Microbiome interactions increase plant haplotype richness

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Abstract The genetic makeup of natural plant populations often allows them to persist for many years without succumbing to disease. Transferring such properties to crops could increase resilience and reduce reliance on chemical pesticides​. However, the population genomics of plant-microbiome interactions remain poorly understood. Here, we use Lotus japonicus, which has persisted as a natural population in Japan for ~20’000 years​, to identify genomic selection signatures caused by soil microbes. We found strong genetic associations with root microbiome structure within a gene we name ROOT MICROBIOME ESTABLISHMENT 1 (ROOMIE1) located in a region with high haplotype richness. This led us to quantify haplotype richness genome-wide using a new metric, HAPk. We found haplotype-rich regions strongly enriched for microbiome genetic associations, suggesting that soil microbes were imposing negative frequency-dependent selection. We validated this hypothesis by showing increased migration rates of microbiome associated alleles and by determining that ROOMIE1 shows standing variation in local populations and impacts rhizosphere colonization in native Japanese soil. Our results indicate that interactions with soil microbes represent a major selective force in plant genome evolution and suggest that haplotype-rich regions constitute a genetic resource for improvement of crop resilience.
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Microbiome interactions increase plant haplotype richness | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Biological Sciences - Article Microbiome interactions increase plant haplotype richness Stig Andersen, Johan Quilbé, Troels Mouritzen, Turgut Akyol, Yusdar Mustamin, and 3 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5130034/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract The genetic makeup of natural plant populations often allows them to persist for many years without succumbing to disease. Transferring such properties to crops could increase resilience and reduce reliance on chemical pesticides​. However, the population genomics of plant-microbiome interactions remain poorly understood. Here, we use Lotus japonicus, which has persisted as a natural population in Japan for ~20’000 years​, to identify genomic selection signatures caused by soil microbes. We found strong genetic associations with root microbiome structure within a gene we name ROOT MICROBIOME ESTABLISHMENT 1 (ROOMIE1) located in a region with high haplotype richness. This led us to quantify haplotype richness genome-wide using a new metric, HAPk. We found haplotype-rich regions strongly enriched for microbiome genetic associations, suggesting that soil microbes were imposing negative frequency-dependent selection. We validated this hypothesis by showing increased migration rates of microbiome associated alleles and by determining that ROOMIE1 shows standing variation in local populations and impacts rhizosphere colonization in native Japanese soil. Our results indicate that interactions with soil microbes represent a major selective force in plant genome evolution and suggest that haplotype-rich regions constitute a genetic resource for improvement of crop resilience. Biological sciences/Plant sciences/Natural variation in plants Biological sciences/Plant sciences/Plant evolution Biological sciences/Microbiology/Microbial communities Balancing selection microbiome genome evolution plant-microbe interactions commensal bacteria Full Text Additional Declarations There is NO Competing Interest. Supplementary Files 20240618SupplFile1.xlsx Supplementary Table 1 Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. 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