Root-associated microorganisms reprogram plant life history along the growth–stress resistance tradeoff

Abstract

Growth–defense tradeoffs are a major constraint on plant evolution. While the genetics of resource allocation is well established, the regulatory role of plant-associated microorganisms is still unclear. Here, we demonstrate that plant-associated microorganisms can reposition the plant phenotype along the same growth–defense tradeoff that determines phenotypic effects of plant mutations. We grew plants with microorganisms altering ethylene balance, a key hormone regulating plant investment into growth and stress tolerance. Microbial ethylene reduction had a similar effect to mutations disrupting ethylene signaling: both increased plant growth but at the cost of a strong stress hypersensitivity. We conclude that microbial impact on phenotype can offset the effects of mutations and that apparent plant growth promotion has strong pleiotropic effects. This study confirms that plant life history should be addressed as a joint product of plant genotype and its associated microbiota.

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Acknowledgements

Laurentius A.C.J. Voesenek and Rashmi Sasidharan are acknowledged for their contribution to the project design. The authors would like to thank Prof. Bernard Glick, Department of Biology, University of Waterloo, Waterloo, ON, Canada for providing the bacteria strains. Francisco X Nascimento from the plant–microbe interaction of Utrecht University is acknowledged for his inputs for experimental setup on the agar plate. Sjon Hartman from the ecophysiology group of Utrecht University is acknowledged for his inputs in ethylene pretreatment. Gerrit Rouwenhorst from Ecology and Biodiversity group, Utrecht University is acknowledged for his valuable advice for plant and soil digestions and doing ICP measurements. Rob Welschen from the Plant Ecophysiology group, Peter Veenhuizen, G.P. Verduyn, and Paolo Carril Vaglini from the Ecology and Biodiversity group, Utrecht University are acknowledged for their technical assistance and advice.

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MR, AJ, and GK designed the experiment. MR collected the data, performed lab work, and analyzed output data. MR and AJ wrote the first draft of the manuscript, and all authors contributed substantially to revisions and final approval.

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Correspondence to Mohammadhossein Ravanbakhsh or Alexandre Jousset.

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Ravanbakhsh, M., Kowalchuk, G.A. & Jousset, A. Root-associated microorganisms reprogram plant life history along the growth–stress resistance tradeoff. ISME J 13, 3093–3101 (2019). https://doi.org/10.1038/s41396-019-0501-1

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