Rapid diversification of five Oryza AA genomes associated with rice adaptation

Abstract

Comparative genomic analyses among closely related species can greatly enhance our understanding of plant gene and genome evolution. We report de novo-assembled AA-genome sequences for Oryza nivara, Oryza glaberrima, Oryza barthii, Oryza glumaepatula, and Oryza meridionalis. Our analyses reveal massive levels of genomic structural variation, including segmental duplication and rapid gene family turnover, with particularly high instability in defense-related genes. We show, on a genomic scale, how lineage-specific expansion or contraction of gene families has led to their morphological and reproductive diversification, thus enlightening the evolutionary process of speciation and adaptation. Despite strong purifying selective pressures on most Oryza genes, we documented a large number of positively selected genes, especially those genes involved in flower development, reproduction, and resistance-related processes. These diversifying genes are expected to have played key roles in adaptations to their ecological niches in Asia, South America, Africa and Australia. Extensive variation in noncoding RNA gene numbers, function enrichment, and rates of sequence divergence might also help account for the different genetic adaptations of these rice species. Collectively, these resources provide new opportunities for evolutionary genomics, numerous insights into recent speciation, a valuable database of functional variation for crop improvement, and tools for efficient conservation of wild rice germplasm.

Keywords: Oryza; comparative genomics; full-genome sequencing; genomic variation; positive selection.

Fig. 1.

Comparative genomics of the six AA-genome Oryza species. (A) Geographical origins (SI Appendix, Table S1). (B) Comparative genome analysis. The outer circle represents the 12 chromosomes of SAT, along with the densities of genes, DNA transposons, RNA transposons, and other types of genome components labeled as shown in the color matrix (Left). Moving inward, the five sequenced and assembled genomes are symbolized by different colored circles. The heat map beside each circle indicates the average number of indels per kilobase in 50 kb-bins for each genome in comparison to SAT. The inner heat map illustrates the similarity among the six genomes. Blank points show the association constant dN/dS ratios of entire genes estimated by site models for 2,272 1:1 orthologous gene families. SAT centromere positions are signified by black triangles (▲). (C) Phylogeny of the six AA-genome species with BRA as an outgroup. Estimates of divergence time are given at each node, all supported with 100% bootstrap values.

Fig. 2.

Rapid evolution of the Oryza AA genomes. (A) Gene synteny. The collinear region is located on SAT chromosome 7 (279 kb, 2,711,024–2,989,979 kb; Michigan State University 7.0; ref. 60). Orthologous genes (blue boxes), DNA transposons (green boxes), and RNA transposons (light green boxes) are connected by gray lines between genomes. (B) Distribution of genomic SVs from 50 bp to 1 kb in length for the five sequenced genomes in comparison to SAT. The peak at ∼250 bp is due to extensive TE turnover. (C) Numbers of genomic structural insertion (red) and deletion (blue) events are indicated at the terminus of each branch of the rice phylogeny while comparing the SAT genome; the pie charts at each branch terminus illustrate the insertion/deletion ratios.

Fig. 3.

Evolutionary dynamics of rice gene families. (A) Venn diagram showing unique and shared gene families between and among the six AA-genome Oryza species plus BRA. (B) Gene family evolution among the seven Oryza species. Numerical values on each branch of the tree represent numbers of gene gain and/or loss events.

Fig. 4.

PSGs involved in the predicted integrated pathways of rice flower development. Within the genes assigned to categories of “flower development” (GO: 0009908) and “pollination” (GO: 0009856), the 14 genes that are homologs to reproduction-related genes or associated with the flowering process are shown with evidence of positive selection (in red boxes). ASHH2, ABSENT, SMALL, OR HOMEOTIC DISCS 1 HOMOLOG 2; CRY2, CRYPTOCHROME 2; HEN1, HUA ENHANCER 1; le, lemma; lo, lodicule; LHY, LATE ELONGATED HYPOCOTYL; MOS3/SAR3, MODIFIER OF SNC1,3/SUPPRESSOR OF AUXIN RESISTANCE 3; pa, palea; PDIL, PROTEIN DISULFIDE ISOMERASE-LIKE; PEP, PEPPER; PFT1, PHYTOCHROME AND FLOWERING TIME 1; PG, POLYGALACTURONASE; pi, pistil; SEC5, EXOCYST COMPLEX COMPONENT; st, stamen; TAF6, TATA BOX BINDING PROTEIN-ASSOCIATED FACTOR 6; TMS1, THERMOSENSITIVE MALE STERILE 1; VIL1, VERNALIZATION INSENSITIVE 3-LIKE 1; XTH, XYLOGLUCAN ENDOTRANSGLUCOSYLASE/HYDROLASE.