Abstract
BackgroundUnderstanding the genetic and environmental factors that structure plant microbiomes is necessary for leveraging these interactions to address critical needs in agriculture, conservation, and sustainability. Legumes, which form root nodule symbioses with nitrogen-fixing rhizobia, have served as model plants for understanding the genetics and evolution of beneficial plant-microbe interactions for decades, and thus have added value as models of plant-microbiome interactions. Here we use a common garden experiment with 16S rRNA gene amplicon and shotgun metagenomic sequencing to study the drivers of microbiome diversity and composition in three genotypes of the model legume Medicago truncatula grown in two native soil communities.ResultsBacterial diversity decreased between external (rhizosphere) and internal plant compartments (root endosphere, nodule endosphere, and leaf endosphere). Community composition was shaped by strong compartment × soil origin and compartment × plant genotype interactions, driven by significant soil origin effects in the rhizosphere and significant plant genotype effects in the root endosphere. Nevertheless, all compartments were dominated by Ensifer, the genus of rhizobia that forms root nodule symbiosis with M. truncatula, and additional shotgun metagenomic sequencing suggests that the nodulating Ensifer were not genetically distinguishable from those elsewhere in the plant. We also identify a handful of OTUs that are common in nodule tissues, which are likely colonized from the root endosphere.ConclusionsOur results demonstrate strong host filtering effects, with rhizospheres driven by soil origin and internal plant compartments driven by host genetics, and identify several key nodule-inhabiting taxa that coexist with rhizobia in the native range. Our results set the stage for future functional genetic experiments aimed at expanding our pairwise understanding of legume-rhizobium symbiosis toward a more mechanistic understanding of plant microbiomes.4yG9Be_5fuxNDH9Lv9Ven5Video
Highlights
Understanding the genetic and environmental factors that structure plant microbiomes is necessary for leveraging these interactions to address critical needs in agriculture, conservation, and sustainability
Root endophyte samples with a high percentage of reads mapped to E. medicae WSM419 produced more than 30 scaffolds ranging from 50 to 427 kb, while nodule samples regularly produced 40 or more scaffolds greater than 50 kb, and each nodule sample produced more than 15 scaffolds greater than 100 kb
Medicago is a well-studied genetic model for plant-microbe symbiosis [60, 61, 65], and ours is the first NGS study of its native soil microbiome; we anticipate that our results will be of interest to many in the plant genetics community who are interested in building on our mechanistic understanding of 2-player plant-microbe interactions to better understand plant microbiomes
Summary
Understanding the genetic and environmental factors that structure plant microbiomes is necessary for leveraging these interactions to address critical needs in agriculture, conservation, and sustainability. Plants grow in close co-association with a striking diversity of microorganisms [1]. These microbes, including bacteria, archaea, fungi, and protists, can inhabit every conceivable plant organ and tissue as either epiphytes or endophytes. A fuller understanding of plant microbiomes is critical for improvements in environmental sustainability [17], agriculture [18], and conservation [19]. To leverage microbiomes to address critical needs, we must better understand the factors that structure microbial communities within and among plant hosts, building a predictive understanding of microbiome assembly
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