2018) 2 Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant... 63 underlie how root exudates inﬂuence microbe-mediated C cycling are complicated and difﬁcult to study within an intact soil matrix. For example, the increased concentration of labile soil C near roots has been shown to both stimulate and repress soil organic carbon mineralization (Kuzyakov et al. 2000; Fontaine et al. 2007), and some studies suggest that exudates are just as likely to persist within soil as root tissue carbon (Sokol et al. 2018). One speciﬁc complication is the highly complex nature of root exudate compounds, which vary with plant genotype, root maturity, and in response to environmental stimulations (Jones 1998). Another difﬁculty is accurate characterization of exudate chemical composition because of the large background signal contributed by soil and microbial components (Kuzyakov and Domanski 2000). Advances in sequencing approaches and high-resolution metabolite analysis have recently made it possible to measure direct links between speciﬁc exudate compounds and responses of speciﬁc microbial populations. It seems likely that the increased microbial activity and growth in the rhizosphere is fueled by root exudation patterns, which change in composition and abundance as plants grow. Our studies indicate that the chemical landscape of the Avena spp. rhizosphere, compris- ing osmolytes, fatty acids, senescence hormones, amino acids, sugars, and nucleotides (Table 2.1), changes during plant growth in a successional pattern (Fig. 2.5). Indeed, as community composition, richness, and microbe–microbe interactions are changing during the growth of an Avena plant, plant exudation proﬁles also shift in a remarkably similar manner (Fig. 2.5, Estera 2017). Recent studies have identiﬁed direct predictive links between plant exudate composition and rhizosphere microbiome. Zhalnina et al. (2018) used a combination of comparative genomics and liquid chromatography–mass spectrometry (LC–MS)/ MS exometabolite proﬁling of Avena root exudate consumption by sequenced bacterial isolates to show that developmental processes in A. barbata generated consistent patterns in root exudate composition. They showed that the chemical succession of Avena root exudates interacted with microbial metabolite substrate preferences (speciﬁcally for amino acids, osmolytes, and aromatics) that were predictable from the microbe’s genome sequences. They hypothesized that the combination of plant exudation traits and microbial substrate uptake traits interacted to yield the patterns of microbial community assembly observed in the rhizosphere of this annual grass. Nuccio et al. (2020) show that, around older roots (that have ceased producing exudates and may have begun to senesce), distinct microbial populations (e.g., Streptomycetaceae and Catenulisporales from Actinobacteria) begin to have high d-CAZy gene transcription, expressing many enzymes involved in cellulose and xylose breakdown. Thus, it appears that temporal changes in root exudates over time and space may be directly linked to the successional changes in the rhizosphere microbial community identiﬁed by Shi et al. (2015) and may be the key determinants of soil C turnover. 64 J. Pett-Ridge et al. Fig. 2.5 Plot of partial least squares discriminant analysis (PLS-DA) components 1 and 2 for metabolite samples collected over 9 weeks from a sterile plant growth experiment. Sterilized A. barbata seedlings were planted in sterile plant chambers (SPCs) with sterilized sand, and grown in either 400 ppm (ambient) or 700 ppm (elevated) CO2 conditions. The pore space of the SPCs were fully drained and refreshed with diluted Hoagland solution once a week. SPCs were sampled at weeks 1, 2, 3, 4, 6, and 9 for root exudate proﬁles analyzed via gas chromatography– mass spectrometry (GC–MS). Metabolite abundances of identiﬁed GC-MS peaks were then normalized and analyzed via PLS-DA and ANOVA. Data were normalized from root exudate samples from weeks 1, 2, 3, 4, 6, and 9. There was a signiﬁcant difference in the metabolic proﬁles over time, as plants grew, regardless of CO2 treatment. Colors represent the different time points at which the samples were collected and circles represent the individual samples collected. Components 1 and 2 account for 27.3% of the variance in the dataset and are signiﬁcant predictors of time. Ellipses indicate the 95% conﬁdence interval for each sample grouping (#1–#9) 2 Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant... 65 2.7 Effect of eCO2 and Root Exudates Elevated CO2 can promote higher rates of photosynthesis and increased allocation of C to roots and various soil C pools (Table 2.2). In Avena spp., eCO2 changes exudate composition and temporal patterns of exudation over time (Fig. 2.6). Hence eCO2 studies provide a unique opportunity to assess the effects of altered root exudation patterns on microbial community succession and function, and in turn, how these population dynamics inﬂuence C transformations and stabilization processes. eCO2 concentrations stimulate many plant responses and lead to higher rates of photosynthesis, increased belowground biomass production, and soil depo- sition of labile C (Hungate 1999; Liu et al. 2009; Phillips et al. 2011) as well as lower transpiration rates and potentially increased soil water content due to reduced stomatal conductance (Hungate 1999). Previous studies suggest that eCO2 dispro- portionately affects root-associated microbial communities compared to those in the surrounding bulk soil (Drigo et al. 2008, 2009, 2010), and appears to consistently increase fungal populations in rhizosphere soil (Carney et al. 2007; Cheng et al. 2012; Drigo et al. 2013). In one study, eCO2 increased both rhizosphere fungal populations and the activities of carbon decomposition enzymes, resulting in an overall loss of soil carbon (Carney et al. 2007). However, the effect of eCO2 on the temporal variation in soil and rhizosphere microbial communities, and the impact of eCO2 on plant–microbe interactions (Drigo et al. 2010, 2013) remain poorly understood. These interactions may inﬂu- ence plant growth and net primary productivity by altering beneﬁcial microbial colonization and/or pathogen infection. Therefore, it is important to examine the effect of eCO2 on the abundance, composition, and function of rhizosphere micro- bial communities over time; the integration of such information could greatly improve the predictions of rhizosphere-driven C cycling. From our research on Avena spp., we have found that plants grown under elevated (700 ppm) CO2 increased both C allocated belowground and the amount of root- Table 2.2 Root biomass and plant-derived soil carbon pools after growing Avena spp. for one season under eCO2 and ambient CO2 (aCO2) conditions in 13CO2 growth chambers Treatment aCO2-Planted eCO2-Planted P-value Root biomass (g) 0.57 0.03 0.88 0.10 0.039 Total belowground 13C 225.6 20.0 266.5 22.9 0.050 13 C soil excluding roots 101.1 12.9 153.1 18.1 0.035 13 C-fLF (μg C/g soil) 79.9 9.2 103.5 12.9 0.275 13 C-oLF (μg C/g soil) 4.9 1.0 7.5 1.6 0.192 13 C-HF (μg C/g soil) 68.2 8.6 112.5 12.7 0.001 Total belowground 13C is in μg 13C/g soil + roots. 13C soil excluding roots is in μg 13C/g soil. 13C associated with different soil fractions was measured by isotope ratio mass spectrometry (IRMS) following separation of soil into three fractions: free light fraction (fLF), occluded light fraction (oLF), and heavy fraction (HF), according to the established methods (Golchin et al. 1994; Bird et al. 2011). P values shown in bold indicate signiﬁcant changes between aCO2 and eCO2 treatments (P < 0.05). Data are presented as mean standard errors (n ¼ 8) 66 J. Pett-Ridge et al. Fig. 2.6 Heat maps and cluster trees of metabolites from a plant growth experiment where A. barbata was grown in sterile plant chambers (SPC). (a) Heat map of root exudate proﬁles using the top 25 metabolites that were most important in the projection of the plot from a partial least squares discriminant analysis (PLS-DA). Warm colors reﬂect a larger abundance of metabolites and cooler colors a decreased abundance. Heat maps and cluster trees were constructed using a Euclidean distance measure and ward clustering algorithm, respectively. Heat maps summarize the root exudate changes in each SPC sample over time. Speciﬁcally, root exudates produced during weeks 1, 2, and 3 have lower abundance that those produced during weeks 6 and 9. Conversely, some root exudates produced during weeks 6 and 9 are not produced during the earlier weeks of 1, 2, and 3. (b) Metabolite heat map and cluster tree showing autoscaled abundances for root exudates that are signiﬁcantly different between eCO2 and aCO2 treatments as analyzed by a two-way ANOVA and Tukey’s HSD (honestly signiﬁcant difference) with p < 0.05. Out of 125 different metabolites detected from root exudate samples, only 7 were signiﬁcantly different between the two CO2 treatments. Trees show the degree of similarity among metabolites based on Euclidean distance, and metabolites are clustered to minimize the sum of squares derived 13C in the mineral-associated fraction of soil (Table 2.2). The increase in C associated with the soil mineral fraction (“heavy fraction”) suggests a potential for increased stabilization of root C under eCO2. In addition, metabolites produced in 2 Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant... 67 early weeks of plant growth under eCO2 conditions clustered distinctly from later produced metabolites (Fig. 2.6). Since we observed that eCO2 both increased and decreased speciﬁc exudate components (Fig. 2.6), additional studies are needed to parse how these changes affect the long-term fate of plant-derived exudate C. 2.8 Role of Soil Moisture Previous studies have reported a signiﬁcant interaction between eCO2 and gravimet- ric soil moisture (as well as N and P availability), possibly due to enhanced plant growth (Hu et al. 1999, 2001). Such eCO2- and soil moisture-induced changes in C sources and soil microenvironments are likely to have a substantial inﬂuence on the composition and function of soil microbiota and consequently in mediating the ecosystem processes (e.g., C, N cycling) (Hungate et al. 1997; Cheng and Johnson 1998; Luo et al. 2006; Carney et al. 2007; Phillips et al. 2012). Actively transpiring roots can impact soil C cycling processes by altering nearby soil water content. Castanha et al. (2018) report that Avena spp. caused increased decomposition of soil root detritus early in the growing season, when soil moisture was relatively high; however, as soil moisture levels declined, the plants suppressed decomposition rates of soil litter. In studies of Avena spp. we have found (not surprisingly) that rhizosphere soils have consistently lower soil moisture than unplanted soils (Shi et al. 2018; Nuccio et al. 2020) and this affects the rate of litter decomposition in the root zone versus the surrounding soil. The presence of plant roots also signiﬁcantly increased the abundance of proV and proW, two common bacterial osmotic stress genes (He et al. 2007; Shi et al. 2018). Altered bacterial community composition and bacterial and fungal functional gene proﬁles also accompany reduced water in rhizosphere soils (Webb et al. 2002). In CA annual grassland soils where Avena spp. grow, we have found that bacteria and fungi are differentially sensitive to soil moisture; bacteria tend to be substantially more sensitive and responsive to soil moisture than fungi (Barnard et al. 2013). These results suggest that bacterial communities in the rhizosphere may be differentially affected by the water stresses common in Mediterranean climate grasslands, likely impairing their metabolic activities and leading to downstream impacts on decomposition rates and rhizosphere C cycling. 2.9 Downstream Effects on Soil Carbon Stocks and Fluxes Root-microbial dynamics have signiﬁcant “downstream” effects on the soil C cycle, altering the amount and types of organic matter that become associated with mineral surfaces (Shi et al. 2018; Whitman et al. 2018), which may persist for long timescales. These effects can be measured by the extent of colonization of nearby soil minerals, decomposition of a prior season’s root litter, and the balance of stabilized versus lost soil carbon. In a study where we incubated fresh minerals 68 J. Pett-Ridge et al. (quartz, ferrihydrite, kaolinite) in the presence of an active Avena spp. rhizosphere, we found that both the quantity and composition of mineral-associated SOM were largely a factor of mineralogy and the inﬂuences of nearby roots (Whitman et al. 2018; Neurath, unpublished data). We also found signiﬁcant differences in microbial community composition (16S rRNA and ITS) on different mineral types (Whitman et al. 2018). Because different microbial populations have different inherent eco- physiological traits (cell wall biochemistry, carbon use efﬁciency, growth rate) that can affect soil C persistence, the colonization patterns and habitat preferences of individual microbial populations may be foundational to the persistence of C entering soil via plant roots. 2.10 Conclusions Interactions between plants and soil microorganisms are of primary importance to terrestrial ecosystem functions and particularly C cycling. Drawing heavily on the results from a “wild model” system, the common grass Avena spp. (wild oat) grown in CA annual grassland soils where it is ubiquitous, we summarize the important aspects of root–microbial interactions that have been commonly underappreciated, and provide the rough outlines of a mechanistic roadmap for how plant root C enters microbial and mineralized soil pools. Most of the root C entering soils returns to the atmosphere as CO2, but a small portion becomes stabilized as longer-lived SOM. The actual path taken by each photosynthetically ﬁxed plant C atom is a result of its consumption and use by bacteria, archaea, fungi, and viruses that make up the rhizosphere microbiome. Our results suggest that the sum of soil microbial ecophys- iological traits (shaped by their phylogeny and deﬁned by their genomes and gene expression) predict the fate of root C in soils when interpreted in the physicochemi- cal soil–root environment. However, creating a predictive roadmap for the pathways taken by plant C as it enters the soil continues to be a long-term challenge for soil scientists. Acknowledgments This study is based on research supported by the US Department of Energy, Ofﬁce of Science, Ofﬁce of Biological and Environmental Research Genomic Science Program under Award Numbers DE-SC0014079, DE-SC0010570, and DE-SC0016247 to MKF. Part of this work was performed at the University of Oklahoma, funded by the DOE under UC-subcontract number 00008322. J. Pett-Ridge and E. Nuccio contributed under the auspices of the US Depart- ment of Energy at LLNL under Contract DE-AC52-07NA27344 and US DOE Genomics Science program awards SCW1039, SCW 1632, SCW1589, and SCW1421. The study performed at the Lawrence Berkeley National Laboratory was supported by the DOE, Ofﬁce of Science, Ofﬁce of Biological and Environmental Research through Contract No. DE-AC02-05CH11231. We thank the current and past members of the DOE Genomic Science Carbon Cycling “Cradle to Grave” research team for their support on the multiple projects conducted as part of this research. 2 Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant... 69 References Austin EE, Wickings K, McDaniel MD, Robertson GP, Grandy AS (2017) Cover crop root contributions to soil carbon in a no-till corn bioenergy cropping system. GCB Bioenergy 9:1252–1263 Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98 Barnard RL, Osborne CA, Firestone MK (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7:2229 Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18 Bird JA, Herman DJ, Firestone MK (2011) Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol Biochem 43:718–725 Blagodatskaya E, Blagodatsky S, Anderson T-H, Kuzyakov Y (2014) Microbial growth and carbon use efﬁciency in the rhizosphere and root-free soil. PLoS One 9:e93282 Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744 Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze- Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403 Canals RM, Herman DJ, Firestone MK (2003) How disturbance by fossorial mammals alters N cycling in a California annual grassland. Ecology 84:875–881 Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci 104:4990–4995 Castanha C, Zhu B, Pries CEH, Georgiou K, Torn MS (2018) The effects of heating, rhizosphere, and depth on root litter decomposition are mediated by soil moisture. Biogeochemistry 137:267–279 Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803 Cheng W, Johnson DW (1998) Elevated CO2, rhizosphere processes, and soil organic matter decomposition. Plant Soil 202:167–174 Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087 Chenu C, Stotzky G (2002) Interactions between microorganisms and soil particles: an overview. In: Huang PM, Bollag JM, Senesi N (eds) Interactions between soil particles and microorganisms and the impact on the terrestrial environment. Wiley, West Sussex, pp 161–179 Clarholm M, Skyllberg U, Rosling A (2015) Organic acid induced release of nutrients from metal- stabilized soil organic matter–the unbutton model. Soil Biol Biochem 84:168–176 Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–1618 Colombo C, Palumbo G, He JZ, Pinton R, Cesco S (2014) Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. J Soils Sediments 14:538–548 Davidson EA, Ishida FY, Nepstad DC (2004) Effects of an experimental drought on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest. Glob Chang Biol 10:718–730 DeAngelis KM, Ji P, Firestone MK, Lindow SE (2005) Two novel bacterial biosensors for detection of nitrate availability in the rhizosphere. Appl Environ Microbiol 71:8537–8547 DeAngelis KM, Firestone MK, Lindow SE (2007) Sensitive whole-cell biosensor suitable for detecting a variety of N-Acyl homoserine lactones in intact rhizosphere microbial communities. Appl Environ Microbiol 73:3724–3727 70 J. Pett-Ridge et al. DeAngelis KM, Lindow SE, Firestone MK (2008) Bacterial quorum sensing and nitrogen cycling in rhizosphere soil. FEMS Microbiol Ecol 66:197–207 DeAngelis KM, Brodie EL, DeSantis T, Andersen G, Lindow S, Firestone MK (2009) Selective progressive response of soil microbial community to wild oat. ISME J 3:168–178 Dignac MF, Bahri H, Rumpel C, Rasse DP, Bardoux G, Balesdent J, Girardin C, Chenu C, Mariotti A (2005) Carbon-13 natural abundance as a tool to study the dynamics of lignin monomers in soil: an appraisal at the Closeaux experimental ﬁeld (France). Geoderma 128:3–17 Donn S, Kirkegaard JA, Perera G, Richardson AE, Watt M (2015) Evolution of bacterial communities in the wheat crop rhizosphere. Environ Microbiol 17:610–621 Drigo B, Kowalchuk G, Veen J (2008) Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667–679 Drigo B, van Veen JA, Kowalchuk GA (2009) Speciﬁc rhizosphere bacterial and fungal groups respond differently to elevated atmospheric CO2. ISME J 3:1204–1217 Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ, Boschker HTS, Bodelier PLE, Whiteley AS, van Veen JA, Kowalchuk GA (2010) Shifting carbon ﬂow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci 107:10938–10942 Drigo B, Kowalchuk GA, Knapp BA, Pijl AS, Boschker HTS, van Veen JA (2013) Impacts of 3 years of elevated atmospheric CO2 on rhizosphere carbon ﬂow and microbial community dynamics. Glob Chang Biol 19:621–636 Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci 112:E911–E920 Estera K (2017) The characterization of Avena barbata exudates. M.S. thesis, Range Management Group, University of California, Berkeley Eviner VT, Firestone MK (2007) Mechanisms determining patterns of nutrient dynamics, in California Grasslands. In: Stromberg M, Corbin J, D'Antonio C (eds) California grasslands: ecology and management. University of California Press, Berkeley, CA, pp 94–106 Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA, Kramer MA, Phillips RP (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutri- ent cycles. Glob Chang Biol 21:2082–2094 Fontaine S, Barot S, Barre P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280 Gleixner G, Poirier N, Bol R, Balesdent J (2002) Molecular dynamics of organic matter in a cultivated soil. Org Geochem 33:357–366 Golchin A, Oades JM, Skjemstad JO, Clarke P (1994) Study of free and occluded particulate organic matter in soils by solid state 13C Cp/MAS NMR spectroscopy and scanning electron microscopy. Aust J Soil Res 32:285–309 Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon ﬂow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56 Haichar F e Z, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221 Hartman K, van der Heijden MG, Roussely-Provent V, Walser J-C, Schlaeppi K (2017) Deciphering composition and function of the root microbiome of a legume plant. Microbiome 5:2 Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985 Hawkes C, Belnap J, D’Antonio C, Firestone M (2006) Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses. Plant Soil 281:369–380 2 Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant... 71 Hawkes C, DeAngelis K, Firestone M (2007) Root interactions with soil microbial communities and processes. In: Cardon Z, Whitbeck J (eds) The rhizosphere: an ecological perspective. Academic Press, San Diego, pp 1–30 He Z, Gentry TJ, Schadt CW, Wu L, Liebich J, Chong SC, Huang Z, Wu W, Gu B, Jardine P, Criddle C, Zhou J (2007) GeoChip: a comprehensive microarray for investigating biogeochem- ical, ecological and environmental processes. ISME J 1:67–77 Herman D, Johnson KK, Jaeger CH, Schwartz E, Firestone MK (2006) Root inﬂuence on nitrogen mineralization and nitriﬁcation in Avena barbata rhizosphere soil. Soil Sci Soc Am J 70:1504–1511 Hu S, Firestone MK, Chapin FS (1999) Soil microbial feedbacks to atmospheric CO2 enrichment. Trends Ecol Evol 14:433–437 Hu S, Chapin Iii FS, Firestone MK, Field CB, Chiariello NR (2001) Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature 409:188 Hungate BA (1999) Ecosystem responses to rising atmospheric CO2: feedbacks through the nitrogen cycle. In: Luo Y, Mooney H (eds) Carbon dioxide and environmental stress. Academic Press, San Diego, pp 265–285 Hungate BA, Lund CP, Pearson HL, Chapin FS (1997) Elevated CO2 and nutrient addition after soil N cycling and N trace gas ﬂuxes with early season wet-up in a California annual grassland. Biogeochemistry 37:89–109 Iannucci A, Fragasso M, Platani C, Narducci A, Miullo V, Papa R (2012) Dynamics of release of allelochemical compounds from roots of wild oat (Avena fatua L.). Agrochimica 6:185–192 Jackson RB, Lajtha K, Crow SE, Hugelius G, Kramer MG, Piñeiro G (2017) The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu Rev Ecol Evol Syst 48:419–445 Jain SK, Marshall DR (1967) Population studies in predominantly self-pollinating species. X. variation in natural populations of Avena fatua and A. barbata. Am Nat 101:19–33 Jones DL (1998) Organic acids in the rhizosphere–a critical review. Plant Soil 205:25–44 Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323 Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5:588–595 Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464 Khorassani R, Hettwer U, Ratzinger A, Steingrobe B, Karlovsky P, Claassen N (2011) Citramalic acid and salicylic acid in sugar beet root exudates solubilize soil phosphorus. BMC Plant Biol 11:121 Kiem R, Kögel-Knabner I (2003) Contribution of lignin and polysaccharides to the refractory carbon pool in C-depleted arable soils. Soil Biol Biochem 35:101–118 Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162 Kolton M, Green SJ, Harel YM, Sela N, Elad Y, Cytryn E (2012) Draft genome sequence of Flavobacterium sp. strain F52, isolated from the rhizosphere of bell pepper (Capsicum annuum L. cv. Maccabi). J Bacteriol 194:5462–5463 Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review. J Plant Nutr Soil Sci 163:421–431 Kuzyakov Y, Friedel J, Stahr K (2000) Review of mechanisms and quantiﬁcation of priming effects. Soil Biol Biochem 32:1485–1498 Letunic I, Bork P (2011) Interactive tree of life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478 Li X, Rui J, Mao Y, Yannarell A, Mackie R (2014) Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biol Biochem 68:392–401 72 J. Pett-Ridge et al. Liu L, King JS, Booker FL, Giardina CP, Lee Allen H, Hu S (2009) Enhanced litter input rather than changes in litter chemistry drive soil carbon and nitrogen cycles under elevated CO2: a microcosm study. Glob Chang Biol 15:441–453 Luo Y, Hui D, Zhang D (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53–63 Lynch JM, Whipps JM (1990) Substrate ﬂow in the rhizosphere. Plant Soil 129:1–10 Madigan MT, Clark DP, Stahl D, Martinko JM (2010) Brock biology of microorganisms, 13th edn. Benjamin Cummings, San Francisco Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938 Nuccio EE, Anderson-Furgeson J, Estera KY, Pett-Ridge J, Valpine P, Brodie EL, Firestone MK (2016) Climate and edaphic controllers inﬂuence rhizosphere community assembly for a wild annual grass. Ecology 97:1307–1318 Nuccio EE, Starr E, Karaoz U, Brodie EL, Zhou J, Tringe S, Malstrom RR, Woyke T, Banﬁeld J, Firestone MK, Pett-Ridge J (2020) Niche differentiation is spatially and temporally regulated in the rhizosphere. ISME J 14:999–1014 Pérez-Jaramillo JE, Carrión VJ, Bosse M, Ferrão LF, de Hollander M, Garcia AA, Ramírez CA, Mendes R, Raaijmakers JM (2017) Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits. ISME J 11:2244 Pett-Ridge J, Firestone MK (2017) Using stable isotopes to explore root-microbe-mineral interactions in soil. Rhizosphere 3:244–253 Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194 Phillips RP, Meier IC, Bernhardt ES, Grandy AS, Wickings K, Finzi AC (2012) Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecol Lett 15:1042–1049 Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneﬁcial inﬂuences of plant growth-promoting rhizobacteria on nutrient acquisi- tion process. A review. Biol Fertil Soils 51:403–415 Price MN, Dehal PS, Arkin AP (2010) FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490 Rasse D, Rumpel C, Dignac M-F (2005) Is soil carbon mostly root carbon? Mechanisms for a speciﬁc stabilisation. Plant Soil 269:341–356 Schlaeppi K, Dombrowski N, Oter RG, van Themaat EVL, Schulze-Lefert P (2014) Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc Natl Acad Sci 111:585–592 Shi S, Richardson AE, O'Callaghan M, DeAngelis KM, Jones EE, Stewart A, Firestone MK, Condron LM (2011) Effects of selected root exudate components on soil bacterial communities. FEMS Microbiol Ecol 77:600–610 Shi S, Nuccio E, Herman DJ, Rijkers R, Estera K, Li J, da Rocha UN, He Z, Pett-Ridge J, Brodie EL, Zhou J, Firestone M (2015) Successional trajectories of rhizosphere bacterial communities over consecutive seasons. MBio 6:e00746-00715 Shi S, Nuccio EE, He Z, Zhou J, Firestone MK (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19:926–936 Shi S, Herman DJ, He Z, Pett-Ridge J, Wu L, Zhou J, Firestone MK (2018) Plant roots alter microbial functional genes supporting root litter decomposition. Soil Biol Biochem 127:90–99 Sokol NW, Kuebbing SE, Karlsen-Ayala E, Bradford MA (2018) Evidence for the primacy of living root inputs, not root or shoot litter, in forming soil organic carbon. New Phytol 221:233–246 Starr EP, Nuccio EE, Pett-Ridge J, Banﬁeld JF, Firestone MK (2019) Metatranscriptomic recon- struction reveals RNA viruses w

Rhizosphere Biology: Interactions Between Microbes and Plants PDF

Document Details

Tags

Related

Summary

Full Transcript

Upgrade to continue