A syntelog-based pan-genome provides insights into rice domestication and de-domestication.
De-domestication
Domestication
Introgression
Rice pan-genome
Syntelog
Journal
Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660
Informations de publication
Date de publication:
03 08 2023
03 08 2023
Historique:
received:
09
06
2023
accepted:
19
07
2023
medline:
7
8
2023
pubmed:
4
8
2023
entrez:
3
8
2023
Statut:
epublish
Résumé
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. 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. 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.
Sections du résumé
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.
Identifiants
pubmed: 37537691
doi: 10.1186/s13059-023-03017-5
pii: 10.1186/s13059-023-03017-5
pmc: PMC10401782
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
179Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Molina J, Sikora M, Garud N, Flowers JM, Rubinstein S, Reynolds A, et al. Molecular evidence for a single evolutionary origin of domesticated rice. Proc Natl Acad Sci U S A. 2011;108(20):8351–6.
pubmed: 21536870
pmcid: 3101000
Huang X, Kurata N, Wei X, Wang Z, Wang A, Zhao Q, et al. A map of rice genome variation reveals the origin of cultivated rice. Nature. 2012;490(7421):497–501.
pubmed: 23034647
pmcid: 7518720
Civáň P, Craig H, Cox CJ, Brown TA. Three geographically separate domestications of Asian rice. Nat Plants. 2015;1(11):15164.
pubmed: 27251535
pmcid: 4900444
Gross BL, Zhao Z. Archaeological and genetic insights into the origins of domesticated rice. Proc Natl Acad Sci U S A. 2014;111(17):6190–7.
pubmed: 24753573
pmcid: 4035933
Choi JY, Platts AE, Fuller DQ, Hsing Y, Wing RA, Purugganan MD. The rice paradox: multiple origins but single domestication in Asian rice. Mol Biol Evol. 2017;34(4):969–79.
pubmed: 28087768
pmcid: 5400379
Choi JY, Purugganan MD. Multiple origin but single domestication led to Oryza sativa. G3. 2018;8(3):797–803.
pubmed: 29301862
pmcid: 5844301
Wang W, Mauleon R, Hu Z, Chebotarov D, Tai S, Wu Z, et al. Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature. 2018;557(7703):43–9.
pubmed: 29695866
pmcid: 6784863
Carpentier M, Manfroi E, Wei F, Wu H, Lasserre E, Llauro C, et al. Retrotranspositional landscape of Asian rice revealed by 3,000 genomes. Nat Commun. 2019;10(1):24.
pubmed: 30604755
pmcid: 6318337
Zhang F, Wang C, Li M, Cui Y, Shi Y, Wu Z, et al. The landscape of gene-CDS-haplotype diversity in rice: properties, population organization, footprints of domestication and breeding, and implications for genetic improvement. Mol Plant. 2021;14(5):787–804.
pubmed: 33578043
Civáň P, Brown TA. Misconceptions regarding the role of introgression in the origin of Oryza sativa subsp. indica. Front Plant Sci. 2018;9:1750.
pubmed: 30555497
pmcid: 6282103
Chen E, Huang X, Tian Z, Wing RA, Han B. The genomics of Oryza species provides insights into rice domestication and heterosis. Annu Rev Plant Biol. 2019;70:639–65.
pubmed: 31035826
Chen R, Deng Y, Ding Y, Guo J, Qiu J, Wang B, et al. Rice functional genomics: decades’ efforts and roads ahead. Science China Life Sciences. 2022;65(1):33–92.
pubmed: 34881420
Wu D, Lao S, Fan L. De-domestication: an extension of crop evolution. Trends Plant Sci. 2021;26(6):560–74.
pubmed: 33648850
Song B, Chuah T, Tam SM, Olsen KM. Malaysian weedy rice shows its true stripes: wild Oryza and elite rice cultivars shape agricultural weed evolution in southeast Asia. Mol Ecol. 2014;23(20):5003–17.
pubmed: 25231087
Li L, Li Y, Jia Y, Caicedo AL, Olsen KM. Signatures of adaptation in the weedy rice genome. Nat Genet. 2017;49(5):811–4.
pubmed: 28369039
Qiu J, Jia L, Wu D, Weng X, Chen L, Sun J, et al. Diverse genetic mechanisms underlie worldwide convergent rice feralization. Genome Biol. 2020;21(1):70.
pubmed: 32213201
pmcid: 7098168
Zhao Q, Feng Q, Lu H, Li Y, Wang A, Tian Q, et al. Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet. 2018;50(2):278–84.
pubmed: 29335547
Qin P, Lu H, Du H, Wang H, Chen W, Chen Z, et al. Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell. 2021;184(13):3542–58.
pubmed: 34051138
Zhou Y, Chebotarov D, Kudrna D, Llaca V, Lee S, Rajasekar S, et al. A platinum standard pan-genome resource that represents the population structure of Asian rice. Sci Data. 2020;7(1):113.
pubmed: 32265447
pmcid: 7138821
Zhang F, Xue H, Dong X, Li M, Zheng X, Li Z, et al. Long-read sequencing of 111 rice genomes reveals significantly larger pan-genomes. Genome Res. 2022;32(5):853–63.
pubmed: 35396275
pmcid: 9104699
Shang L, Li X, He H, Yuan Q, Song Y, Wei Z, et al. A super pan-genomic landscape of rice. Cell Res. 2022;32(10):878–96.
pubmed: 35821092
pmcid: 9525306
Song J, Xie W, Wang S, Guo Y, Koo D, Kudrna D, et al. Two gap-free reference genomes and a global view of the centromere architecture in rice. Mol Plant. 2021;14(10):1757–67.
pubmed: 34171480
Long Y, Zhao L, Niu B, Su J, Wu H, Chen Y, et al. Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci U S A. 2008;105(48):18871–6.
pubmed: 19033192
pmcid: 2596266
Zhan C, Lei L, Liu Z, Zhou S, Yang C, Zhu X, et al. Selection of a subspecies-specific diterpene gene cluster implicated in rice disease resistance. Nat Plants. 2020;6(12):1447–54.
pubmed: 33299150
Tseng I, Hong C, Yu S, Ho TD. Abscisic acid- and stress-induced highly proline-rich glycoproteins regulate root growth in rice. Plant Physiol. 2013;163(1):118–34.
pubmed: 23886623
pmcid: 3762635
Wu D, Shen E, Jiang B, Feng Y, Tang W, Lao S, et al. Genomic insights into the evolution of Echinochloa species as weed and orphan crop. Nat Commun. 2022;13(1):689.
pubmed: 35115514
pmcid: 8814039
Wang H, Vieira FG, Crawford JE, Chu C, Nielsen R. Asian wild rice is a hybrid swarm with extensive gene flow and feralization from domesticated rice. Genome Res. 2017;27(6):1029–38.
pubmed: 28385712
pmcid: 5453317
Wang M, Li W, Fang C, Xu F, Liu Y, Wang Z, et al. Parallel selection on a dormancy gene during domestication of crops from multiple families. Nat Genet. 2018;50(10):1435–41.
pubmed: 30250128
Wang Z, Wei K, Xiong M, Wang JD, Zhang CQ, Fan XL, et al. Glucan, Water-Dikinase 1 (GWD1), an ideal biotechnological target for potential improving yield and quality in rice. Plant Biotechnol J. 2021;19(12):2606–18.
pubmed: 34416068
pmcid: 8633486
Wang J, Deng Q, Li Y, Yu Y, Liu X, Han Y, et al. Transcription factors Rc and OsVP1 coordinately regulate preharvest sprouting tolerance in red pericarp rice. J Agric Food Chem. 2020;68(50):14748–57.
pubmed: 33264008
Zhu B, Si L, Wang Z, Jingjie Zhu YZ, Shangguan Y, Lu D, et al. Genetic control of a transition from black to straw-white seed hull in rice domestication. Plant Physiol. 2011;155(3):1301–11.
pubmed: 21263038
pmcid: 3046587
Civáň P, Brown TA. Origin of rice (Oryza sativa L.) domestication genes. Genet Resour Crop Evol. 2017;64(6):1125–32.
pubmed: 28736485
pmcid: 5498617
Gutaker RM, Groen SC, Bellis ES, Choi JY, Pires IS, Bocinsky RK, et al. Genomic history and ecology of the geographic spread of rice. Nat Plants. 2020;6(5):492–502.
pubmed: 32415291
Wang Z, Wang W, Xie X, Wang Y, Yang Z, Peng H, et al. Dispersed emergence and protracted domestication of polyploid wheat uncovered by mosaic ancestral haploblock inference. Nat Commun. 2022;13(1):3891.
pubmed: 35794156
pmcid: 9259585
Cheng H, Concepcion GT, Feng X, Zhang H, Li H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat Methods. 2021;18(2):170–5.
pubmed: 33526886
pmcid: 7961889
Guan D, McCarthy SA, Wood J, Howe K, Wang Y, Durbin R. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics. 2020;36(9):2896–8.
pubmed: 31971576
pmcid: 7203741
Vaser R, Sović I, Nagarajan N, Šikić M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 2017;27(5):737–46.
pubmed: 28100585
pmcid: 5411768
Alonge M, Soyk S, Ramakrishnan S, Wang X, Goodwin S, Sedlazeck FJ, et al. Ragoo: fast and accurate reference-guided scaffolding of draft genomes. Genome Biol. 2019;20(1):224.
pubmed: 31661016
pmcid: 6816165
Du H, Yu Y, Ma Y, Gao Q, Cao Y, Chen Z, et al. Sequencing and de novo assembly of a near complete indica rice genome. Nat Commun. 2017;8(1):15324.
pubmed: 28469237
pmcid: 5418594
Sun J, Ma D, Tang L, Zhao M, Zhang G, Wang W, et al. Population genomic analysis and de novo assembly reveal the origin of weedy rice as an evolutionary game. Mol Plant. 2019;12(5):632–47.
pubmed: 30710646
Wang L, Zhao L, Zhang X, Zhang Q, Jia Y, Wang G, et al. Large-scale identification and functional analysis of NLR genes in blast resistance in the Tetep rice genome sequence. Proc Natl Acad Sci. 2019;116(37):18479–87.
pubmed: 31451649
pmcid: 6744916
Ma X, Fan J, Wu Y, Zhao S, Zheng X, Sun C, et al. Whole-genome de novo assemblies reveal extensive structural variations and dynamic organelle-to-nucleus DNA transfers in African and Asian rice. Plant J. 2020;104(3):596–612.
pubmed: 32748498
pmcid: 7693357
Xie X, Du H, Tang H, Tang J, Tan X, Liu W, et al. A chromosome-level genome assembly of the wild rice Oryza rufipogon facilitates tracing the origins of Asian cultivated rice. Science China Life Sciences. 2021;64(2):282–93.
pubmed: 32737856
Choi JY, Lye ZN, Groen SC, Dai X, Rughani P, Zaaijer S, et al. Nanopore sequencing-based genome assembly and evolutionary genomics of circum-basmati rice. Genome Biol. 2020;21(1):21.
pubmed: 32019604
pmcid: 7001208
Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012;9(4):357–9.
pubmed: 22388286
pmcid: 3322381
Ou S, Jiang N. LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol. 2018;176(2):1410–22.
pubmed: 29233850
Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31(19):3210–2.
pubmed: 26059717
Rhie A, Walenz BP, Koren S, Phillippy AM. Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biol. 2020;21(1):245.
pubmed: 32928274
pmcid: 7488777
Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A. MUMmer4: a fast and versatile genome alignment system. Plos Comput Biol. 2018;14(1):e1005944.
pubmed: 29373581
pmcid: 5802927
Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26(7):1641–50.
pubmed: 19377059
pmcid: 2693737
Wu D, Qiu J, Sun J, Song B, Olsen KM, Fan L. Weedy rice, a hidden gold mine in the paddy field. Mol Plant. 2022;15(4):566–8.
pubmed: 35032686
Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience. 2015;4(1):7.
pubmed: 25722852
pmcid: 4342193
Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006;34:W435–9.
pubmed: 16845043
pmcid: 1538822
Salamov AA, Solovyev VV. Ab initio gene finding in Drosophila genomic DNA. Genome Res. 2000;10(4):516–22.
pubmed: 10779491
pmcid: 310882
Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol. 2008;9(1):R7.
pubmed: 18190707
pmcid: 2395244
Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, et al. Interproscan 5: genome-scale protein function classification. Bioinformatics. 2014;30(9):1236–40.
pubmed: 24451626
pmcid: 3998142
Emms DM, Kelly S. Orthofinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20(1):238.
pubmed: 31727128
pmcid: 6857279
Buchfink B, Reuter K, Drost H. Sensitive protein alignments at tree-of-life scale using diamond. Nat Methods. 2021;18(4):366–8.
pubmed: 33828273
pmcid: 8026399
Haas BJ, Delcher AL, Wortman JR, Salzberg SL. DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics. 2004;20(18):3643–6.
pubmed: 15247098
Zheng X, Pang H, Wang J, Yao X, Song Y, Li F, et al. Genomic signatures of domestication and adaptation during geographical expansions of rice cultivation. Plant Biotechnol J. 2022;20(1):16–8.
pubmed: 34664353
Nguyen L, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74.
pubmed: 25371430
Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, et al. A draft sequence of the Neandertal genome. Science. 2010;328(5979):710–22.
pubmed: 20448178
pmcid: 5100745
Martin SH, Davey JW, Jiggins CD. Evaluating the use of ABBA-BABA statistics to locate introgressed loci. Mol Biol Evol. 2015;32(1):244–57.
pubmed: 25246699
Ge SX, Jung D, Yao R. ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics. 2020;36(8):2628–9.
pubmed: 31882993
Jayakodi M, Padmarasu S, Haberer G, Bonthala VS, Gundlach H, Monat C, et al. The barley pan-genome reveals the hidden legacy of mutation breeding. Nature. 2020;588(7837):284–9.
pubmed: 33239781
pmcid: 7759462
Nattestad M, Schatz MC. Assemblytics: a web analytics tool for the detection of variants from an assembly. Bioinformatics. 2016;32(19):3021–3.
pubmed: 27318204
pmcid: 6191160
Wu D, Xie L, Sun Y, Huang Y, Jia L, Dong C, et al., A syntelog-based pan-genome provides insights into rice domestication and de-domestication. Datasets. Genome Sequence Archive. 2023. https://ngdc.cncb.ac.cn/bioproject/browse/PRJCA012143 .
Wu D, Xie L, Sun Y, Huang Y, Jia L, Dong C, et al., A syntelog-based pan-genome provides insights into rice domestication and de-domestication. Datasets. Genome Sequence Archive. 2023. https://ngdc.cncb.ac.cn/bioproject/browse/PRJCA012309 .
Zheng X, Pang H, Wang J, Yao X, Song Y, Li F, et al. Genomic signatures of domestication and adaptation during geographical expansions of rice cultivation. Datasets. European Nucleotide Archive. 2023. https://www.ebi.ac.uk/ena/browser/view/PRJNA657701 .
Wu D, Xie L, Sun Y, Huang Y, Jia L, Dong C, et al. A syntelog-based pan-genome provides insights into rice domestication and de-domestication. 2023. Zenodo Code. https://doi.org/10.5281/zenodo.7196576 .
Wu D, Xie L, Sun Y, Huang Y, Jia L, Dong C, et al., A syntelog-based pan-genome provides insights into rice domestication and de-domestication. Datasets. Genome Variation Map. 2023. https://ngdc.cncb.ac.cn/bioproject/browse/PRJCA018336 .
Wu D, Xie L, Sun Y, Huang Y, Jia L, Dong C, et al. A syntelog-based pan-genome provides insights into rice domestication and de-domestication. 2023. Zenodo. https://doi.org/10.5281/zenodo.7248110 .
Wu D, Xie L, Sun Y, Huang Y, Jia L, Dong C, et al., A syntelog-based pan-genome provides insights into rice domestication and de-domestication. Github. 2023. https://github.com/dongyawu/PangenomeEvolution .
Wu D, Xie L, Sun Y, Huang Y, Jia L, Dong C, et al. A syntelog based pan genome provides insights into rice domestication and de domestication. Zenodo. 2023. https://doi.org/10.5281/zenodo.8157689 .
doi: 10.5281/zenodo.8157689