Exploring the roles of microbes in facilitating plant adaptation to climate change
Abstract
Plants benefit from their close association with soil microbes which assist in their response to abiotic and biotic stressors. Yet much of what we know about plant stress responses is based on studies where the microbial partners were uncontrolled and unknown. Under climate change, the soil microbial community will also be sensitive to and respond to abiotic and biotic stressors. Thus, facilitating plant adaptation to climate change will require a systems-based approach that accounts for the multi-dimensional nature of plant–microbe–environment interactions. In this perspective, we highlight some of the key factors influencing plant–microbe interactions under stress as well as new tools to facilitate the controlled study of their molecular complexity, such as fabricated ecosystems and synthetic communities. When paired with genomic and biochemical methods, these tools provide researchers with more precision, reproducibility, and manipulability for exploring plant–microbe–environment interactions under a changing climate.
- Authors:
-
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1855211
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Biochemical Journal
- Additional Journal Information:
- Journal Volume: 479; Journal Issue: 3; Journal ID: ISSN 0264-6021
- Publisher:
- Biochemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; climate change; fabricated ecosystems; microbiome; plant biology; plant–microbe interactions; synthetic communities
Citation Formats
Barnes, Elle M., and Tringe, Susannah G. Exploring the roles of microbes in facilitating plant adaptation to climate change. United States: N. p., 2022.
Web. doi:10.1042/bcj20210793.
Barnes, Elle M., & Tringe, Susannah G. Exploring the roles of microbes in facilitating plant adaptation to climate change. United States. https://doi.org/10.1042/bcj20210793
Barnes, Elle M., and Tringe, Susannah G. 2022.
"Exploring the roles of microbes in facilitating plant adaptation to climate change". United States. https://doi.org/10.1042/bcj20210793. https://www.osti.gov/servlets/purl/1855211.
@article{osti_1855211,
title = {Exploring the roles of microbes in facilitating plant adaptation to climate change},
author = {Barnes, Elle M. and Tringe, Susannah G.},
abstractNote = {Plants benefit from their close association with soil microbes which assist in their response to abiotic and biotic stressors. Yet much of what we know about plant stress responses is based on studies where the microbial partners were uncontrolled and unknown. Under climate change, the soil microbial community will also be sensitive to and respond to abiotic and biotic stressors. Thus, facilitating plant adaptation to climate change will require a systems-based approach that accounts for the multi-dimensional nature of plant–microbe–environment interactions. In this perspective, we highlight some of the key factors influencing plant–microbe interactions under stress as well as new tools to facilitate the controlled study of their molecular complexity, such as fabricated ecosystems and synthetic communities. When paired with genomic and biochemical methods, these tools provide researchers with more precision, reproducibility, and manipulability for exploring plant–microbe–environment interactions under a changing climate.},
doi = {10.1042/bcj20210793},
url = {https://www.osti.gov/biblio/1855211},
journal = {Biochemical Journal},
issn = {0264-6021},
number = 3,
volume = 479,
place = {United States},
year = {Fri Feb 04 00:00:00 EST 2022},
month = {Fri Feb 04 00:00:00 EST 2022}
}
Works referenced in this record:
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?
journal, January 2018
- Sasse, Joelle; Martinoia, Enrico; Northen, Trent
- Trends in Plant Science, Vol. 23, Issue 1
Scientists’ warning to humanity: microorganisms and climate change
journal, June 2019
- Cavicchioli, Ricardo; Ripple, William J.; Timmis, Kenneth N.
- Nature Reviews Microbiology, Vol. 17, Issue 9
Design of synthetic bacterial communities for predictable plant phenotypes
journal, February 2018
- Herrera Paredes, Sur; Gao, Tianxiang; Law, Theresa F.
- PLOS Biology, Vol. 16, Issue 2
Climate Disruption of Plant-Microbe Interactions
journal, November 2020
- Rudgers, Jennifer A.; Afkhami, Michelle E.; Bell-Dereske, Lukas
- Annual Review of Ecology, Evolution, and Systematics, Vol. 51, Issue 1
Cheating fosters species co-existence in well-mixed bacterial communities
journal, January 2017
- Leinweber, Anne; Fredrik Inglis, R.; Kümmerli, Rolf
- The ISME Journal, Vol. 11, Issue 5
Plant-microbe Cross-talk in the Rhizosphere: Insight and Biotechnological Potential
journal, March 2015
- Haldar, Shyamalina; Sengupta, Sanghamitra
- The Open Microbiology Journal, Vol. 9, Issue 1
The RootChip: An Integrated Microfluidic Chip for Plant Science
journal, December 2011
- Grossmann, Guido; Guo, Woei-Jiun; Ehrhardt, David W.
- The Plant Cell, Vol. 23, Issue 12
Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass
journal, January 2019
- Sasse, Joelle; Kant, Josefine; Cole, Benjamin J.
- New Phytologist, Vol. 222, Issue 2
Root exudates: from plant to rhizosphere and beyond
journal, July 2019
- Vives-Peris, Vicente; de Ollas, Carlos; Gómez-Cadenas, Aurelio
- Plant Cell Reports, Vol. 39, Issue 1
Climate Change, Aboveground-Belowground Interactions, and Species' Range Shifts
journal, December 2012
- Van der Putten, Wim H.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 43, Issue 1
Ecosystem Fabrication (EcoFAB) Protocols for The Construction of Laboratory Ecosystems Designed to Study Plant-microbe Interactions
journal, January 2018
- Gao, Jian; Sasse, Joelle; Lewald, Kyle M.
- Journal of Visualized Experiments, Issue 134
Genomes OnLine database (GOLD) v.7: updates and new features
journal, October 2018
- Mukherjee, Supratim; Stamatis, Dimitri; Bertsch, Jon
- Nucleic Acids Research, Vol. 47, Issue D1
Prolonged drought imparts lasting compositional changes to the rice root microbiome
journal, July 2021
- Santos-Medellín, Christian; Liechty, Zachary; Edwards, Joseph
- Nature Plants, Vol. 7, Issue 8
High-throughput generation, optimization and analysis of genome-scale metabolic models
journal, August 2010
- Henry, Christopher S.; DeJongh, Matthew; Best, Aaron A.
- Nature Biotechnology, Vol. 28, Issue 9
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018
- Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao
- Nature Microbiology, Vol. 3, Issue 4
Microbial Interkingdom Interactions in Roots Promote Arabidopsis Survival
journal, November 2018
- Durán, Paloma; Thiergart, Thorsten; Garrido-Oter, Ruben
- Cell, Vol. 175, Issue 4
Unraveling the sugar code: the role of microbial extracellular glycans in plant–microbe interactions
journal, September 2020
- Wanke, Alan; Malisic, Milena; Wawra, Stephan
- Journal of Experimental Botany, Vol. 72, Issue 1
Climate-smart crops with enhanced photosynthesis
journal, May 2018
- Jansson, Christer; Vogel, John; Hazen, Samuel
- Journal of Experimental Botany, Vol. 69, Issue 16
Arbuscular mycorrhizal fungi reduce decomposition of woody plant litter while increasing soil aggregation
journal, February 2015
- Leifheit, E. F.; Verbruggen, E.; Rillig, M. C.
- Soil Biology and Biochemistry, Vol. 81
MAGI: A Method for Metabolite Annotation and Gene Integration
journal, March 2019
- Erbilgin, Onur; Rübel, Oliver; Louie, Katherine B.
- ACS Chemical Biology, Vol. 14, Issue 4
Impacts of experimental alteration of water table regime and vascular plant community composition on peat mercury profiles and methylmercury production
journal, September 2019
- Haynes, Kristine M.; Kane, Evan S.; Potvin, Lynette
- Science of The Total Environment, Vol. 682
Editorial: Novel Insights Into the Response of the Plant Microbiome to Abiotic Factors
journal, May 2021
- Haichar, Feth el Zahar; Cernava, Tomislav; Liu, Jia
- Frontiers in Plant Science, Vol. 12
The BioCyc collection of microbial genomes and metabolic pathways
journal, August 2017
- Karp, Peter D.; Billington, Richard; Caspi, Ron
- Briefings in Bioinformatics, Vol. 20, Issue 4
Dealing with the unknown: Metabolomics and Metabolite Atlases
journal, September 2010
- Bowen, Benjamin P.; Northen, Trent R.
- Journal of the American Society for Mass Spectrometry, Vol. 21, Issue 9
Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria
journal, May 2011
- Mendes, R.; Kruijt, M.; de Bruijn, I.
- Science, Vol. 332, Issue 6033
Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change
journal, September 2019
- Malik, Ashish A.; Martiny, Jennifer B. H.; Brodie, Eoin L.
- The ISME Journal, Vol. 14, Issue 1
Flavonoids and Strigolactones in Root Exudates as Signals in Symbiotic and Pathogenic Plant-Fungus Interactions
journal, July 2007
- Steinkellner, Siegrid; Lendzemo, Venasius; Langer, Ingrid
- Molecules, Vol. 12, Issue 7
Drought dampens microbiome development
journal, July 2021
- Song, Yi; Haney, Cara H.
- Nature Plants, Vol. 7, Issue 8
Elevated CO2 stimulates grassland soil respiration by increasing carbon inputs rather than by enhancing soil moisture
journal, July 2011
- Carol Adair, E.; Reich, Peter B.; Trost, Jared J.
- Global Change Biology, Vol. 17, Issue 12
EcoFABs: advancing microbiome science through standardized fabricated ecosystems
journal, June 2019
- Zengler, Karsten; Hofmockel, Kirsten; Baliga, Nitin S.
- Nature Methods, Vol. 16, Issue 7
The plant microbiome explored: implications for experimental botany
journal, November 2015
- Berg, Gabriele; Rybakova, Daria; Grube, Martin
- Journal of Experimental Botany, Vol. 67, Issue 4
Biochemistry and genetics of ACC deaminase: a weapon to “stress ethylene” produced in plants
journal, September 2015
- Singh, Rajnish P.; Shelke, Ganesh M.; Kumar, Anil
- Frontiers in Microbiology, Vol. 6
Establishing Causality: Opportunities of Synthetic Communities for Plant Microbiome Research
journal, August 2017
- Vorholt, Julia A.; Vogel, Christine; Carlström, Charlotte I.
- Cell Host & Microbe, Vol. 22, Issue 2
Plant root exudation under drought: implications for ecosystem functioning
journal, October 2019
- Williams, Alex; Vries, Franciska T.
- New Phytologist, Vol. 225, Issue 5
Creation and analysis of biochemical constraint-based models using the COBRA Toolbox v.3.0
journal, February 2019
- Heirendt, Laurent; Arreckx, Sylvain; Pfau, Thomas
- Nature Protocols, Vol. 14, Issue 3
Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems
journal, November 2019
- Pugnaire, Francisco I.; Morillo, José A.; Peñuelas, Josep
- Science Advances, Vol. 5, Issue 11
More than words: the chemistry behind the interactions in the plant holobiont
journal, September 2020
- Berlanga‐Clavero, María Victoria; Molina‐Santiago, Carlos; Vicente, Antonio
- Environmental Microbiology, Vol. 22, Issue 11
Genomic features of bacterial adaptation to
plants
journal, December 2017
- Levy, Asaf; Salas Gonzalez, Isai; Mittelviefhaus, Maximilian
- Nature Genetics, Vol. 50, Issue 1
Microbiota-root-shoot-environment axis and stress tolerance in plants
journal, August 2021
- Hou, Shiji; Wolinska, Katarzyna W.; Hacquard, Stéphane
- Current Opinion in Plant Biology, Vol. 62
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis
journal, July 2010
- Bonfante, Paola; Genre, Andrea
- Nature Communications, Vol. 1, Issue 1
Selective Pressure of Temperature on Competition and Cross-Feeding within Denitrifying and Fermentative Microbial Communities
journal, January 2016
- Hanke, Anna; Berg, Jasmine; Hargesheimer, Theresa
- Frontiers in Microbiology, Vol. 6
Initial soil microbiome composition and functioning predetermine future plant health
journal, September 2019
- Wei, Zhong; Gu, Yian; Friman, Ville-Petri
- Science Advances, Vol. 5, Issue 9
Microbial interactions within the plant holobiont
journal, March 2018
- Hassani, M. Amine; Durán, Paloma; Hacquard, Stéphane
- Microbiome, Vol. 6, Issue 1
Antimicrobial activity screening of rhizosphere soil bacteria from tomato and genome-based analysis of their antimicrobial biosynthetic potential
journal, January 2021
- Zhou, Lu; Song, Chunxu; Li, Zhibo
- BMC Genomics, Vol. 22, Issue 1
The IMG/M data management and analysis system v.6.0: new tools and advanced capabilities
journal, October 2020
- Chen, I-Min A.; Chu, Ken; Palaniappan, Krishnaveni
- Nucleic Acids Research, Vol. 49, Issue D1
Bridging the Gap Between Single-Strain and Community-Level Plant-Microbe Chemical Interactions
journal, February 2020
- O’Banion, Bridget S.; O’Neal, Lindsey; Alexandre, Gladys
- Molecular Plant-Microbe Interactions®, Vol. 33, Issue 2
MIBiG 2.0: a repository for biosynthetic gene clusters of known function
journal, October 2019
- Kautsar, Satria A.; Blin, Kai; Shaw, Simon
- Nucleic Acids Research
Root exudates drive interspecific facilitation by enhancing nodulation and N 2 fixation
journal, May 2016
- Li, Bai; Li, Yu-Ying; Wu, Hua-Mao
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 23
KBase: The United States Department of Energy Systems Biology Knowledgebase
journal, July 2018
- Arkin, Adam P.; Cottingham, Robert W.; Henry, Christopher S.
- Nature Biotechnology, Vol. 36, Issue 7
From climate chambers to biodiversity chambers
journal, April 2018
- Eisenhauer, Nico; Türke, Manfred
- Frontiers in Ecology and the Environment, Vol. 16, Issue 3
Climate change effects on beneficial plant-microorganism interactions: Climate change and beneficial plant-microorganism interactions
journal, May 2010
- Compant, Stéphane; Van Der Heijden, Marcel G. A.; Sessitsch, Angela
- FEMS Microbiology Ecology
Microbial Community Metabolic Modeling: A Community Data-Driven Network Reconstruction: COMMUNITY DATA-DRIVEN METABOLIC NETWORK MODELING
journal, June 2016
- Henry, Christopher S.; Bernstein, Hans C.; Weisenhorn, Pamela
- Journal of Cellular Physiology, Vol. 231, Issue 11
Understanding and Engineering Distributed Biochemical Pathways in Microbial Communities
journal, November 2018
- Cao, Xinyun; Hamilton, Joshua J.; Venturelli, Ophelia S.
- Biochemistry, Vol. 58, Issue 2
Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking
journal, August 2016
- Wang, Mingxun; Carver, Jeremy J.; Phelan, Vanessa V.
- Nature Biotechnology, Vol. 34, Issue 8
Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase
journal, October 2005
- Glick, Bernard R.
- FEMS Microbiology Letters, Vol. 251, Issue 1
Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria
journal, April 2018
- Xu, Ling; Naylor, Dan; Dong, Zhaobin
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 18
Field study reveals core plant microbiota and relative importance of their drivers: Core microbiota of field-grown sugarcane and their drivers
journal, January 2018
- Hamonts, Kelly; Trivedi, Pankaj; Garg, Anshu
- Environmental Microbiology, Vol. 20, Issue 1
Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism
journal, August 2018
- Hoeksema, Jason D.; Bever, James D.; Chakraborty, Sounak
- Communications Biology, Vol. 1, Issue 1
Root exudate of Solanum tuberosum is enriched in galactose-containing molecules and impacts the growth of Pectobacterium atrosepticum
journal, July 2016
- Koroney, Abdoul Salam; Plasson, Carole; Pawlak, Barbara
- Annals of Botany, Vol. 118, Issue 4
Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley
journal, March 2015
- Bulgarelli, Davide; Garrido-Oter, Ruben; Münch, Philipp C.
- Cell Host & Microbe, Vol. 17, Issue 3
Polysaccharide Utilization Loci: Fueling Microbial Communities
journal, January 2017
- Grondin, Julie M.; Tamura, Kazune; Déjean, Guillaume
- Journal of Bacteriology, Vol. 199, Issue 15
Past and future global transformation of terrestrial ecosystems under climate change
journal, August 2018
- Nolan, Connor; Overpeck, Jonathan T.; Allen, Judy R. M.
- Science, Vol. 361, Issue 6405
The RAVEN Toolbox and Its Use for Generating a Genome-scale Metabolic Model for Penicillium chrysogenum
journal, March 2013
- Agren, Rasmus; Liu, Liming; Shoaie, Saeed
- PLoS Computational Biology, Vol. 9, Issue 3
Ecology and Evolution of Plant Microbiomes
journal, September 2019
- Cordovez, Viviane; Dini-Andreote, Francisco; Carrión, Víctor J.
- Annual Review of Microbiology, Vol. 73, Issue 1
Metabolome searcher: a high throughput tool for metabolite identification and metabolic pathway mapping directly from mass spectrometry and using genome restriction
journal, February 2015
- Dhanasekaran, A. Ranjitha; Pearson, Jon L.; Ganesan, Balasubramanian
- BMC Bioinformatics, Vol. 16, Issue 1
antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline
journal, April 2019
- Blin, Kai; Shaw, Simon; Steinke, Katharina
- Nucleic Acids Research, Vol. 47, Issue W1
A database for post-genome analysis
journal, September 1997
- Kanehisa, Minoru
- Trends in Genetics, Vol. 13, Issue 9
Harnessing rhizosphere microbiomes for drought-resilient crop production
journal, April 2020
- de Vries, Franciska T.; Griffiths, Rob I.; Knight, Christopher G.
- Science, Vol. 368, Issue 6488
High-order interactions distort the functional landscape of microbial consortia
journal, December 2019
- Sanchez-Gorostiaga, Alicia; Bajić, Djordje; Osborne, Melisa L.
- PLOS Biology, Vol. 17, Issue 12
Dissecting Disease-Suppressive Rhizosphere Microbiomes by Functional Amplicon Sequencing and 10× Metagenomics
journal, June 2021
- Tracanna, Vittorio; Ossowicki, Adam; Petrus, Marloes L. C.
- mSystems, Vol. 6, Issue 3
Cell wall extensins in root–microbe interactions and root secretions
journal, June 2018
- Castilleux, Romain; Plancot, Barbara; Ropitaux, Marc
- Journal of Experimental Botany, Vol. 69, Issue 18
High-resolution 3D mapping of rhizosphere glycan patterning using molecular probes in a transparent soil system
journal, December 2021
- Jones, Catherine Y.; Engelhardt, Ilonka; Patko, Daniel
- The Cell Surface, Vol. 7
Mechanisms that promote bacterial fitness in fungal-affected soil microhabitats
journal, February 2010
- Nazir, Rashid; Warmink, Jan A.; Boersma, Hidde
- FEMS Microbiology Ecology, Vol. 71, Issue 2
GNPS Dashboard: collaborative exploration of mass spectrometry data in the web browser
journal, December 2021
- Petras, Daniel; Phelan, Vanessa V.; Acharya, Deepa
- Nature Methods, Vol. 19, Issue 2
Plant–microbiome interactions: from community assembly to plant health
journal, August 2020
- Trivedi, Pankaj; Leach, Jan E.; Tringe, Susannah G.
- Nature Reviews Microbiology, Vol. 18, Issue 11
Evidence of a strong coupling between root exudation, C and N availability, and stimulated SOM decomposition caused by rhizosphere priming effects
journal, July 2012
- Bengtson, Per; Barker, Jason; Grayston, Sue J.
- Ecology and Evolution, Vol. 2, Issue 8
Host Genotype and Colonist Arrival Order Jointly Govern Plant Microbiome Composition and Function
journal, August 2020
- Leopold, Devin R.; Busby, Posy E.
- Current Biology, Vol. 30, Issue 16
Novel and Emerging Capabilities that Can Provide a Holistic Understanding of the Plant Root Microbiome
journal, January 2021
- Singer, Esther; Vogel, John P.; Northen, Trent
- Phytobiomes Journal, Vol. 5, Issue 2
DNA Stable-Isotope Probing (DNA-SIP)
journal, January 2010
- Dunford, Eric A.; Neufeld, Josh D.
- Journal of Visualized Experiments, Issue 42
Metabolic dependencies drive species co-occurrence in diverse microbial communities
journal, May 2015
- Zelezniak, Aleksej; Andrejev, Sergej; Ponomarova, Olga
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 20
Soil microbiomes and climate change
journal, October 2019
- Jansson, Janet K.; Hofmockel, Kirsten S.
- Nature Reviews Microbiology, Vol. 18, Issue 1
Linking soil biology and chemistry in biological soil crust using isolate exometabolomics
journal, January 2018
- Swenson, Tami L.; Karaoz, Ulas; Swenson, Joel M.
- Nature Communications, Vol. 9, Issue 1
Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota
journal, July 2018
- Hu, Lingfei; Robert, Christelle A. M.; Cadot, Selma
- Nature Communications, Vol. 9, Issue 1