Plant-Microbe Interfaces: Molecular Insights into the Mutualistic Symbiosis Between Populus and Plant Growth-Promoting Bacteria
Authors:
Bryan Piatkowski1* ([email protected]), Dana L. Carper1, Alyssa Carrell1, Caroline Harwood2, Sara Jawdy1, Jennifer Morrell-Falvey1, Yasuhiro Oda2, Dale Pelletier1, Amy Schaefer2, Amber Webb1, Dave Weston1, Xiaohan Yang1, and Mitchel Doktycz1
Institutions:
1Oak Ridge National Laboratory (ORNL); and 2University of Washington
URLs:
Goals
The goal of the Plant-Microbe Interfaces (PMI) Science Focus Area (SFA) is to characterize and interpret the physical, molecular, and chemical interfaces between plants and microbes and determine their functional roles in biological and environmental systems. Populus and its associated microbial community serve as the experimental system for understanding the dynamic exchange of energy, information, and materials across this interface and its expression as functional properties at diverse spatial and temporal scales. To achieve this goal, the product focuses on (1) defining the bidirectional progression of molecular and cellular events involved in selecting and maintaining specific, mutualistic Populus-microbe interfaces, (2) defining the chemical environment and molecular signals that influence community structure and function, and (3) understanding the dynamic relationship and extrinsic stressors that shape microbiome composition and affect host performance.
Abstract
Plants have been co-evolving with microbes since their emergence onto land some half a billion years ago, yet predictive understanding of how mutualistic symbioses between these diverse groups of organisms are selected and maintained is still in its infancy. Recently, considerable attention has been focused on plant growth–promoting bacteria (PGPB) for their application to agriculture, bioprotection, and phytoremediation. Such PGPB are known to stimulate plant growth through enhancing nutrient acquisition or modulating hormone levels in select crop species, but little is known about their potential impacts on woody perennials like poplar that are relevant to sustainable biofuel production. To address this knowledge gap, researchers first isolated and sequenced bacteria from the roots of field grown Populus (Blair et al. 2018; Carper et al. 2021). This culture collection represents over 3,200 unique bacterial isolates, and full genome sequences are available for over 550 of these isolates. Using comparative genomics, the team identified potential PGPB isolates that have the enzymatic machinery required for nitrogen fixation. Results showed that one of these isolates, Rahnella sp. OV588, catalyzes acetylene reduction in vitro and that this activity is dependent on the nitrogenase (nifH) enzyme. In co-culture experiments, Rahnella efficiently colonized the endosphere of axenic poplar plants and catalyzed acetylene reduction in planta under nitrogen-limiting conditions. Bacterial inoculation significantly increased root biomass, suggesting that the plant host can benefit from treatment with PGPB. To understand the molecular mechanisms involved in the establishment of this plant-microbe symbiosis, researchers quantified host transcriptomic response over a time course. Gene expression was affected by both time and microbial treatment, with the largest treatment effect observed at 24 hours post-inoculation. Genes induced by PGPB treatment were enriched for biological processes, including root morphogenesis, hormone metabolism, and sugar signaling, but also show signatures of an induced systemic immune response. Findings elucidate the mechanisms by which mutualistic relationships are established between poplar and members of its microbiome and highlight possible strategies to improve biofuel feedstock production in marginal habitats.
References
Blair, P. M., et al. 2018. “Exploration of the Biosynthetic Potential of the Populus Microbiome,” mSystems 3(5), e00045-18. DOI:10.1128/mSystems.00045-18.
Carper, D. L., et al. 2021. “Cultivating the Bacterial Microbiota of Populus Roots,” mSystems 6(3), e01306-20. DOI:10.1128/mSystems.01306-20.
Funding Information
Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the U.S. Department of Energy under contract no. DE-AC05-00OR22725. The Plant-Microbe Interfaces SFA is sponsored by the Genomic Science program, U.S Department of Energy, Office of Science, Biological and Environmental Research (BER) Program under FWP ERKP730.