Abstract

The plastid is an essential organelle in autotrophic plant cells, descending from free-living cyanobacteria and acquired by early eukaryotic cells through endosymbiosis roughly one billion years ago. It contained a streamlined genome (plastome) that is uniparentally inherited and non-recombinant, which makes it an ideal tool for resolving the origin and diversity of plant species and populations. In the present study, a large dataset was amassed by de novo assembling plastomes from 295 common wild rice (Oryza rufipogon Griff.) and 1135 Asian cultivated rice (Oryza sativa L.) accessions, supplemented with 34 plastomes from other Oryza species. From this dataset, the phylogenetic relationships and biogeographic history of O. rufipogon and O. sativa were reconstructed. Our results revealed two major maternal lineages across the two species, which further diverged into nine well supported genetic clusters. Among them, the Or-wj-I/II/III and Or-wi-I/II genetic clusters were shared with cultivated (percentage for each cluster ranging 54.9%∼99.3%) and wild rice accessions. Molecular dating, phylogeographic analyses and reconstruction of population historical dynamics indicated an earlier origin of the Or-wj-I/II genetic clusters from East Asian with at least two population expansions, and later origins of other genetic clusters from multiple regions with one or more population expansions. These results supported a single origin of japonica rice (mainly in Or-wj-I/II) and multiple origins of indica rice (in all five clusters) for the history of rice domestication. The massive plastomic data set presented here provides an important resource for understanding the history and evolution of rice domestication as well as a genomic resources for use in future breeding and conservation efforts.

Highlights

  • The domestication and improvement of wild plant species forms the basis of our current global food system (Hancock, 2004)

  • The highest GC content was observed in the inverted repeats (IRs), followed by the large single copy region (LSC) and SSC, suggesting that different functions and/or evolutionary biases exist between these regions

  • The plastid genome possesses a number of special characteristics such as lack of recombination, conserved gene order and content, and differential rates of mutation (Supplementary Figure 2). These characteristics make plastomes ideally suited in the study of evolution and historical biogeography in plants (Gitzendanner et al, 2018), intergenomic transfer between organelles and nuclear genomes (Ma et al, 2020), plastid genetic engineering (South et al, 2019), and breeding and conservation of important crop germplasm (TontiFilippini et al, 2017; Gao et al, 2019)

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Summary

Introduction

The domestication and improvement of wild plant species forms the basis of our current global food system (Hancock, 2004). Among plant lineages that have been domesticated to feed humans directly, Asian cultivated rice (Oryza sativa L.) is one of the most important given that it provides roughly 20% of the calories consumed by humans worldwide (Smith, 1998). There are numerous well-known examples using organellar DNA in studies of origin, dispersal, and diversity, like the resolution of our own human history using mitochondrial DNA (Ballinger et al, 1992; Forster et al, 2001; Tanaka et al, 2004) and the use of plastid DNA as a standard phylogenetic marker in the Angiosperm Phylogeny Group (APG) classification of flowering plant orders and families (Byng et al, 2016). Pangenomic approaches to plastomic DNA analyses are expected to provide useful insights into the origin, and diversity of numerous domesticated crop species

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