Domestication of Oryza species eco-evolutionarily shapes bacterial and fungal communities in rice seed

Abstract

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 Structure of Rhizosphere Fungal Communities of Wild and Domesticated Rice: Changes in Diversity and Co-occurrence Patterns

“…Studies on the rhizomicrobiomes of O. sativa and their relative wild accessions O. rufipogon have shown that the domesticated rice is different from wild rice due to its long domestication history and some distinct rhizomicrobial groups of wild rice that were gradually eliminated ( Shenton et al, 2016 ; Tian et al, 2017 ; Chang et al, 2021 ). These observations are in accordance with the hypothesis that the plant host coevolved with their rhizomicrobiomes, and that rhizomicrobial communities are primarily determined by a series of changes due to domestication ( Moran and Sloan, 2015 ; Sasse et al, 2017 ; Kim et al, 2020 ).…”

Heterogeneity of the rice microbial community of the Chinese centuries‐old Honghe Hani rice terraces system

“…All four of the unweighted UniFrac distance matrices of microbial communities were significantly correlated with the genetic distances between the rice genotypes they are associated with (Table S7). This result is consistent with previous studies focusing on wild and modern rice varieties (Shenton et al ., 2016; Kim et al ., 2020), maize and other Poaceae (Bouffaud et al ., 2014) suggesting that the evolutionary history of poaceous crop plants has had an impact on the evolutionary history of their microbial communities.…”

“…The microbial community associated with the rice rhizosphere has been the most intensively investigated (Edwards et al ., 2015; Wang et al ., 2016; Edwards et al ., 2018; Moronta‐Barrios et al ., 2018; Ding et al ., 2019). Specifically, several studies have focused on the comparison of the rhizosphere or seed‐associated microbial communities of wild Oryza , rice landraces and modern rice varieties (Shenton et al ., 2016; Shi et al ., 2019; Kim et al ., 2020). For instance, Shenton and colleagues (2016) have shown that the rhizosphere bacterial community of wild Oryza differed substantially from that of cultivated rice in terms of both species richness and composition (Shenton et al ., 2016).…”

“…Interestingly, this study also revealed that landraces had a rhizosphere bacterial community composition that was intermediate between that of wild Oryza and cultivated rice varieties (Shenton et al ., 2016). It is also apparent that fungal communities differ more substantially than bacterial communities between the seed or rhizosphere microbial communities of cultivated varieties and wild Oryza (Shi et al ., 2019; Kim et al ., 2020).…”

Deciphering Core-Phyllomicrobiome of Rice Genotypes Grown in Contrasting Mountain and Island Agroclimatic Zones: Implications for Microbiome Engineering Against Blast Disease

“…Bacterial genera such as Curtobacterium, Enterobacter, Methylobacterium, Microbacterium, and Sphingomonas are frequently reported as the core-spermosphere microbiome of rice [68,69]. Kim et al [70] also reported dominance of Pantoea (42.5 %), Methlyobacterium (11.8 %), Curtobacterium (9.3 %), Pseudomonas (8.7 %), andSphingomonas (8.6 %) on rice spermosphere. They also observed that the seed microbiome appeared to be highly stable and protected owing to their natural encapsulation in the seed coat that enables them to be inherited, known as vertical transmission.…”