Frontiers of soybean pan-genome studies
Received date: 2023-12-29
Revised date: 2024-02-09
Online published: 2024-02-22
Supported by
National Natural Science Foundation of China(32201775);National Natural Science Foundation of China(U22A20473);CAS Project for Young Scientists in Basic Research(YSBR-078)
Artificial domestication provided the original motivation to the blooming of agriculture, following with the dramatic change of the genetic background of crops and livestock. According to theory and technology upgradation that contributing to the omics, we appreciate using the pan-genome instead of single reference genome for crop study. By comparison and integration of multiple genomes under the guidance of pan-genome theory, we can estimate the genomic information range of a species, leading to a global understanding of its genetic diversity. Combining pan-genome with large size chromosomal structural variations, high throughput population resequencing, and multi-omics data, we can profoundly study the genetic basis behind species traits we focus on. Soybean is one of the most important commercial crops over the world. It is also essential to our food security. Dissecting the formation of genetic diversity and the causal loci of key agricultural traits of soybean will make the modern soybean breeding more efficiently. In this review, we summarize the core idea of pan-genome and clarified the characteristics of construction strategies of pan-genome such as de novo/mapping assembly, iterative assembly and graph-based genome. Then we used the soybean pan-genome work as a case study to introduce the general way to study pan-genome. We highlighted the contribution of structural variation (SV) to the evolution/domestication of soybean and its value in understanding the genetic bases of agronomy traits. By those, we approved the value of graph-based pan-genome for data integration and SV calculation. Future research directions are also discussed for crop genomics and data science.
Key words： soybean; pan-genome; structural variation; evolution; domestication
Yucheng Liu, Yanting Shen, Zhixi Tian . Frontiers of soybean pan-genome studies[J]. Hereditas(Beijing), 2024 , 46(3) : 183 -198 . DOI: 10.16288/j.yczz.23-321
| [1] | Clark JW, Donoghue PCJ. Whole-genome duplication and plant macroevolution. Trends Plant Sci, 2018, 23(10): 933-945. |
| [2] | Danilevicz MF, Tay Fernandez CG, Marsh JI, Bayer PE, Edwards D. Plant pangenomics: approaches, applications and advancements. Curr Opin Plant Biol, 2020, 54: 18-25. |
| [3] | Saxena RK, Edwards D, Varshney RK. Structural variations in plant genomes. Brief Funct Genomics, 2014, 13(4): 296-307. |
| [4] | Golicz AA, Batley J, Edwards D. Towards plant pangenomics. Plant Biotechnol J, 2016, 14(4): 1099-1105. |
| [5] | Tao YF, Zhao XR, Mace E, Henry R, Jordan D. Exploring and exploiting pan-genomics for crop improvement. Mol Plant, 2019, 12(2): 156-169. |
| [6] | Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen TM, Mora M, Scarselli M, Margarit y Ros I, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou LW, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O'Connor KJB, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci USA, 2005, 102(39): 13950-13955. |
| [7] | Baker M. De novo genome assembly: what every biologist should know. Nat Methods, 2012, 9(4): 333-337. |
| [8] | Edger PP, Poorten TJ, VanBuren R, Hardigan MA, Colle M, McKain MR, Smith RD, Teresi SJ, Nelson ADL, Wai CM, Alger EI, Bird KA, Yocca AE, Pumplin N, Ou SJ, Ben-Zvi G, Brodt A, Baruch K, Swale T, Shiue L, Acharya CB, Cole GS, Mower JP, Childs KL, Jiang N, Lyons E, Freeling M, Puzey JR, Knapp SJ. Origin and evolution of the octoploid strawberry genome. Nat Genet, 2019, 51(3): 541-547. |
| [9] | Huang SF, Kang MJ, Xu AL. HaploMerger2: rebuilding both haploid sub-assemblies from high-heterozygosity diploid genome assembly. Bioinformatics, 2017, 33(16): 2577-2579. |
| [10] | Zhang JS, Zhang XT, Tang HB, Zhang Q, Hua XT, Ma XK, Zhu F, Jones T, Zhu XG, Bowers J, Wai CM, Zheng CF, Shi Y, Chen S, Xu XM, Yue JJ, Nelson DR, Huang LX, Li Z, Xu HM, Zhou D, Wang YJ, Hu WC, Lin JS, Deng YJ, Pandey N, Mancini M, Zerpa D, Nguyen JK, Wang LM, Yu L, Xin YH, Ge LF, Arro J, Han JO, Chakrabarty S, Pushko M, Zhang WP, Ma YH, Ma PP, Lv MJ, Chen FM, Zheng GY, Xu JS, Yang ZH, Deng F, Chen XQ, Liao ZY, Zhang XX, Lin ZC, Lin H, Yan HS, Kuang Z, Zhong WM, Liang PP, Wang GF, Yuan Y, Shi JX, Hou JX, Lin JX, Jin JJ, Cao PJ, Shen QC, Jiang Q, Zhou P, Ma YY, Zhang XD, Xu RR, Liu J, Zhou YM, Jia HF, Ma Q, Qi R, Zhang ZL, Fang JP, Fang HK, Song JJ, Wang MJ, Dong GR, Wang G, Chen Z, Ma T, Liu H, Dhungana SR, Huss SE, Yang XP, Sharma A, Trujillo JH, Martinez MC, Hudson M, Riascos JJ, Schuler M, Chen LQ, Braun DM, Li L, Yu QY, Wang JP, Wang K, Schatz MC, Heckerman D, Van Sluys MA, Souza GM, Moore PH, Sankoff D, VanBuren R, Paterson AH, Nagai C, Ming R. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet, 2018, 50(11): 1565-1573. |
| [11] | Sherman RM, Salzberg SL. Pan-genomics in the human genome era. Nat Rev Genet, 2020, 21(4): 243-254. |
| [12] | Ni LB, Liu YC, Ma X, Liu TF, Yang XY, Wang Z, Liang QJ, Liu SL, Zhang M, Wang Z, Shen YT, Tian ZX. Pan-3D genome analysis reveals structural and functional differentiation of soybean genomes. Genome Biol, 2023, 24(1): 12. |
| [13] | Hirsch CN, Foerster JM, Johnson JM, Sekhon RS, Muttoni G, Vaillancourt B, Pe?agaricano F, Lindquist E, Pedraza MA, Barry K, de Leon N, Kaeppler SM, Buell CR. Insights into the maize pan-genome and pan-transcriptome. Plant Cell, 2014, 26(1): 121-135. |
| [14] | Vernikos G, Medini D, Riley DR, Tettelin H. Ten years of pan-genome analyses. Curr Opin Microbiol, 2015, 23: 148-154. |
| [15] | De Coster W, Weissensteiner MH, Sedlazeck FJ.Towards population-scale long-read sequencing. Nat Rev Genet, 2021, 22(9): 572-587. |
| [16] | Gordon SP, Contreras-Moreira B, Woods DP, Des Marais DL, Burgess D, Shu SQ, Stritt C, Roulin AC, Schackwitz W, Tyler L, Martin J, Lipzen A, Dochy N, Phillips J, Barry K, Geuten K, Budak H, Juenger TE, Amasino R, Caicedo AL, Goodstein D, Davidson P, Mur LAJ, Figueroa M, Freeling M, Catalan P, Vogel JP. Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. Nat Commun, 2017, 8(1): 2184. |
| [17] | Li YH, Zhou GY, Ma JX, Jiang WK, Jin LG, Zhang ZH, Guo Y, Zhang JB, Sui Y, Zheng LT, Zhang SS, Zuo QY, Shi XH, Li YF, Zhang WK, Hu YY, Kong GY, Hong HL, Tan B, Song J, Liu ZX, Wang YS, Ruan H, Yeung CKL, Liu J, Wang HL, Zhang LJ, Guan RX, Wang KJ, Li WB, Chen SY, Chang RZ, Jiang Z, Jackson SA, Li RQ, Qiu LJ. De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat Biotechnol, 2014, 32(10): 1045-1052. |
| [18] | Stein JC, Yu Y, Copetti D, Zwickl DJ, Zhang L, Zhang CJ, Chougule K, Gao DY, Iwata A, Goicoechea JL, Wei SR, Wang J, Liao Y, Wang MH, Jacquemin J, Becker C, Kudrna D, Zhang JW, Londono CEM, Song X, Lee S, Sanchez P, Zuccolo A, Ammiraju JSS, Talag J, Danowitz A, Rivera LF, Gschwend AR, Noutsos C, Wu CC, Kao SM, Zeng JW, Wei FJ, Zhao Q, Feng Q, El Baidouri M, Carpentier MC, Lasserre E, Cooke R, da Rosa Farias D, da Maia LC, Dos Santos RS, Nyberg KG, McNally KL, Mauleon R, Alexandrov N, Schmutz J, Flowers D, Fan CZ, Weigel D, Jena KK, Wicker T, Chen MS, Han B, Henry R, Hsing YC, Kurata N, de Oliveira AC, Panaud O, Jackson SA, Machado CA, Sanderson MJ, Long MY, Ware D, Wing RA.Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet, 2018, 50(2): 285-296. |
| [19] | Gao L, Gonda I, Sun HH, Ma QY, Bao K, Tieman DM, Burzynski-Chang EA, Fish TL, Stromberg KA, Sacks GL, Thannhauser TW, Foolad MR, Diez MJ, Blanca J, Canizares J, Xu YM, van der Knaap E, Huang SW, Klee HJ, Giovannoni JJ, Fei ZQ. The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor. Nat Genet, 2019, 51(6): 1044-1051. |
| [20] | Hübner S, Bercovich N, Todesco M, Mandel JR, Odenheimer J, Ziegler E, Lee JS, Baute GJ, Owens GL, Grassa CJ, Ebert DP, Ostevik KL, Moyers BT, Yakimowski S, Masalia RR, Gao LX, ?ali? I, Bowers JE, Kane NC, Swanevelder DZH, Kubach T, Mu?os S, Langlade NB, Burke JM, Rieseberg LH. Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance. Nat Plants, 2019, 5(1): 54-62. |
| [21] | Wang WS, Mauleon R, Hu ZQ, Chebotarov D, Tai SS, Wu ZC, Li M, Zheng TQ, Fuentes RR, Zhang F, Mansueto L, Copetti D, Sanciangco M, Palis KC, Xu JL, Sun C, Fu BY, Zhang HL, Gao YM, Zhao XQ, Shen F, Cui X, Yu H, Li ZC, Chen ML, Detras J, Zhou YL, Zhang XY, Zhao Y, Kudrna D, Wang CC, Li R, Jia B, Lu JY, He XC, Dong ZT, Xu JB, Li YH, Wang M, Shi JX, Li J, Zhang DB, Lee S, Hu WS, Poliakov A, Dubchak I, Ulat VJ, Borja FN, Mendoza JR, Ali J, Li J, Gao Q, Niu YC, Yue Z, Naredo MEB, Talag J, Wang XQ, Li JJ, Fang XD, Yin Y, Glaszmann JC, Zhang JW, Li JY, Hamilton RS, Wing RA, Ruan J, Zhang GY, Wei CC, Alexandrov N, McNally KL, Li ZK, Leung H. Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature, 2018, 557(7703): 43-49. |
| [22] | Golicz AA, Bayer PE, Barker GC, Edger PP, Kim H, Martinez PA, Chan CKK, Severn-Ellis A, McCombie WR, Parkin IAP, Paterson AH, Pires JC, Sharpe AG, Tang HB, Teakle GR, Town CD, Batley J, Edwards D. The pangenome of an agronomically important crop plant Brassica oleracea. Nat Commun, 2016, 7: 13390. |
| [23] | Iqbal Z, Caccamo M, Turner I, Flicek P, McVean G. De novo assembly and genotyping of variants using colored de Bruijn graphs. Nat Genet, 2012, 44(2): 226-232. |
| [24] | Audano PA, Sulovari A, Graves-Lindsay TA, Cantsilieris S, Sorensen M, Welch AE, Dougherty ML, Nelson BJ, Shah A, Dutcher SK, Warren WC, Magrini V, McGrath SD, Li YI, Wilson RK, Eichler EE. Characterizing the major structural variant alleles of the human genome. Cell, 2019, 176(3): 663-675. |
| [25] | Eggertsson HP, Kristmundsdottir S, Beyter D, Jonsson H, Skuladottir A, Hardarson MT, Gudbjartsson DF, Stefansson K, Halldorsson BV, Melsted P. GraphTyper 2 enables population-scale genotyping of structural variation using pangenome graphs. Nat Commun, 2019, 10(1): 5402. |
| [26] | Garrison E, Sirén J, Novak AM, Hickey G, Eizenga JM, Dawson ET, Jones W, Garg S, Markello C, Lin MF, Paten B, Durbin R. Variation graph toolkit improves read mapping by representing genetic variation in the reference. Nat Biotechnol, 2018, 36(9): 875-879. |
| [27] | Marcus S, Lee H, Schatz MC. SplitMEM: a graphical algorithm for pan-genome analysis with suffix skips. Bioinformatics, 2014, 30(24): 3476-3483. |
| [28] | Zhao YB, Jia XM, Yang JH, Ling YC, Zhang Z, Yu J, Wu JY, Xiao JF. PanGP: a tool for quickly analyzing bacterial pan-genome profile. Bioinformatics, 2014, 30(9): 1297-1299. |
| [29] | Sirén J, Monlong J, Chang X, Novak AM, Eizenga JM, Markello C, Sibbesen JA, Hickey G, Chang PC, Carroll A, Gupta N, Gabriel S, Blackwell TW, Ratan A, Taylor KD, Rich SS, Rotter JI, Haussler D, Garrison E, Paten B. Pangenomics enables genotyping of known structural variants in 5202 diverse genomes. Science, 2021, 374(6574): abg8871. |
| [30] | Guarracino A, Heumos S, Nahnsen S, Prins P, Garrison E. ODGI: understanding pangenome graphs. Bioinformatics, 2022, 38(13): 3319-3326. |
| [31] | Garrison E, Guarracino A, Heumos S, Villani F, Bao ZG, Tattini L, Hagmann J, Vorbrugg S, Marco-Sola S, Kubica C, Ashbrook DG, Thorell K, Rusholme-Pilcher RL, Liti G, Rudbeck E, Nahnsen S, Yang ZY, Moses MN, Nobrega FL, Wu Y, Chen H, de Ligt J, Sudmant PH, Soranzo N, Colonna V, Williams RW, Prins P. Building pangenome graphs. bioRxiv, 2023. |
| [32] | Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol, 2019, 37(8): 907-915. |
| [33] | Gan XC, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, Kahles A, Bohnert R, Jean G, Derwent P, Kersey P, Belfield EJ, Harberd NP, Kemen E, Toomajian C, Kover PX, Clark RM, Ratsch G, Mott R. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature, 2011, 477(7365): 419-423. |
| [34] | Qin P, Lu HW, Du HL, Wang H, Chen WL, Chen Z, He Q, Ou SJ, Zhang HY, Li XZ, Li XX, Li Y, Liao Y, Gao Q, Tu B, Yuan H, Ma BT, Wang YP, Qian YW, Fan SJ, Li WT, Wang J, He M, Yin JJ, Li T, Jiang N, Chen XW, Liang CZ, Li SG. Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell, 2021, 184(13): 3542-3558. |
| [35] | Zhou Y, Zhang ZY, Bao ZG, Li HB, Lyu YQ, Zan YJ, Wu YY, Cheng L, Fang YH, Wu K, Zhang JZ, Lyu HJ, Lin T, Gao Q, Saha S, Mueller L, Fei ZJ, St?dler T, Xu SZ, Zhang ZW, Speed D, Huang SW. Graph pangenome captures missing heritability and empowers tomato breeding. Nature, 2022, 606(7914): 527-534. |
| [36] | Huang Y, He JX, Xu YT, Zheng WK, Wang SH, Chen P, Zeng B, Yang SZ, Jiang XL, Liu ZS, Wang L, Wang X, Liu SJ, Lu ZH, Liu Z, Yu HW, Yue JQ, Gao JY, Zhou XY, Long CR, Zeng XL, Guo YJ, Zhang WF, Xie ZZ, Li CL, Ma ZC, Jiao WB, Zhang F, Larkin RM, Krueger RR, Smith MW, Ming R, Deng XX, Xu Q. Pangenome analysis provides insight into the evolution of the orange subfamily and a key gene for citric acid accumulation in citrus fruits. Nat Genet, 2023, 55(11): 1964-1975. |
| [37] | Jin SK, Han ZG, Hu Y, Si ZF, Dai F, He L, Cheng Y, Li YQ, Zhao T, Fang L, Zhang TZ. Structural variation (SV)-based pan-genome and GWAS reveal the impacts of SVs on the speciation and diversification of allotetraploid cottons. Mol Plant, 2023, 16(4): 678-693. |
| [38] | Li HB, Wang SH, Chai S, Yang ZQ, Zhang QQ, Xin HJ, Xu YC, Lin SG, Chen XX, Yao ZW, Yang QY, Fei ZJ, Huang SW, Zhang ZH. Graph-based pan-genome reveals structural and sequence variations related to agronomic traits and domestication in cucumber. Nat Commun, 2022, 13(1): 682. |
| [39] | Liu YC, Du HL, Li PC, Shen YT, Peng H, Liu SL, Zhou G-A, Zhang HK, Liu Z, Shi M, Huang XH, Li Y, Zhang M, Wang Z, Zhu BG, Han B, Liang CZ, Tian ZX. Pan-genome of wild and cultivated soybeans. Cell, 2020, 182(1): 162-176. |
| [40] | He Q, Tang S, Zhi H, Chen JF, Zhang J, Liang HK, Alam O, Li HB, Zhang H, Xing LH, Li XK, Zhang W, Wang HL, Shi JP, Du HL, Wu HP, Wang LW, Yang P, Xing L, Yan HS, Song ZQ, Liu JR, Wang HG, Tian X, Qiao ZJ, Feng GJ, Guo RF, Zhu WJ, Ren YM, Hao HB, Li MZ, Zhang AY, Guo EH, Yan F, Li QQ, Liu YL, Tian BH, Zhao XQ, Jia RL, Feng BL, Zhang JW, Wei JH, Lai JS, Jia GQ, Purugganan M, Diao XM. A graph-based genome and pan-genome variation of the model plant Setaria. Nat Genet, 2023, 55(7): 1232-1242. |
| [41] | Chen S, Wang PJ, Kong WL, Chai K, Zhang SC, Yu JX, Wang YB, Jiang MW, Lei WL, Chen X, Wang WL, Gao YY, Qu SY, Wang F, Wang YH, Zhang Q, Gu MY, Fang KX, Ma CL, Sun WJ, Ye NX, Wu HL, Zhang XT. Gene mining and genomics-assisted breeding empowered by the pangenome of tea plant Camellia sinensis. Nat Plants, 2023, 9(12): 1986-1999. |
| [42] | Zhao Q, Feng Q, Lu HY, Li Y, Wang AH, Tian QL, Zhan QL, Lu YQ, Zhang L, Huang T, Wang YC, Fan DL, Zhao Y, Wang ZQ, Zhou CC, Chen JY, Zhu CR, Li WJ, Weng QJ, Xu Q, Wang ZX, Wei XH, Han B, Huang XH. Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet, 2018, 50(2): 278-284. |
| [43] | Song JM, Guan ZL, Hu JL, Guo CC, Yang ZQ, Wang S, Liu DX, Wang B, Lu SP, Zhou R, Xie WZ, Cheng YF, Zhang YT, Liu KD, Yang QY, Chen LL, Guo L. Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nat Plants, 2020, 6(1): 34-45. |
| [44] | Shang LG, Li XX, He HY, Yuan QL, Song YN, Wei ZR, Lin H, Hu M, Zhao FL, Zhang C, Li YH, Gao HS, Wang TY, Liu XP, Zhang H, Zhang Y, Cao SM, Yu XM, Zhang BT, Zhang Y, Tan YQ, Qin M, Ai C, Yang YX, Zhang B, Hu ZQ, Wang HR, Lv Y, Wang YX, Ma J, Wang Q, Lu HW, Wu Z, Liu SL, Sun ZY, Zhang HL, Guo LB, Li ZC, Zhou YF, Li JY, Zhu ZF, Xiong GS, Ruan J, Qian Q. A super pan-genomic landscape of rice. Cell Res, 2022, 32(10): 878-896. |
| [45] | Alonge M, Wang XG, Benoit M, Soyk S, Pereira L, Zhang L, Suresh H, Ramakrishnan S, Maumus F, Ciren D, Levy Y, Harel TH, Shalev-Schlosser G, Amsellem Z, Razifard H, Caicedo AL, Tieman DM, Klee H, Kirsche M, Aganezov S, Ranallo-Benavidez TR, Lemmon ZH, Kim J, Robitaille G, Kramer M, Goodwin S, McCombie WR, Hutton S, Van Eck J, Gillis J, Eshed Y, Sedlazeck FJ, van der Knaap E, Schatz MC, Lippman ZB. Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell, 2020, 182(1): 145-161. |
| [46] | Chen JF, Liu Y, Liu MX, Guo WL, Wang YQ, He Q, Chen WY, Liao Y, Zhang W, Gao YZ, Dong KJ, Ren RY, Yang TY, Zhang LY, Qi MY, Li ZG, Zhao M, Wang HG, Wang JJ, Qiao ZJ, Li HQ, Jiang YM, Liu GQ, Song XQ, Deng YR, Li H, Yan F, Dong Y, Li QQ, Li T, Yang WY, Cui JH, Wang HR, Zhou YF, Zhang XM, Jia GQ, Lu P, Zhi H, Tang S, Diao XM. Pangenome analysis reveals genomic variations associated with domestication traits in broomcorn millet. Nat Genet, 2023, 55(12): 2243-2254. |
| [47] | Gijzen M, Weng CR, Kuflu K, Woodrow L, Yu KF, Poysa V. Soybean seed lustre phenotype and surface protein cosegregate and map to linkage group E. Genome, 2003, 46(4): 659-664. |
| [48] | Jones CD, Begun DJ. Parallel evolution of chimeric fusion genes. Proc Natl Acad Sci USA, 2005, 102(32): 11373-11378. |
| [49] | Watanabe S, Hideshima R, Xia ZJ, Tsubokura Y, Sato S, Nakamoto Y, Yamanaka N, Takahashi R, Ishimoto M, Anai T, Tabata S, Harada K.Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics, 2009, 182(4): 1251-1262. |
| [50] | Tsubokura Y, Watanabe S, Xia ZJ, Kanamori H, Yamagata H, Kaga A, Katayose Y, Abe J, Ishimoto M, Harada K. Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean. Ann Bot, 2014, 113(3): 429-441. |
| [51] | Lam HM, Xu X, Liu X, Chen WB, Yang GH, Wong FL, Li MW, He WM, Qin N, Wang B, Li J, Jian M, Wang J, Shao GH, Wang J, Sun SSM, Zhang GY. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet, 2010, 42(12): 1053-1059. |
| [52] | Lu SJ, Zhao XH, Hu YL, Liu SL, Nan HY, Li XM, Fang C, Cao D, Shi XY, Kong LP, Su T, Zhang FG, Li SC, Wang Z, Yuan XH, Cober ER, Weller JL, Liu BH, Hou XL, Tian ZX, Kong FJ. Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield. Nat Genet, 2017, 49(5): 773-779. |
| [53] | Torkamaneh D, Laroche J, Tardivel A, O'Donoughue L, Cober E, Rajcan I, Belzile F. Comprehensive description of genomewide nucleotide and structural variation in short-season soya bean. Plant Biotechnol J, 2018, 16(3): 749-759. |
| [54] | Zhou ZK, Jiang Y, Wang Z, Gou ZH, Lyu J, Li WY, Yu YJ, Shu LP, Zhao YJ, Ma YM, Fang C, Shen YT, Liu TF, Li CC, Li Q, Wu M, Wang M, Wu YS, Dong Y, Wan WT, Wang X, Ding ZL, Gao YD, Xiang H, Zhu BG, Lee SH, Wang W, Tian ZX. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol, 2015, 33(4): 408-414. |
| [55] | Woodworth CM. Inheritance of cotyledon, seed-coat, hilum and pubescence colors in soy-beans. Genetics, 1921, 6(6): 487-553. |
| [56] | Tuteja JH, Clough SJ, Chan WC, Vodkin LO. Tissue- specific gene silencing mediated by a naturally occurring chalcone synthase gene cluster in Glycine max. Plant Cell, 2004, 16(4): 819-835. |
| [57] | Tuteja JH, Zabala G, Varala K, Hudson M, Vodkin LO. Endogenous, tissue-specific short interfering RNAs silence the chalcone synthase gene family in Glycine max seed coats. Plant Cell, 2009, 21(10): 3063-3077. |
| [58] | Wang CS, Todd JJ, Vodkin LO. Chalcone synthase mRNA and activity are reduced in yellow soybean seed coats with dominant I alleles. Plant Physiol, 1994, 105(2): 739-748. |
| [59] | Xie M, Chung CYL, Li MW, Wong FL, Wang X, Liu AL, Wang ZL, Leung AKY, Wong TH, Tong SW, Xiao ZX, Fan KJ, Ng MS, Qi XP, Yang LF, Deng TQ, He LJ, Chen L, Fu AS, Ding Q, He JX, Chung G, Isobe S, Tanabata T, Valliyodan B, Nguyen HT, Cannon SB, Foyer CH, Chan TF, Lam HM. A reference-grade wild soybean genome. Nat Commun, 2019, 10(1): 1216. |
| [60] | Lin S, Cianzio S, Shoemaker R. Mapping genetic loci for iron deficiency chlorosis in soybean. Mol Breeding, 1997, 3(3): 219-229. |
| [61] | Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH. A unified classification system for eukaryotic transposable elements. Nat Rev Genet, 2007, 8(12): 973-982. |
| [62] | Zhuang YB, Wang XT, Li XC, Hu JM, Fan LC, Landis JB, Cannon SB, Grimwood J, Schmutz J, Jackson SA, Doyle JJ, Zhang XS, Zhang DJ, Ma JX. Phylogenomics of the genus Glycine sheds light on polyploid evolution and life-strategy transition. Nat Plants, 2022, 8(3): 233-244. |
| [63] | Wendel JF. The wondrous cycles of polyploidy in plants. Am J Bot, 2015, 102(11): 1753-1756. |
| [64] | Zhao MX, Zhang B, Lisch D, Ma JX. Patterns and consequences of subgenome differentiation provide insights into the nature of paleopolyploidy in plants. Plant Cell, 2017, 29(12): 2974-2994. |
| [65] | Ameur A. Goodbye reference, hello genome graphs. Nat Biotechnol, 2019, 37(8): 866-868. |
| [66] | Bayer PE, Golicz AA, Scheben A, Batley J, Edwards D. Plant pan-genomes are the new reference. Nature Plants, 2020, 6: 914-920. |
| [67] | Lappalainen T, Scott AJ, Brandt M, Hall IM. Genomic analysis in the age of human genome sequencing. Cell, 2019, 177(1): 70-84. |
| [68] | Huang XH, Huang SW, Han B, Li JY. The integrated genomics of crop domestication and breeding. Cell, 2022, 185(15): 2828-2839. |
| [69] | Shi JP, Tian ZX, Lai JS, Huang XH. Plant pan-genomics and its applications. Mol Plant, 2023, 16(1): 168-186. |
| [70] | Lei L, Goltsman E, Goodstein D, Wu GA, Rokhsar DS, Vogel JP. Plant pan-genomics comes of age. Annu Rev Plant Biol, 2021, 72: 411-435. |
| [71] | Yu H, Lin T, Meng XB, Du HL, Zhang JK, Liu GF, Chen MJ, Jing YH, Kou LQ, Li XX, Gao Q, Liang Y, Liu XD, Fan ZL, Liang YT, Cheng ZK, Chen MS, Tian ZX, Wang YH, Chu CC, Zuo JR, Wan JM, Qian Q, Han B, Zuccolo A, Wing RA, Gao CX, Liang CZ, Li JY. A route to de novo domestication of wild allotetraploid rice. Cell, 2021, 184(5): 1156-1170. e14. |
| [72] | Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington JA, Crandall KA, Durbin R, Edwards SV, Forest F, Gilbert MTP, Goldstein MM, Grigoriev IV, Hackett KJ, Haussler D, Jarvis ED, Johnson WE, Patrinos A, Richards S, Castilla-Rubio JC, van Sluys MA, Soltis PS, Xu X, Yang HM. Earth BioGenome Project: sequencing life for the future of life. Proc Natl Acad Sci USA, 2018, 115(17): 4325-4333. |
| [73] | Cheng S, Melkonian M, Smith SA, Brockington SF, Archibald JM, Delaux PM, Li F, Melkonian B, Mavrodiev EV, Sun WJ, Fu Y, Yang HM, Soltis DE, Graham SW, Soltis PS, Liu X, Xu X, Wong GKS. 10KP: a phylodiverse genome sequencing plan. GigaScience, 2018, 7(3): 1-9. |
| [74] | Liu YC, Zhang Y, Liu XN, Shen YT, Tian DM, Yang XY, Liu SL, Ni LB, Zhang Z, Song SH, Tian ZX. SoyOmics: a deeply integrated database on soybean multi-omics. Mol Plant, 2023, 16(5): 794-797. |
| [75] | Han LQ, Zhong WS, Qian J, Jin ML, Tian P, Zhu WC, Zhang HW, Sun YH, Feng JW, Liu XG, Chen G, Farid B, Li RN, Xiong ZM, Tian ZH, Li J, Luo Z, Du DX, Chen SJ, Jin QX, Li JX, Li Z, Liang Y, Jin XM, Peng Y, Zheng C, Ye XN, Yin YJ, Chen H, Li WF, Chen LL, Li Q, Yan JB, Yang F, Li L. A multi-omics integrative network map of maize. Nat Genet, 2023, 55(1): 144-153. |
| [76] | Zhou P, Silverstein KAT, Ramaraj T, Guhlin J, Denny R, Liu JQ, Farmer AD, Steele KP, Stupar RM, Miller JR, Tiffin P, Mudge J, Young ND. Exploring structural variation and gene family architecture with De novo assemblies of 15 Medicago genomes. BMC Genomics, 2017, 18(1): 261. |
| [77] | Ou LJ, Li D, Lv JH, Chen WC, Zhang ZQ, Li XF, Yang BZ, Zhou SD, Yang S, Li WG, Gao HZ, Zeng Q, Yu HY, Ouyang B, Li F, Liu F, Zheng JY, Liu YH, Wang J, Wang BB, Dai XZ, Ma YQ, Zou XX. Pan-genome of cultivated pepper (Capsicum) and its use in gene presence-absence variation analyses. New Phytol, 2018, 220(2): 360-363. |
| [78] | Yu JY, Golicz AA, Lu K, Dossa K, Zhang YX, Chen JF, Wang LH, You J, Fan DD, Edwards D, Zhang XR. Insight into the evolution and functional characteristics of the pan-genome assembly from sesame landraces and modern cultivars. Plant Biotechnol J, 2019, 17(5): 881-892. |
| [79] | Jayakodi M, Padmarasu S, Haberer G, Bonthala VS, Gundlach H, Monat C, Lux T, Kamal N, Lang D, Himmelbach A, Ens J, Zhang XQ, Angessa TT, Zhou GF, Tan C, Hill C, Wang PH, Schreiber M, Boston LB, Plott C, Jenkins J, Guo Y, Fiebig A, Budak H, Xu DD, Zhang J, Wang CC, Grimwood J, Schmutz J, Guo GG, Zhang GP, Mochida K, Hirayama T, Sato K, Chalmers KJ, Langridge P, Waugh R, Pozniak CJ, Scholz U, Mayer KFX, Spannagl M, Li C, Mascher M, Stein N. The barley pan-genome reveals the hidden legacy of mutation breeding. Nature, 2020, 588(7837): 284-289. |
| [80] | Varshney RK, Roorkiwal M, Sun S, Bajaj P, Chitikineni A, Thudi M, Singh NP, Du X, Upadhyaya HD, Khan AW, Wang Y, Garg V, Fan Gy, Cowling WA, Crossa J, Gentzbittel L, Voss-Fels KP, Valluri VK, Sinha P, Singh VK, Ben C, Rathore A, Punna R, Singh MK, Tar'an B, Bharadwaj C, Yasin M, Pithia MS, Singh S, Soren KR, Kudapa H, Jarquín D, Cubry P, Hickey LT, Dixit GP, Thuillet AC, Hamwieh A, Kumar S, Deokar AA, Chaturvedi SK, Francis A, Howard R, Chattopadhyay D, Edwards D, Lyons E, Vigouroux Y, Hayes BJ, von Wettberg E, Datta SK, Yang HM, Nguyen HT, Wang J, Siddique KHM, Mohapatra T, Bennetzen JL, Xu X, Liu X. A chickpea genetic variation map based on the sequencing of 3,366 genomes. Nature, 2021, 599(7886): 622-627. |
| [81] | Li JY, Yuan DJ, Wang PC, Wang QQ, Sun ML, Liu ZP, Si H, Xu ZP, Ma YZ, Zhang BY, Pei LL, Tu LL, Zhu LF, Chen LL, Lindsey K, Zhang XL, Jin SX, Wang MJ. Cotton pan-genome retrieves the lost sequences and genes during domestication and selection. Genome Biol, 2021, 22(1): 119. |
| [82] | Tao YF, Luo H, Xu JB, Cruickshank A, Zhao XR, Teng F, Hathorn A, Wu XY, Liu YM, Shatte T, Jordan D, Jing HC, Mace E. Extensive variation within the pan-genome of cultivated and wild sorghum. Nat Plants, 2021, 7(6): 766-773. |
| [83] | Hufford MB, Seetharam AS, Woodhouse MR, Chougule KM, Ou SJ, Liu JN, Ricci WA, Guo TT, Olson A, Qiu YJ, Della Coletta R, Tittes S, Hudson AI, Marand AP, Wei SR, Lu ZY, Wang B, Tello-Ruiz MK, Piri RD, Wang N, Kim DW, Zeng YB, O'Connor CH, Li XR, Gilbert AM, Baggs E, Krasileva KV, Portwood JL, 2nd, Cannon EKS, Andorf CM, Manchanda N, Snodgrass SJ, Hufnagel DE, Jiang QH, Pedersen S, Syring ML, Kudrna DA, Llaca V, Fengler K, Schmitz RJ, Ross-Ibarra J, Yu JM, Gent JI, Hirsch CN, Ware D, Dawe RK. De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science, 2021, 373(6555): 655-662. |
| [84] | Zhang XH, Liu TJ, Wang JL, Wang P, Qiu Y, Zhao W, Pang S, Li XM, Wang HP, Song JP, Zhang WL, Yang WL, Sun YY, Li XX. Pan-genome of Raphanus highlights genetic variation and introgression among domesticated, wild, and weedy radishes. Mol Plant, 2021, 14(12): 2032-2055. |
| [85] | Li N, He Q, Wang J, Wang BK, Zhao JT, Huang SY, Yang T, Tang YP, Yang SB, Aisimutuola P, Xu RQ, Hu JH, Jia CP, Ma K, Li ZQ, Jiang FL, Gao J, Lan HY, Zhou YF, Zhang XY, Huang SW, Fei ZJ, Wang H, Li HB, Yu QH. Super-pangenome analyses highlight genomic diversity and structural variation across wild and cultivated tomato species. Nat Genet, 2023, 55(5): 852-860. |
| [86] | Wang MJ, Li JY, Qi ZY, Long YX, Pei LL, Huang XH, Grover CE, Du XM, Xia CJ, Wang PC, Liu ZP, You JQ, Tian XH, Ma YZ, Wang RP, Chen XY, He X, Fang DD, Sun YQ, Tu LL, Jin SX, Zhu LF, Wendel JF, Zhang XL. Genomic innovation and regulatory rewiring during evolution of the cotton genus Gossypium. Nat Genet, 2022, 54(12): 1959-1971. |
| [87] | Tang D, Jia YX, Zhang JZ, Li HB, Cheng L, Wang P, Bao ZG, Liu ZH, Feng SS, Zhu XJ, Li DW, Zhu GT, Wang HR, Zhou Y, Zhou YF, Bryan GJ, Buell CR, Zhang CZ, Huang SW. Genome evolution and diversity of wild and cultivated potatoes. Nature, 2022, 606(7914): 535-541. |
| [88] | Wang BB, Hou M, Shi JP, Ku LX, Song W, Li CH, Ning Q, Li X, Li CY, Zhao BB, Zhang RY, Xu H, Bai ZJ, Xia ZC, Wang H, Kong DX, Wei HB, Jing YF, Dai ZY, Wang HHL, Zhu XY, Li CH, Sun X, Wang SS, Yao W, Hou GG, Qi Z, Dai H, Li XM, Zheng HK, Zhang ZX, Li Y, Wang TY, Jiang TJ, Wan ZM, Chen YH, Zhao JR, Lai JS, Wang HY. De novo genome assembly and analyses of 12 founder inbred lines provide insights into maize heterosis. Nat Genet, 2023, 55(2): 312-323. |
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