Precipitation legacy effects on soil microbiota facilitate adaptive drought responses in plants.

Nichole A Ginnan, Valéria Custódio, David Gopaulchan, Natalie Ford, Isai Salas-González, Dylan H Jones, Darren M Wells, Ângela Moreno, Gabriel Castrillo, Maggie R Wagner

Journal: Nature microbiology 2025;10(11):2823-2844

PMID: 41168432

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Abstract

Drought alters the soil microbiota by selecting for functional traits that preserve fitness in dry conditions. Legacy effects or ecological memory refers to how past stress exposure influences microbiota responses to future environmental challenges. How precipitation legacy effects impact soil microorganisms and plants is unclear, especially in the context of subsequent drought. Here we characterized the metagenomes of six prairie soils spanning a precipitation gradient in Kansas, United States. A microbial precipitation legacy, which persisted over a 5-month-long experimental drought, mitigated the negative physiological effects of acute drought for a native wild grass species, but not for the domesticated crop species maize. RNA sequencing of roots revealed that soil microbiota with a low precipitation legacy altered expression of plant genes that mediate transpiration and intrinsic water-use efficiency during drought. Our results show how historical exposure to water stress alters soil microbiota, with consequences for future drought responses of some plant species.

Address: Kansas Biological Survey and Center for Ecological Research, University of Kansas, Lawrence, KS, USA.; Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA, USA.; Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, USA.; School of Biosciences, University of Nottingham, Sutton Bonington Campus, Nottingham, UK.; Kansas Biological Survey and Center for Ecological Research, University of Kansas, Lawrence, KS, USA.; Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, USA.; Centre for Genomics Sciences, Universidad Nacional Autónoma de México, Cuernavaca, Mexico.; Ministério da Agricultura e Ambiente - Empresa Pública Água de Rega, SA, Praia, Cabo Verde.; School of Biosciences, University of Nottingham, Sutton Bonington Campus, Nottingham, UK. [email protected].; Kansas Biological Survey and Center for Ecological Research, University of Kansas, Lawrence, KS, USA. [email protected].; Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, USA. [email protected].

DOI: 10.1038/s41564-025-02148-8

MeSH Terms: Droughts, Soil Microbiology, Microbiota, Zea mays, Soil, Rain, Kansas, Plant Roots, Stress, Physiological, Metagenome, Adaptation, Physiological, Water, Plants, Bacteria