Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula

Abstract

Background 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. 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. Results Bacterial 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. Conclusions Our 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 towards a more mechanistic understanding of plant microbiomes.

Endophytes isolated from Panax notoginseng converted ginsenosides

“…Fungal endophytes can facilitate mineral nutrient uptake, promote plant growth and development, and induce defence resistance against pathogens (Taghinasab et al ., 2018). In a previous Medicago truncatula study, LEfSe analyses identified the following: 10 biomarkers OTUs for leaves dominated by Pseudomonas , Niastella and Phormidium ; and 12 biomarker OTUs for roots dominated by Thioalkalibacter , Neorhizobium and Ohtaekwangia , plus one OTU ( Ensifer ) for nodules (Brown et al ., 2020). These results indicated that different parts of P .…”

The microbiome of Lotus nodules varies with plant health in a species-specific manner

“…Soil is the main influencing factor on the rhizosphere, root, or nodule microbiomes in non-legumes (43) (44) and legumes, such as Medicago truncatula (45) and soybean (46,47). However, many of these studies cite vast differences in the diversity of the microbial communities or physicochemical properties of the soil inputs as the reason for the disparity in plant microbiomes (43,45,47). Our results showed that the nodule microbiomes of plants inoculated with different soil suspensions varied significantly (Table S3).…”

“…Plant genotype influence on plant-related microbiomes varies among legume species. Brown et al, reported that the rhizosphere microbial community of M. truncatula is mainly influenced by soil type, while the host genotype is the main determinant of the microbiota in internal plant compartments (45). Similarly, the nodule microbiome of soybean and alfalfa are primarily influenced by host genotype, while the rhizosphere microbiome is more regulated by soil type (52).…”

Hormones as go‐betweens in plant microbiome assembly

“…They can live in neutral, beneficial or pathogenic interaction within or outside of the plant (Raaijmakers et al ., 2009; Turner et al ., 2013a). Unsurprisingly, in addition to environmental niche effects and edaphic factors, plants have evolved mechanisms to shape such communities, benefit from and even exploit microbiomes as a huge genetic resource to expand their ability to cope with changing environmental conditions (Bulgarelli et al ., 2012; Lundberg et al ., 2012; Philippot et al ., 2013; Reinhold‐Hurek et al ., 2015; Liu et al ., 2019; Brown et al ., 2020). The ability of plant roots to modify microbial communities is strongest in the endosphere but can reach well beyond the rhizosphere.…”