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 flowering plant life cycle consists of alternating haploid (gametophyte) and diploid (sporophyte) generations, where the sporophytic generation begins with fertilization of haploid gametes. In Arabidopsis, genome-wide DNA demethylation is required for normal development, catalyzed by the DEMETER (DME) DNA demethylase in the gamete companion cells of male and female gametophytes. In the sporophyte, postembryonic growth and development are largely dependent on the activity of numerous stem cell niches, or meristems. Analyzing Arabidopsis plants homozygous for a loss-of-function dme-2 allele, we show that DME influences many aspects of sporophytic growth and development. dme-2 mutants exhibited delayed seed germination, variable root hair growth, aberrant cellular proliferation and differentiation followed by enhanced de novo shoot formation, dysregulation of root quiescence and stomatal precursor cells, and inflorescence meristem (IM) resurrection. We also show that sporophytic DME activity exerts a profound effect on the transcriptome of developing Arabidopsis plants, including discrete groups of regulatory genes that are misregulated in dme-2 mutant tissues, allowing us to potentially link phenotypes to changes in specific gene expression pathways. These results show that DME plays a key role in sporophytic development and suggest that DME-mediated active DNA demethylation may be involved in the maintenance of stem cell activities during the sporophytic life cycle in Arabidopsis.

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.

Microbial co-occurrence network analysis is being widely used for data exploration in plant microbiome research. Still, challenges lie in how well these microbial networks represent natural microbial communities and how well we can interpret and extract eco-evolutionary insights from the networks. Although many technical solutions have been proposed, in this perspective, we touch on the grave problem of kingdom-level bias in network representation and interpretation. We underscore the eco-evolutionary significance of using cross-kingdom (bacterial-fungal) co-occurrence networks to increase the network’s representability of natural communities. To do so, we demonstrate how ecosystem-level interpretation of plant microbiome evolution changes with and without multi-kingdom analysis. Then, to overcome oversimplified interpretation of the networks stemming from the stereotypical dichotomy between bacteria and fungi, we recommend three avenues for ecological interpretation: (1) understanding dynamics and mechanisms of co-occurrence networks through generalized Lotka-Volterra and consumer-resource models, (2) finding alternative ecological explanations for individual negative and positive fungal-bacterial edges, and (3) connecting cross-kingdom networks to abiotic and biotic (host) environments.

The soil environment determines plants’ health and performance during their life cycle. Therefore, ecological understanding on variations in soil environments, including physical, chemical, and biological properties, is crucial for managing agricultural fields. Here, we present a comprehensive and extensive blueprint of the bacterial, archaeal, and fungal communities in rice paddy soils with differing soil types and chemical properties. We discovered that natural variations of soil nutrients are important factors shaping microbial diversity. The responses of microbial diversity to soil nutrients were related to the distribution of microbial trophic lifestyles (oligotrophy and copiotrophy) in each community. The compositional changes of bacterial and archaeal communities in response to soil nutrients were mainly governed by oligotrophs, whereas copiotrophs were mainly involved in fungal compositional changes. Compositional shift of microbial communities by fertilization is linked to switching of microbial trophic lifestyles. Random forest models demonstrated that depletion of prokaryotic oligotrophs and enrichment of fungal copiotrophs are the dominant responses to fertilization in low-nutrient conditions, whereas enrichment of putative copiotrophs was important in high-nutrient conditions. Network inference also revealed that trophic lifestyle switching appertains to decreases in intra- and inter-kingdom microbial associations, diminished network connectivity, and switching of hub nodes from oligotrophs to copiotrophs. Our work provides ecological insight into how soil nutrient-driven variations in microbial communities affect soil health in modern agricultural systems.