Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

Joshua C Stein ,Richard Cooke ,Kevin G Nyberg ,Dave Flowers ,Jetty S.s Ammiraju ,Jeremy Schmutz ,Detlef Weigel ,Antônio Costa De Oliveira ,Chuanzhu Fan ,Feng Chen ,Kenneth L Mcnally ,Qiang Zhao ,Carlos A Machado ,Éric Lasserre ,Marie-Christine Carpentier ,Andrea R Gschwend ,Scott A Jackson ,Moaine El Baidouri ,Ann Danowitz ,Muhua Wang ,Jianwei Zhang ,Luis Fernando Rivera ,Jun Wang ,Kapeel Chougule ,Dongying Gao ,Bin Han ,Olivier Panaud ,Andrea Zuccolo ,Derrick J Zwickl ,Akihisa Iwata ,Nori Kurata ,Sharon Wei ,Ramil Mauleon ,Luciano Carlos Da Maia ,Xiang Song ,Daniel Da Rosa Farias ,Cheng Chieh Wu ,Dario Copetti ,Shu Min Kao ,Nickolai Alexandrov ,Yeisoo Yu ,Li Zhang ,Railson Schreinert Dos Santos ,Michael J Sanderson ,Jhih Wun Zeng ,Thomas Wicker ,Manyuan Long ,Qi Feng ,Christos Noutsos ,Jayson Talag ,José Luis Goicoechea ,Mingsheng Chen ,Y I Hsing ,Yi Liao ,Carlos E.m Londono ,Paul L Sanchez ,Claude Becker ,Robert J Henry ,Doreen Ware ,Dave Kudrna ,Julie Jacquemin ,Seung‐Hee Lee ,Fu‐Jin Wei ,Kshirod K Jena ,Rod A Wing

doi:10.1038/s41588-018-0040-0

Abstract

The genus Oryza is a model system for the study of molecular evolution over time scales ranging from a few thousand to 15 million years. Using 13 reference genomes spanning the Oryza species tree, we show that despite few large-scale chromosomal rearrangements rapid species diversification is mirrored by lineage-specific emergence and turnover of many novel elements, including transposons, and potential new coding and noncoding genes. Our study resolves controversial areas of the Oryza phylogeny, showing a complex history of introgression among different chromosomes in the young ‘AA’ subclade containing the two domesticated species. This study highlights the prevalence of functionally coupled disease resistance genes and identifies many new haplotypes of potential use for future crop protection. Finally, this study marks a milestone in modern rice research with the release of a complete long-read assembly of IR 8 ‘Miracle Rice’, which relieved famine and drove the Green Revolution in Asia 50 years ago.

Highlights

The genus Oryza stands out in its significance to human civilization and food security with two species having been independently domesticated as rice: Oryza sativa in Asia ~10,000 years ago and Oryza glaberrima in Africa ~3,000 years ago
As a first step toward a deeper evolutionary understanding of the genus, we developed a large array of publicly available genomic tools from BAC libraries[9,10] and BAC-end sequences to physical maps[11,12] and subgenome assemblies[13]
With two independently domesticated species, Oryza has had a significant role in advancing human civilization, leading some ricedependent cultures to revere ‘rice is life’, as exemplified in dramatic fashion ~50 years ago with the release of IR8 in Asia

Summary

Introduction

The genus Oryza stands out in its significance to human civilization and food security with two species having been independently domesticated as rice: Oryza sativa in Asia ~10,000 years ago and Oryza glaberrima in Africa ~3,000 years ago. Because the wild relatives of rice are adapted to different biogeographic ranges (Fig. 1a) and can tolerate many biotic and abiotic stresses[1,2,3,4,5,6], they constitute an important reservoir for crop improvement. Strategies to harness such traits for crop improvement show clear promise, as exemplified by the introgression of bacterial blight resistance (Xa21) from the wild species Oryza longistaminata[7]. Our comparative evolutionary genomics analysis includes these and four previously published genomes (O. sativa vg. japonica (AA)[29] and indica (AA)[30], O. glaberrima (AA)[25] and O. brachyantha (FF)28), which were together reannotated using a common pipeline with the integration of baseline RNA-seq and bisulfite sequencing data

Methods

Results

Conclusion