A syntelog-based pan-genome provides insights into rice domestication and de-domestication

Abstract

Background Asian rice is one of the world’s most widely cultivated crops. Large-scale resequencing analyses have been undertaken to explore the domestication and de-domestication genomic history of Asian rice, but the evolution of rice is still under debate. Results Here, we construct a syntelog-based rice pan-genome by integrating and merging 74 high-accuracy genomes based on long-read sequencing, encompassing all ecotypes and taxa of Oryza sativa and Oryza rufipogon. Analyses of syntelog groups illustrate subspecies divergence in gene presence-and-absence and haplotype composition and identify massive genomic regions putatively introgressed from ancient Geng/japonica to ancient Xian/indica or its wild ancestor, including almost all well-known domestication genes and a 4.5-Mbp centromere-spanning block, supporting a single domestication event in main rice subspecies. Genomic comparisons between weedy and cultivated rice highlight the contribution from wild introgression to the emergence of de-domestication syndromes in weedy rice. Conclusions This work highlights the significance of inter-taxa introgression in shaping diversification and divergence in rice evolution and provides an exploratory attempt by utilizing the advantages of pan-genomes in evolutionary studies.

Population genomic analysis unravels the evolutionary roadmap of pericarp color in rice

“…A considerable amount of archaeological and genomic evidence has been proposed to infer the origin of rice ( Molina et al., 2011 ; Huang et al., 2012b ; Gross and Zhao, 2014 ; Civáň et al., 2015 ; Choi et al., 2017 ; Choi and Purugganan, 2018 ; Wang et al., 2018 ; Zheng et al., 2021 ; Wu et al., 2023 ). The evolutionary trajectory of single domestication with multiple origins (i.e., GJ was first domesticated from wild rice, and XI originated from proto-GJ by introgression to local wild rice) has been well documented on the basis of genomic data ( Huang et al., 2012b ; Choi et al., 2017 ; Choi and Purugganan, 2018 ; Wu et al., 2023 ). The history of rice dispersal has also been reconstructed using whole-genome sequences ( Gutaker et al., 2020 ).…”

“…The evolutionary trajectory of rice has attracted significant attention in the last 10 years (e.g., Huang et al., 2012b ; Civáň et al., 2015 ; Choi et al., 2017 ; Jing et al., 2023 ; Wu et al., 2023 ). Specific efforts have been undertaken to unravel the domestication trajectory of red rice ( Sweeney et al, 2007 ; Gross and Olsen, 2010 ).…”

“…The major-effect loci ( qSD7-1 and qPC7 ) that overlap with the Rc locus in weedy rice have been studied in several population genomic studies ( Li et al., 2017 ; Qiu et al., 2017 ). Reversion of Rc to a functional state in weedy rice has been attributed to spontaneous back mutations ( Sweeney et al, 2007 ; Cui et al., 2016 ; Sun et al., 2018 ), gene flow from wild rice ( Song et al., 2014 ; Wedger et al., 2019 ; Wu et al., 2023 ), or standing variation from older landraces that lack the domestication allele ( Qiu et al., 2020 ; Wu et al., 2022 ).…”

Porous borders at the wild-crop interface promote weed adaptation in Southeast Asia

“…Here we examine the evolution of weedy rice in Southeast Asia, a region of sympatry with wild rice, in comparison to temperate weed stains, to assess the role of wild rice introgression in the evolution and adaptation of these tropical weed strains. Our population genomic inferences reveal that in comparison to weedy rice strains in temperate regions, which appear to be descended almost exclusively from domesticated rice ancestors (either directly via de-domestication or indirectly via crop-weed or weed-weed hybridization) 28 , 30 , 40 , 41 , Southeast Asian weedy rice presents a far more dynamic and heterogeneous picture of weedy crop relatives and their mechanisms of adaptation in the presence of reproductively compatible wild species. Our study thereby provides an evolutionary perspective on how adaptive introgression from wild relatives can overcome the ‘cost of domestication’ in agricultural weeds that are descended from domesticated ancestors.…”

Current status of community resources and priorities for weed genomics research

“…comm.) Leersia perrieri Cutgrass 12 12 0.267 [ 175 ] Oryza sativa f. spontanea Weedy rice 12 12 0.37 [ 176 ] Panicum miliaceum Wild proso millet 9 18 0.85 [ 177 ] Poa annua Annual bluegrass 7 14 1.78 [ 178 ] 1.89 [ 129 ] Poa infirma Early meadow-grass 7 7 1.17 [ 179 ] 1.13 [ 179 ] Poa supina Supine bluegrass 7 7 0.66 [ 179 ] 0.64 [ 179 ] Poa trivialis Roughstalk bluegrass 7 7 1.35 [ 180 ] Pueraria montana var. lobata Kudzu 11 11 0.98 [ 181 ] Setaria viridis Green foxtail 9 9 …”