Heritable microbiome variation is correlated with source environment in locally adapted maize varieties

23 páginas.- 6 figuras.- 89 referencias.- Supplementary information The online version contains supplementary material available at https://doi.org/10.1038/s41477-024-01654-7

Beneficial interactions with microorganisms are pivotal for crop performance and resilience. However, it remains unclear how heritable the microbiome is with respect to the host plant genotype and to what extent host genetic mechanisms can modulate plant–microbiota interactions in the face of environmental stresses. Here we surveyed 3,168 root and rhizosphere microbiome samples from 129 accessions of locally adapted Zea, sourced from diverse habitats and grown under control and different stress conditions. We quantified stress treatment and host genotype effects on the microbiome. Plant genotype and source environment were predictive of microbiome abundance. Genome-wide association analysis identified host genetic variants linked to both rhizosphere microbiome abundance and source environment. We identified transposon insertions in a candidate gene linked to both the abundance of a keystone bacterium Massilia in our controlled experiments and total soil nitrogen in the source environment. Isolation and controlled inoculation of Massilia alone can contribute to root development, whole-plant biomass production and adaptation to low nitrogen availability. We conclude that locally adapted maize varieties exert patterns of genetic control on their root and rhizosphere microbiomes that follow variation in their home environments, consistent with a role in tolerance to prevailing stress.

This work is supported by Deutsche Forschungsgemeinschaft (DFG) grants HO2249/9-3, HO2249/12-1 to F.H. and YU272/4-1 and Emmy Noether Programme 444755415 to P.Y., the German Excellence Strategy – EXC 2070 – grant 390732324 to P.Y. and G.S., and DFG Priority Program (SPP2089) ‘Rhizosphere Spatiotemporal Organisation - A Key to Rhizosphere Functions’ grant 403671039 to F.H. and P.Y. Germplasm propagation is funded by the TRA Sustainable Futures (University of Bonn) as part of the Excellence Strategy of the federal and state governments. X.C.’s research is supported by The Changjiang Scholarship, Ministry of Education, China, State Cultivation Base of Eco-agriculture for Southwest Mountainous Land (Southwest University, Chongqing, China), and the National Maize Production System in China (grant no. CARS-02-15). R.J.H.S. is funded by USDA Hatch Appropriations under project number PEN04734 and accession number 1021929.

Peer reviewed