Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?

Sasse, Joelle; Martinoia, Enrico; Northen, Trent

doi:10.1016/j.tplants.2017.09.003

Title: Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?

Journal Article · Tue Oct 17 00:00:00 EDT 2017 · Trends in Plant Science

DOI:https://doi.org/10.1016/j.tplants.2017.09.003· OSTI ID:1532289

Sasse, Joelle ^[1]; Martinoia, Enrico ^[2]; Northen, Trent ^[3]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of Zurich (Switzerland)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Plant health in natural environments depends on interactions with complex and dynamic communities comprising macro- and microorganisms. While many studies have provided insights into the composition of rhizosphere microbiomes (rhizobiomes), little is known about whether plants shape their rhizobiomes. In this work, we discuss physiological factors of plants that may govern plant–microbe interactions, focusing on root physiology and the role of root exudates. Given that only a few plant transport proteins are known to be involved in root metabolite export, we suggest novel families putatively involved in this process. Finally, building off of the features discussed in this review, and in analogy to well-known symbioses, we elaborate on a possible sequence of events governing rhizobiome assembly. Recent advances in sequencing technology have been enabling high-throughput characterization of highly complex plant-associated microbial communities, which are relevant for plant health. Metagenomic approaches have been identifying the metabolic potential of microbes, and are starting to reveal functional groups of microbes, reducing the overall complexity of rhizobiomes. Metabolomic studies are uncovering differential root exudation in various environments and plant developmental stages, as well as consumption of specific exometabolites by microbes. Genome-wide association studies and other comparative genomic approaches have been revealing a link between plant genetic factors, exudation profiles, and microbiome compositions. Finally, molecular studies have been characterizing plant transport proteins necessary for interactions with specific microbes, although the transport of most nutrients and signaling molecules remains unexplored.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1532289

Alternate ID(s):: OSTI ID: 1549384

Journal Information:: Trends in Plant Science, Vol. 23, Issue 1; ISSN 1360-1385

Publisher:: Cell PressCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 741 works

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Drivers of the composition of active rhizosphere bacterial communities in temperate grasslands Vieira, Selma; Sikorski, Johannes; Dietz, Sophie The ISME Journal, Vol. 14, Issue 2 https://doi.org/10.1038/s41396-019-0543-4	journal	October 2019
Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota Hu, Lingfei; Robert, Christelle A. M.; Cadot, Selma Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05122-7	journal	July 2018
Root Exudation of Primary Metabolites: Mechanisms and Their Roles in Plant Responses to Environmental Stimuli Canarini, Alberto; Kaiser, Christina; Merchant, Andrew Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00157	journal	February 2019
Rhizosphere modelling reveals spatiotemporal distribution of daidzein shaping soybean rhizosphere bacterial community Okutani, Fuki; Hamamoto, Shoichiro; Aoki, Yuichi Plant, Cell & Environment, Vol. 43, Issue 4 https://doi.org/10.1111/pce.13708	journal	January 2020
Recognition of dominant attractants by key chemoreceptors mediates recruitment of plant growth-promoting rhizobacteria: Key determinants for rhizosphere chemotaxis Feng, Haichao; Zhang, Nan; Fu, Ruixin Environmental Microbiology, Vol. 21, Issue 1 https://doi.org/10.1111/1462-2920.14472	journal	January 2019
Need for Laboratory Ecosystems To Unravel the Structures and Functions of Soil Microbial Communities Mediated by Chemistry Zhalnina, Kateryna; Zengler, Karsten; Newman, Dianne mBio, Vol. 9, Issue 4 https://doi.org/10.1128/mbio.01175-18	journal	July 2018
Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere Couradeau, Estelle; Giraldo-Silva, Ana; De Martini, Francesca Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0661-2	journal	April 2019
Strigolactones: Plant Hormones with Promising Features Bouwmeester, Harro J.; Fonne‐Pfister, Raymonde; Screpanti, Claudio Angewandte Chemie International Edition, Vol. 58, Issue 37 https://doi.org/10.1002/anie.201901626	journal	August 2019
Root exudation of mature beech forests across a nutrient availability gradient: the role of root morphology and fungal activity Meier, Ina C.; Tückmantel, Timo; Heitkötter, Julian New Phytologist, Vol. 226, Issue 2 https://doi.org/10.1111/nph.16389	journal	January 2020
The Effects of Different Lead Pollution Levels on Soil Microbial Quantities and Metabolic Function with/without Salix integra Thunb. Planting Niu, Xiaoyun; Zhou, Yong; Zhou, Jian Forests, Vol. 10, Issue 2 https://doi.org/10.3390/f10020077	journal	January 2019
Sticky mucilages and exudates of plants: putative microenvironmental design elements with biotechnological value Galloway, Andrew F.; Knox, Paul; Krause, Kirsten New Phytologist, Vol. 225, Issue 4 https://doi.org/10.1111/nph.16144	journal	September 2019
Specialized bacteriome uncovered in the coralloid roots of the epiphytic gymnosperm, Zamia pseudoparasitica Bell‐Doyon, Philip; Laroche, Jérôme; Saltonstall, Kristin Environmental DNA, Vol. 2, Issue 4 https://doi.org/10.1002/edn3.66	journal	January 2020
Plant root exudation under drought: implications for ecosystem functioning Williams, Alex; Vries, Franciska T. New Phytologist, Vol. 225, Issue 5 https://doi.org/10.1111/nph.16223	journal	October 2019
The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics Vincent, Delphine; Rafiqi, Maryam; Job, Dominique Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01626	journal	January 2020
Nitrogen- and phosphorus-starved Triticum aestivum show distinct belowground microbiome profiles Pagé, Antoine P.; Tremblay, Julien; Masson, Luke PLOS ONE, Vol. 14, Issue 2 https://doi.org/10.1371/journal.pone.0210538	journal	February 2019
Plant Host-Associated Mechanisms for Microbial Selection Jones, Piet; Garcia, Benjamin J.; Furches, Anna Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00862	journal	July 2019
Manipulation of vegetation with activated carbon reveals the role of root exudates in shaping native grassland communities Nettan, Siim; Thetloff, Marge; Lepik, Anu Journal of Vegetation Science, Vol. 30, Issue 6 https://doi.org/10.1111/jvs.12808	journal	September 2019
Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly Liu, Fang; Hewezi, Tarek; Lebeis, Sarah L. BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1572-x	journal	September 2019
The Chemistry of Plant–Microbe Interactions in the Rhizosphere and the Potential for Metabolomics to Reveal Signaling Related to Defense Priming and Induced Systemic Resistance Mhlongo, Msizi I.; Piater, Lizelle A.; Madala, Ntakadzeni E. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00112	journal	February 2018
Root exudates drive the soil-borne legacy of aboveground pathogen infection Yuan, Jun; Zhao, Jun; Wen, Tao Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0537-x	journal	September 2018
Genome-wide transcriptome profiling provides insights into the responses of maize (Zea mays L.) to diazotrophic bacteria Hardoim, Pablo R.; de Carvalho, Thais L. G.; Ballesteros, Helkin G. F. Plant and Soil https://doi.org/10.1007/s11104-019-04193-9	journal	July 2019
Pseudomonas chlororaphis Produces Multiple R-Tailocin Particles That Broaden the Killing Spectrum and Contribute to Persistence in Rhizosphere Communities Dorosky, Robert J.; Pierson, Leland S.; Pierson, Elizabeth A. Applied and Environmental Microbiology, Vol. 84, Issue 18 https://doi.org/10.1128/aem.01230-18	journal	July 2018
Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass Sasse, Joelle; Kant, Josefine; Cole, Benjamin J. New Phytologist, Vol. 222, Issue 2 https://doi.org/10.1111/nph.15662	journal	January 2019
Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System Poudel, Ravin; Jumpponen, Ari; Kennelly, Megan M. Applied and Environmental Microbiology, Vol. 85, Issue 2 https://doi.org/10.1128/aem.01765-18	journal	November 2018
Metabolic Overlap in Environmentally Diverse Microbial Communities Hester, Eric R.; Jetten, Mike S. M.; Welte, Cornelia U. Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00989	journal	October 2019
Microbiome Selection Could Spur Next-Generation Plant Breeding Strategies Gopal, Murali; Gupta, Alka Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01971	journal	December 2016
Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota Hu, Lingfei; Robert, Christelle A. M.; Cadot, Selma Nature Publishing Group https://doi.org/10.5167/uzh-168377	text	January 2018
Switchgrass Rhizosphere Metabolite Chemistry Driven by Nitrogen Availability Smercina, Darian N.; Bowsher, Alan W.; Evans, Sarah E. Phytobiomes Journal, Vol. 5, Issue 1 https://doi.org/10.1094/pbiomes-09-19-0055-fi	journal	January 2021
Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots Banerjee, Samiran; Walder, Florian; Büchi, Lucie Nature Publishing Group https://doi.org/10.5167/uzh-182854	text	January 2019
Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass Sasse, Joelle; Kant, Josefine; Cole, Benjamin J. ETH Zurich https://doi.org/10.3929/ethz-b-000334593	text	January 2019
Cytidine 5'-Diphosphate Reductase and Thymidine Kinase Activities in Phytohemagglutinin-stimulated Lymphocytes of Normal Subjects of Various Ages and Patients with Immunodeficiency Takeda, Eiji; Kuroda, Yasuhiro; Watanabe, Toshiyuki Pediatric Research, Vol. 18, Issue 8 https://doi.org/10.1203/00006450-198408000-00002	journal	August 1984
Changes in rhizosphere microbial communities in potted cucumber seedlings treated with syringic acid Wang, Zhilin; Zhang, Jianhui; Wu, Fengzhi PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0200007	journal	June 2018
Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass T. R., Northen,; J., Sasse,; B. P., Bowen, Blackwell Publishing Ltd https://doi.org/10.17615/xy8v-sa53	text	January 2019
Land Management and Microbial Seed Load Effect on Rhizosphere and Endosphere Bacterial Community Assembly in Wheat Kavamura, Vanessa Nessner; Robinson, Rebekah J.; Hayat, Rifat Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02625	journal	November 2019
Comparative Analysis of Rhizosphere Microbiomes of Southern Highbush Blueberry (Vaccinium corymbosum L.), Darrow’s Blueberry (V. darrowii Camp), and Rabbiteye Blueberry (V. virgatum Aiton) Li, Jiangang; Mavrodi, Olga V.; Hou, Jinfeng Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00370	journal	March 2020
Cultivar-Dependent Variation of the Cotton Rhizosphere and Endosphere Microbiome Under Field Conditions Wei, Feng; Zhao, Lihong; Xu, Xiangming Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01659	journal	December 2019
Influences of Climate on Phyllosphere Endophytic Bacterial Communities of Wild Poplar Firrincieli, Andrea; Khorasani, Mahsa; Frank, A. Carolin Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00203	journal	February 2020
Prospects for the Study and Improvement of Abiotic Stress Tolerance in Date Palms in the Post-genomics Era Hazzouri, Khaled Michel; Flowers, Jonathan M.; Nelson, David Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00293	journal	March 2020
Culturing Simpler and Bacterial Wilt Suppressive Microbial Communities from Tomato Rhizosphere Roy, Nazish; Choi, Kihyuck; Khan, Raees The Plant Pathology Journal, Vol. 35, Issue 4 https://doi.org/10.5423/ppj.ft.07.2019.0180	journal	August 2019

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