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ABSTRACT Understanding the impact of microbial interactions on plants is critical for maintaining healthy native ecosystems and sustainable agricultural practices. Despite the reality that genetically distinct plants host multiple microbes of large effect in the field, it remains unclear the extent to which host genotypes modulate non‐additive microbial interactions and how these interactions differ between benign/pathogenic environments. Our study fills this gap by performing a large‐scale manipulative microbiome experiment across seven genotypes of the model legumeMedicago truncatula. We combine plant performance metrics, survival analyses, predictive modelling, RNA extractions and targeted gene expression to assess how host genotype and microbes non‐additively interact to shape plant growth and disease ecology. Our results reveal three important findings: (1) host genotypes with high tolerance to pathogens benefit more from multiple mutualist interactions than susceptible genotypes, (2) only high‐tolerance genotypes retain the same beneficial host performance outcomes from the benign environment within the pathogenic environment and (3) the quality of the symbiotic relationship with mutualists is a strong predictor of host survival against pathogenic disease. By applying these findings towards developing crops that promote synergistic microbial interactions, yields and pathogen defence could be simultaneously increased while reducing the need for toxic fertilisers and pesticides.
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Maintaining Symbiotic Homeostasis: How Do Plants Engage With Beneficial Microorganisms While at the Same Time Restricting Pathogens?
This article is part of the Top 10 Unanswered Questions in MPMI invited review series. That plants recruit beneficial microbes while simultaneously restricting pathogens is critical to their survival. Plants must exclude pathogens; however, most land plants are able to form mutualistic symbioses with arbuscular mycorrhizal fungi. Plants also associate with the complex microbial communities that form the microbiome. The outcome of each symbiotic interaction—whether a specific microbe is pathogenic, commensal, or mutualistic—relies on the specific interplay of host and microbial genetics and the environment. Here, we discuss how plants use metabolites as a gate to select which microbes can be symbiotic. Once present, we discuss how plants integrate multiple inputs to initiate programs of immunity or mutualistic symbiosis and how this paradigm may be expanded to the microbiome. Finally, we discuss how environmental signals are integrated with immunity to fine-tune a thermostat that determines whether a plant engages in mutualism, resistance to pathogens, and shapes associations with the microbiome. Collectively, we propose that the plant immune thermostat is set to select for and tolerate a largely nonharmful microbiome while receptor-mediated decision making allows plants to detect and dynamically respond to the presence of potential pathogens or mutualists. [Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .
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- Award ID(s):
- 2010946
- PAR ID:
- 10392539
- Date Published:
- Journal Name:
- Molecular Plant-Microbe Interactions®
- Volume:
- 34
- Issue:
- 5
- ISSN:
- 0894-0282
- Page Range / eLocation ID:
- 462 to 469
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1094/MPMI-11-20-0318-FI
