Host genotype controls ecological change in the leaf fungal microbiome

Abstract

Leaf fungal microbiomes can be fundamental drivers of host plant success, as they contain pathogens that devastate crop plants and taxa that enhance nutrient uptake, discourage herbivory, and antagonize pathogens. We measured leaf fungal diversity with amplicon sequencing across an entire growing season in a diversity panel of switchgrass (Panicum virgatum). We also sampled a replicated subset of genotypes across 3 additional sites to compare the importance of time, space, ecology, and genetics. We found a strong successional pattern in the microbiome shaped both by host genetics and environmental factors. Further, we used genome-wide association (GWA) mapping and RNA sequencing to show that 3 cysteine-rich receptor-like kinases (crRLKs) were linked to a genetic locus associated with microbiome structure. We confirmed GWAS results in an independent set of genotypes for both the internal transcribed spacer (ITS) and large subunit (LSU) ribosomal DNA markers. Fungal pathogens were central to microbial covariance networks, and genotypes susceptible to pathogens differed in their expression of the 3 crRLKs, suggesting that host immune genes are a principal means of controlling the entire leaf microbiome.

The genetic architecture of adaptation to leaf and root bacterial microbiota inArabidopsis thaliana

“…1B). This is in line with the polygenic architecture reported in GWAS conducted on microbial communities (Horton et al 2014; Walters et al 2018; Bergelson et al 2019; Roman-Reyna et al 2020; Deng et al 2021; Brachi et al 2022; VanWallendael et al 2022). Differences in the number of QTLs among the six ‘plant compartment × seasons’ were barely significant (Generalized Linear Model, GLM, F = 2.30, P = 0.0471).…”

“…5B). Such an observation is reminiscent of the strong genetic variation in seasonal microbial community succession observed in diverse plant species including A. thaliana (Copeland et al 2015; Bartoli et al 2018; Beilsmith et al 2021; VanWallendael et al 2022) and the dynamics of genetic architecture along the infection stages when A. thaliana accessions were challenged with the bacterial pathogen Ralstonia solanacearum (Aoun et al 2017; Aoun et al 2020; Demirjian et al 2022).…”

“…All GWAS performed previously on plant microbial communities were conducted on one specific plant compartment (Walters et al 2018; Roman-Reyna et al 2020; Deng et al 2021; Brachi et al 2022; VanWallendael et al 2022), with the exception of one GWAS conducted on worldwide accessions of A. thaliana at the leaf (Horton et al 2014) and root (Bergelson et al 2019) levels. Similar to our results, this latter GWAS showed a small overlap between the leaf and root compartments in candidate genes associated with descriptors of bacterial and fungal communities (Bergelson et al 2019), which is in line with the adaptive differences in microbial community diversity and composition observed among plant niches, from rhizosphere soils to plant canopies (Müller et al 2016; Cregger et al 2018).…”

“…While the importance of host genetics in shaping natural variation on microbial communities has been a long-lasting debate (Roux and Bergelson 2016), an ever-increasing number of studies reported significant microbiota differences between closely related species or among genotypes within a given species (when grown in the same environment), with typical values for the magnitude of these differences ranging from 5% to 30% (Schlaeppi et al 2014;Bergelson, Brachi, et al 2021). Following the detection of significant heritability estimates, seven genome-wide association studies (GWAS) using microbial community descriptors as plant traits have been performed in Arabidopsis thaliana (Horton et al 2014;Bergelson et al 2019;Brachi et al 2022), maize (Walters et al 2018), rice (Roman-Reyna et al 2020), sorghum (Deng et al 2021) and switchgrass (VanWallendael et al 2022). These GWAS revealed a highly polygenic architecture, suggesting a control of natural microbiota assembly by an extensive number of Quantitative Trait Loci (QTLs) with a small effect.…”

The changing influence of host genetics on the leaf fungal microbiome throughout plant development

“…Switchgrass (Panicum virgatum) is a genetically diverse perennial grass native to and distributed throughout North America that is planted in agriculture for feedstock and biomass energy production. A new study published in PLOS Biology by Van Wallendael and colleagues investigates factors influencing the fungal leaf microbiome of switchgrass [7] (Fig 1). This research was an impressive logistical feat involving repeated longitudinal measurements of hundreds of plants, including at field sites at different latitudes in the United States of America.…”