Background: Plant-associated microbiomes, which are shaped by host and environmental factors, support their hosts by providing nutrients and attenuating abiotic and biotic stresses. Although host genetic factors involved in plant growth and immunity are known to shape compositions of microbial communities, the effects of host evolution on microbial communities are not well understood. Results: We show evidence that both host speciation and domestication shape seed bacterial and fungal community structures. Genome types of rice contributed to compositional variations of both communities, showing a significant phylosymbiosis with microbial composition. Following the domestication, abundance inequality of bacterial and fungal communities also commonly increased. However, composition of bacterial community was relatively conserved, whereas fungal membership was dramatically changed. These domestication effects were further corroborated when analyzed by a random forest model. With these changes, hub taxa of inter-kingdom networks were also shifted from fungi to bacteria by domestication. Furthermore, maternal inheritance of microbiota was revealed as a major path of microbial transmission across generations. Conclusions: Our findings show that evolutionary processes stochastically affect overall composition of microbial communities, whereas dramatic changes in environments during domestication contribute to assembly of microbiotas in deterministic ways in rice seed. This study further provides new insights on host evolution and microbiome, the starting point of the holobiome of plants, microbial communities, and surrounding environments. Background The evolution of life on Earth is driven by natural selection, biased mutation, genetic drift, genetic hitchhiking, and gene flow. Regardless of plants, animals, or microorganisms, it has been ongoing for millions of years. Unlike the majority of organisms, crop plants have undergone a distinct evolutionary process called domestication. Plant domestication began~12,000 years ago and 353 food crop plants including rice, wheat, barley, potato, and tomato have undergone domestication [1]. Most crop plants have been selected and been bred for better yield and quality by anthropogenic intervention. In rice, the evolution spans about 15 million years [2]. In the genus Oryza, there are 22 wild relatives which are distributed in Asia, Africa, Australia, and America (Fig. 1). Polyploidization and other evolutionary events contribute to speciation of Oryza species [3]. With the speciation, 8000-9000 years ago, O. sativa subsp. japonica, O. sativa subsp. indica, and O. glaberrima were domesticated from the wild relatives, O. rufipogon, O. nivara, and O. barthii, respectively [2]. These domesticated rice species have been further diversified by breeding to acquire desirable agronomic traits. The phenotypes of the humans, animals, and plants are determined not only by their own genetic makeups but by their associated microbial communities. Hostassociated microbial communities show signi...

The plant microbiome, the consortium of microbes surrounding a plant, has potential for improving crop productivity and sustainability. Despite the necessity of agriculturally applicable microbiomes, plant microbiome studies have been conducted in noncrop plants because of the relative easiness of research. However, in order to make plant microbiomes useful for agriculture, a crop plant-based model is needed. In parallel, overlooked parts of microbiomes other than the bacteria-centered research need to be considered to expand our understandings on microbiomes to the ecosystem level. Beyond the microbial composition, functional properties of microbiomes over time and space will help us to select appropriate microbes that can support crop plants by providing stage-specific functions. Less explored communities such as fungi and protists also can provide novel insights on compositional and functional dynamics of each community, including interkingdom or multitrophic interactions. Finally, identification of host factors on functional microbiomes using genetic information of both the host and the microbiomes will shift host-centered breeding to parallel breeding of host and microbiome. This review will give basic and collective information on the rice microbiome and foster the establishment of a crop plant-based model to meet agricultural needs.

Vertical transmission of microbes is crucial for the persistence of host-associated microbial communities. Although vertical transmission of seed microbes has been reported from diverse plants, ecological mechanisms and dynamics of microbial communities from parent to progeny remain scarce. Here we reveal the veiled ecological mechanism governing transmission of bacterial and fungal communities in rice across two consecutive seasons. We identify 29 bacterial and 34 fungal members transmitted across generations. Abundance-based regression models allow to classify colonization types of the microbes. We find that they are late colonizers dominating each community at the ripening stage. Ecological models further show that the observed temporal colonization patterns are affected by niche change and neutrality. Source-sink modeling reveals that parental seeds and stem endosphere are major origins of progeny seed microbial communities. This study gives empirical evidence for ecological mechanism and dynamics of bacterial and fungal communities as an ecological continuum during seed-to-seed transmission.

Seeds harbor not only genetic information about plants but also microbial communities affecting plants’ vigor. Knowledge on the movement and formation of seed microbial communities during plant development remains insufficient. Here, we address this knowledge gap by investigating endophytic bacterial and fungal communities of seeds, seedlings, and adult rice plants. We found that seed coats act as microbial niches for seed bacterial and fungal communities. The presence or absence of the seed coat affected taxonomic composition and diversity of bacterial and fungal communities associated with seeds and seedlings. Ordination analysis showed that niche differentiation between above- and belowground compartments leads to compositional differences in endophytic bacterial and fungal communities originating from seeds. Longitudinal tracking of the composition of microbial communities from field-grown rice revealed that bacterial and fungal communities originating from seeds persist in the leaf, stem, and root endospheres throughout the life cycle. Our study provides ecological insights into the assembly of the initial endophytic microbial communities of plants from seeds.

Rheumatoid arthritis (RA) is closely associated with the oral and gut microbiomes. Fungal cell wall components initiate inflammatory arthritis in mouse models. However, little is known regarding the role of the fungal community in the pathogenesis of RA. To evaluate the association between RA and the gut microbiome, investigations of bacterial and fungal communities in patients with RA are necessary. Therefore, we investigated the compositions and associations of fecal bacterial and fungal communities in 30 healthy controls and 99 patients with RA. The relative abundances of Bifidobacterium and Blautia decreased, whereas the relative abundance of Streptococcus increased, in patients with RA. The relative abundance of Candida in the fecal fungal community was higher in patients with RA than in healthy controls, while the relative abundance of Aspergillus was higher in healthy controls than in patients with RA. Candida species-specific gene amplification showed that C. albicans was the most abundant species of Candida . Ordination analysis and random forest classification models supported the findings of structural changes in bacterial and fungal communities. Aspergillus was the core fecal fungal genus in healthy controls, although Saccharomyces spp. are typically predominant in Western cohorts. In addition, bacterial–fungal association analyses showed that the hub node had shifted from fungi to bacteria in patients with RA. The finding of fungal dysbiosis in patients with RA suggests that fungi play critical roles in the fecal microbial communities and pathogenesis of RA.