Cited by 191Genetic and Environmental Crop StudiesGenomics and Phylogenetic StudiesChromosomal and Genetic Variations

Improved pea reference genome and pan-genome highlight genomic features and evolutionary characteristics

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Yang, Tao, Liu, Rong, Luo, Yingfeng, Hu, Songnian, Wang, Dong, Wang, Chenyu, Pandey, Manish K., Ge, Song +16 more·2022·Nature Genetics

Abstract

Complete and accurate reference genomes and annotations provide fundamental resources for functional genomics and crop breeding. Here we report a de novo assembly and annotation of a pea cultivar ZW6 with contig N50 of 8.98 Mb, which features a 243-fold increase in contig length and evident improvements in the continuity and quality of sequence in complex repeat regions compared with the existing one. Genome diversity of 118 cultivated and wild pea demonstrated that Pisum abyssinicum is a separate species different from P. fulvum and P. sativum within Pisum . Quantitative trait locus analyses uncovered two known Mendel’s genes related to stem length ( Le/le ) and seed shape ( R/r ) as well as some candidate genes for pod form studied by Mendel. A pan-genome of 116 pea accessions was constructed, and pan-genes preferred in P. abyssinicum and P. fulvum showed distinct functional enrichment, indicating the potential value of them as pea breeding resources in the future.

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  • MUMmer 4.0 introduces improved speed and memory usage through parallel processing of input query sequences.

    “In addition, MUMmer 4.0 introduces improved speed and memory usage through parallel processing of input query sequences [20].”

    From Whole-Genome Alignment: Methods, Challenges, and Future Directions (2024) · cites this paper as [20]

    The Methods section (Pisum pan-genome assembly, annotation and PAV analysis; page unavailable) says the authors used MUMmer v4.0 to align contigs. The References list calls MUMmer4 a fast genome-alignment system, but our copy does not address improved memory usage or parallel processing of input query sequences; searches for those features found no supporting passage. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

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  1. [1]Meyer RS Purugganan MD Evolution of crop species: genetics of domestication and diversification Nat. Rev. Genet. 2013 14 840 852 10.1038/nrg3605 24240513 · DOI
  2. [2]Olsen K Wendel J Crop plants as models for understanding plant adaptation and diversification Front. Plant. Sci. 2013 4 290 10.3389/fpls.2013.00290 23914199 PMC3729982 · DOI
  3. [3]Bevan MW Genomic innovation for crop improvement Nature 2017 543 346 354 10.1038/nature22011 28300107 · DOI
  4. [4]Yuan Y Bayer PE Batley J Edwards D Improvements in genomic technologies: application to crop genomics Trends Biotechnol. 2017 35 547 558 10.1016/j.tibtech.2017.02.009 28284542 · DOI
  5. [5]Edwards D Batley J Snowdon RJ Accessing complex crop genomes with next-generation sequencing Theor. Appl. Genet. 2013 126 1 11 10.1007/s00122-012-1964-x 22948437 · DOI
  6. [6]Jiao Y Improved maize reference genome with single-molecule technologies Nature 2017 546 524 527 10.1038/nature22971 28605751 PMC7052699 · DOI
  7. [7]Zhou Z Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean Nat. Biotechnol. 2015 33 408 414 10.1038/nbt.3096 25643055 · DOI
  8. [8]Varshney RK Whole-genome resequencing of 292 pigeonpea accessions identifies genomic regions associated with domestication and agronomic traits Nat. Genet. 2017 49 1082 1088 10.1038/ng.3872 28530677 · DOI
  9. [9]Wang WS Genomic variation in 3,010 diverse accessions of Asian cultivated rice Nature 2018 557 43 49 10.1038/s41586-018-0063-9 29695866 PMC6784863 · DOI
  10. [10]Wei T Whole-genome resequencing of 445 Lactuca accessions reveals the domestication history of cultivated lettuce Nat. Genet. 2021 53 752 760 10.1038/s41588-021-00831-0 33846635 · DOI
  11. [11]Wu J Resequencing of 683 common bean genotypes identifies yield component trait associations across a north–south cline Nat. Genet. 2020 52 118 125 10.1038/s41588-019-0546-0 31873299 · DOI
  12. [12]Feuk L Marshall CR Wintle RF Scherer SW Structural variants: changing the landscape of chromosomes and design of disease studies Hum. Mol. Genet. 2006 15 R57 R66 10.1093/hmg/ddl057 16651370 · DOI
  13. [13]Wang Y Copy number variation at the GL7 locus contributes to grain size diversity in rice Nat. Genet. 2015 47 944 948 10.1038/ng.3346 26147619 · DOI
  14. [14]Alonge M Major impacts of widespread structural variation on gene expression and crop improvement in tomato Cell 2020 182 145 161 10.1016/j.cell.2020.05.021 32553272 PMC7354227 · DOI
  15. [15]Kou Y Evolutionary genomics of structural variation in asian rice (Oryza sativa) domestication Mol. Biol. Evol. 2020 37 3507 3524 10.1093/molbev/msaa185 32681796 PMC7743901 · DOI
  16. [16]Liu Y Pan-genome of wild and cultivated soybeans Cell 2020 182 162 176 10.1016/j.cell.2020.05.023 32553274 · DOI
  17. [17]Zhou Y The population genetics of structural variants in grapevine domestication Nat. Plants 2019 5 965 979 10.1038/s41477-019-0507-8 31506640 · DOI · Paper page
  18. [18]Khan AW Super-pangenome by integrating the wild side of a species for accelerated crop improvement Trends Plant Sci. 2020 25 148 158 10.1016/j.tplants.2019.10.012 31787539 PMC6988109 · DOI
  19. [19]Tettelin H Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome” Proc. Natl Acad. Sci. USA 2005 102 13950 13955 10.1073/pnas.0506758102 16172379 PMC1216834 · DOI
  20. [20]Golicz AA Batley J Edwards D Towards plant pangenomics Plant Biotechnol. J. 2016 14 1099 1105 10.1111/pbi.12499 26593040 PMC11388911 · DOI
  21. [21]Golicz AA Bayer PE Bhalla PL Batley J Edwards D Pangenomics comes of age: from bacteria to plant and animal applications Trends Plant Sci. 2020 36 132 145 31882191
  22. [22]Gao L The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor Nat. Genet. 2019 51 1044 1051 10.1038/s41588-019-0410-2 31086351 · DOI
  23. [23]Dolezel J Greilhuber J Nuclear genome size: are we getting closer? Cytometry A 2010 77 635 642 10.1002/cyto.a.20915 20583277 · DOI
  24. [24]Smýkal P Pea (Pisum sativum L.) in the genomic era Agronomy 2012 2 74 115 10.3390/agronomy2020074 · DOI
  25. [25]Tayeh N Genomic tools in pea breeding programs: status and perspectives Front. Plant Sci. 2015 6 1037 10.3389/fpls.2015.01037 26640470 PMC4661580 · DOI
  26. [26]Guillon F Champ MM Carbohydrate fractions of legumes: uses in human nutrition and potential for health Br. J. Nutr. 2002 88 S293 S306 10.1079/BJN2002720 12498630 · DOI
  27. [27]Dahl WJ Foster LM Tyler RT Review of the health benefits of peas (Pisum sativum L.) Br. J. Nutr. 2012 108 S3 S10 10.1017/S0007114512000852 22916813 · DOI · Paper page
  28. [28]MacWilliam S Wismer M Kulshreshtha S Life cycle and economic assessment of Western Canadian pulse systems: the inclusion of pulses in crop rotations Agr. Syst. 2014 123 43 53 10.1016/j.agsy.2013.08.009 · DOI
  29. [29]Ellis TH Hofer JM Timmerman-Vaughan GM Coyne CJ Hellens RP Mendel, 150 years on Trends Plant Sci. 2011 16 590 596 10.1016/j.tplants.2011.06.006 21775188 · DOI
  30. [30]Reid JB Ross JJ Mendel’s genes: toward a full molecular characterization Genetics 2011 189 3 10 10.1534/genetics.111.132118 21908742 PMC3176118 · DOI
  31. [31]Zohary D Hopf M Domestication of pulses in the Old World: legumes were companions of wheat and barley when agriculture began in the Near East Science 1973 182 887 894 10.1126/science.182.4115.887 17737521 · DOI
  32. [32]Smýkal P Phylogeny, phylogeography and genetic diversity of the Pisum genus Plant Genet. Resour. 2010 9 4 18 10.1017/S147926211000033X · DOI
  33. [33]Smýkal P Legume crops phylogeny and genetic diversity for science and breeding Crit. Rev. Plant Sci. 2015 34 43 104 10.1080/07352689.2014.897904 · DOI
  34. [34]Kreplak J A reference genome for pea provides insight into legume genome evolution Nat. Genet. 2019 51 1411 1422 10.1038/s41588-019-0480-1 31477930 · DOI
  35. [35]Roberts RJ Carneiro MO Schatz MC The advantages of SMRT sequencing Genome Biol. 2013 14 405 10.1186/gb-2013-14-6-405 23822731 PMC3953343 · DOI
  36. [36]Chaisson MJP Resolving the complexity of the human genome using single-molecule sequencing Nature 2015 517 608 611 10.1038/nature13907 25383537 PMC4317254 · DOI
  37. [37]Sun X Phased diploid genome assemblies and pan-genomes provide insights into the genetic history of apple domestication Nat. Genet. 2020 52 1423 1432 10.1038/s41588-020-00723-9 33139952 PMC7728601 · DOI
  38. [38]Tayeh N Development of two major resources for pea genomics: the GenoPea 13.2K SNP array and a high-density, high-resolution consensus genetic map Plant J. 2015 84 1257 1273 10.1111/tpj.13070 26590015 · DOI
  39. [39]Hufford MB Comparative population genomics of maize domestication and improvement Nat. Genet. 2012 44 808 811 10.1038/ng.2309 22660546 PMC5531767 · DOI
  40. [40]Chen H Patterson N Reich D Population differentiation as a test for selective sweeps Genome Res. 2010 20 393 402 10.1101/gr.100545.109 20086244 PMC2840981 · DOI
  41. [41]Bhattacharyya MK Smith AM Ellis TH Hedley C Martin C The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme Cell 1990 60 115 122 10.1016/0092-8674(90)90721-P 2153053 · DOI
  42. [42]Martin DN Proebsting WM Hedden P Mendel’s dwarfing gene: cDNAs from the Le alleles and function of the expressed proteins Proc. Natl Acad. Sci. USA 1997 94 8907 8911 10.1073/pnas.94.16.8907 9238076 PMC23192 · DOI
  43. [44]Coyne CJ Potential and limits of exploitation of crop wild relatives for pea, lentil, and chickpea improvement Legume Sci. 2020 2 e36 10.1002/leg3.36 · DOI
  44. [45]Smýkal P From Mendel’s discovery on pea to today’s plant genetics and breeding Theor. Appl. Genet. 2016 129 2267 2280 10.1007/s00122-016-2803-2 27717955 · DOI
  45. [46]Ye CY Fan L Orphan crops and their wild relatives in the genomic era Mol. Plant 2021 14 27 39 10.1016/j.molp.2020.12.013 33346062 · DOI
  46. [47]Morrell PL Buckler ES Ross-Ibarra J Crop genomics: advances and applications Nat. Rev. Genet. 2012 13 85 96 10.1038/nrg3097 22207165 · DOI
  47. [48]Pandey AK Omics resources and omics-enabled approaches for achieving high productivity and improved quality in pea (Pisum sativum L.) Theor. Appl. Genet. 2021 134 755 776 10.1007/s00122-020-03751-5 33433637 · DOI
  48. [49]Zong XX Analysis of a diverse global Pisum sp collection and comparison to a Chinese local P. sativum collection with microsatellite markers Theor. Appl. Genet. 2009 118 193 204 10.1007/s00122-008-0887-z 18815768 · DOI
  49. [50]Liu R Population genetic structure and classification of cultivated and wild pea (Pisum sp.) based on morphological traits and SSR markers J. Syst. Evol. 2022 60 85 100 10.1111/jse.12710 · DOI
  50. [51]Maxted, N. & Ambrose, M. in Plant Genetic Resources of Legumes in the Mediterranean (eds Maxted, N. & Bennet, S. J.) 181–190 (Springer, 2001).
  51. [52]Kosterin OE Bogdanova VS Relationship of wild and cultivated forms of Pisum L. as inferred from an analysis of three markers, of the plastid, mitochondrial and nuclear genomes Genet. Resour. Crop Evol. 2008 55 735 755 10.1007/s10722-007-9281-y · DOI
  52. [53]Bogdanova VS Cryptic divergences in the genus Pisum L. (peas), as revealed by phylogenetic analysis of plastid genomes Mol. Phylogenet. Evol. 2018 129 280 290 10.1016/j.ympev.2018.09.002 30195476 · DOI
  53. [55]Weeden NF Domestication of Pea (Pisum sativum L.): the case of the Abyssinian pea Front. Plant Sci. 2018 9 515 10.3389/fpls.2018.00515 29720994 PMC5915832 · DOI
  54. [57]Hellwig T Abbo S Ophir R Phylogeny and disparate selection signatures suggest two genetically independent domestication events in pea (Pisum L.) Plant J. 2022 110 419 439 10.1111/tpj.15678 35061306 PMC9303476 · DOI
  55. [58]Hradilová I A combined comparative transcriptomic, metabolomic, and anatomical analyses of two key domestication traits: pod dehiscence and seed dormancy in pea (Pisum sp.) Front. Plant. Sci. 2017 8 542 10.3389/fpls.2017.00542 28487704 PMC5404241 · DOI
  56. [59]Parker TA Lo S Gepts P Pod shattering in grain legumes: emerging genetic and environment-related patterns Plant Cell 2021 33 179 199 10.1093/plcell/koaa025 33793864 PMC8136915 · DOI
  57. [60]Zhang M Progress in soybean functional genomics over the past decade Plant Biotechnol. J. 2022 20 256 282 10.1111/pbi.13682 34388296 PMC8753368 · DOI
  58. [62]Weeden NF Brauner S Przyborowski JA Genetic analysis of pod dehiscence in pea (Pisum sativum L.) Cell. Mol. Biol. Lett. 2002 7 657 663 12378224
  59. [63]Sun L GmHs1-1, encoding a calcineurin-like protein, controls hard-seededness in soybean Nat. Genet. 2015 47 939 943 10.1038/ng.3339 26098868 · DOI
  60. [64]Wang M Parallel selection on a dormancy gene during domestication of crops from multiple families Nat. Genet. 2018 50 1435 1441 10.1038/s41588-018-0229-2 30250128 · DOI
  61. [65]Sato Y Morita R Nishimura M Yamaguchi H Kusaba M Mendel’s green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway Proc. Natl Acad. Sci. USA 2007 104 14169 14174 10.1073/pnas.0705521104 17709752 PMC1955798 · DOI
  62. [66]Hellens RP Identification of Mendel’s white flower character PLoS ONE 2010 5 e13230 10.1371/journal.pone.0013230 20949001 PMC2952588 · DOI
  63. [67]Varshney RK A chickpea genetic variation map based on the sequencing of 3,366 genomes Nature 2021 599 622 627 10.1038/s41586-021-04066-1 34759320 PMC8612933 · DOI
  64. [68]Hare EE Johnston JS Genome size determination using flow cytometry of propidium iodide-stained nuclei Methods Mol. Biol. 2011 772 3 12 10.1007/978-1-61779-228-1_1 22065429 · DOI
  65. [69]Marçais G Kingsford C A fast, lock-free approach for efficient parallel counting of occurrences of k-mers Bioinformatics 2011 27 764 770 10.1093/bioinformatics/btr011 21217122 PMC3051319 · DOI · Paper page
  66. [70]Wang M Evolutionary dynamics of 3D genome architecture following polyploidization in cotton Nat. Plants 2018 4 90 97 10.1038/s41477-017-0096-3 29379149 · DOI
  67. [71]Koren S Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation Genome Res. 2017 27 722 736 10.1101/gr.215087.116 28298431 PMC5411767 · DOI
  68. [72]Walker BJ Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement PLoS ONE 2014 9 e112963 10.1371/journal.pone.0112963 25409509 PMC4237348 · DOI
  69. [73]Roach MJ Schmidt SA Borneman AR Purge Haplotigs: allelic contig reassignment for third-gen diploid genome assemblies BMC Bioinformatics 2018 19 460 10.1186/s12859-018-2485-7 30497373 PMC6267036 · DOI
  70. [74]Yeo S Coombe L Warren RL Chu J Birol I ARCS: scaffolding genome drafts with linked reads Bioinformatics 2018 34 725 731 10.1093/bioinformatics/btx675 29069293 PMC6030987 · DOI
  71. [75]Warren RL LINKS: Scalable, alignment-free scaffolding of draft genomes with long reads GigaScience 2015 4 35 10.1186/s13742-015-0076-3 26244089 PMC4524009 · DOI
  72. [76]Durand NC Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments Cell Syst. 2016 3 95 98 10.1016/j.cels.2016.07.002 27467249 PMC5846465 · DOI
  73. [77]Dudchenko O De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds Science 2017 356 92 95 10.1126/science.aal3327 28336562 PMC5635820 · DOI
  74. [78]Robinson JT Juicebox.js provides a cloud-based visualization system for Hi-C data Cell Syst. 2018 6 256 258 10.1016/j.cels.2018.01.001 29428417 PMC6047755 · DOI
  75. [79]Tang H ALLMAPS: robust scaffold ordering based on multiple maps Genome Biol. 2015 16 3 10.1186/s13059-014-0573-1 25583564 PMC4305236 · DOI
  76. [80]Altschul SF Gish W Miller W Myers EW Lipman DJ Basic local alignment search tool J. Mol. Biol. 1990 215 403 410 10.1016/S0022-2836(05)80360-2 2231712 · DOI · Paper page
  77. [81]Kent WJ BLAT–the BLAST-like alignment tool Genome Res. 2002 12 656 664 11932250 PMC187518
  78. [82]Shen W Le S Li Y Hu F SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation PLoS ONE 2016 11 e0163962 10.1371/journal.pone.0163962 27706213 PMC5051824 · DOI · Paper page
  79. [83]Waterhouse RM BUSCO applications from quality assessments to gene prediction and phylogenomics Mol. Biol. Evol. 2018 35 543 548 10.1093/molbev/msx319 29220515 PMC5850278 · DOI · Paper page
  80. [84]Rhie A Walenz BP Koren S Phillippy AM Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies Genome Biol. 2020 21 245 10.1186/s13059-020-02134-9 32928274 PMC7488777 · DOI · Paper page
  81. [85]Li H Durbin R Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 2009 25 1754 1760 10.1093/bioinformatics/btp324 19451168 PMC2705234 · DOI · Paper page
  82. [86]Li H Minimap2: pairwise alignment for nucleotide sequences Bioinformatics 2018 34 3094 3100 10.1093/bioinformatics/bty191 29750242 PMC6137996 · DOI · Paper page
  83. [87]Ou S Chen J Jiang N Assessing genome assembly quality using the LTR Assembly Index (LAI) Nucleic Acids Res. 2018 46 e126 30107434 PMC6265445
  84. [88]Ellinghaus D Kurtz S Willhoeft U LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons BMC Bioinformatics 2008 9 18 10.1186/1471-2105-9-18 18194517 PMC2253517 · DOI
  85. [89]Xu Z Wang H LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons Nucleic Acids Res. 2007 35 W265 W268 10.1093/nar/gkm286 17485477 PMC1933203 · DOI
  86. [90]Ou S Jiang N LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons Plant Physiol. 2018 176 1410 1422 10.1104/pp.17.01310 29233850 PMC5813529 · DOI
  87. [91]Ou S Jiang N LTR_FINDER_parallel: parallelization of LTR_FINDER enabling rapid identification of long terminal repeat retrotransposons Mob. DNA 2019 10 48 10.1186/s13100-019-0193-0 31857828 PMC6909508 · DOI
  88. [92]Kim D Langmead B Salzberg SL HISAT: a fast spliced aligner with low memory requirements Nat. Methods 2015 12 357 360 10.1038/nmeth.3317 25751142 PMC4655817 · DOI · Paper page
  89. [93]Pertea M Kim D Pertea GM Leek JT Salzberg SL Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown Nat. Protoc. 2016 11 1650 1667 10.1038/nprot.2016.095 27560171 PMC5032908 · DOI
  90. [94]Niknafs YS Pandian B Iyer HK Chinnaiyan AM Lyer MK TACO produces robust multisample transcriptome assemblies from RNA-seq Nat. Methods 2017 14 68 70 10.1038/nmeth.4078 27869815 PMC5199618 · DOI
  91. [95]Haas BJ Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies Nucleic Acids Res. 2003 31 5654 5666 10.1093/nar/gkg770 14500829 PMC206470 · DOI
  92. [96]Hoff KJ Lomsadze A Borodovsky M Stanke M Whole-genome annotation with BRAKER Methods Mol. Biol. 2019 1962 65 95 10.1007/978-1-4939-9173-0_5 31020555 PMC6635606 · DOI
  93. [97]Gremme G Brendel V Sparks ME Kurtz S Engineering a software tool for gene structure prediction in higher organisms Inf. Softw. Technol. 2005 47 965 978 10.1016/j.infsof.2005.09.005 · DOI
  94. [99]Mistry J Finn RD Eddy SR Bateman A Punta M Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions Nucleic Acids Res. 2013 41 e121 10.1093/nar/gkt263 23598997 PMC3695513 · DOI
  95. [100]El-Gebali S The Pfam protein families database in 2019 Nucleic Acids Res. 2019 47 D427 D432 10.1093/nar/gky995 30357350 PMC6324024 · DOI · Paper page
  96. [101]Consortium TU UniProt: a worldwide hub of protein knowledge Nucleic Acids Res. 2019 47 D506 D515 10.1093/nar/gky1049 30395287 PMC6323992 · DOI · Paper page
  97. [102]Ogata H KEGG: Kyoto encyclopedia of genes and genomes Nucleic Acids Res. 1999 27 29 34 10.1093/nar/27.1.29 9847135 PMC148090 · DOI · Paper page
  98. [103]Ghosh S Chan CK Analysis of RNA-seq data using TopHat and Cufflinks Methods Mol. Biol. 2016 1374 339 361 10.1007/978-1-4939-3167-5_18 26519415 · DOI
  99. [104]Jones P InterProScan 5: genome-scale protein function classification Bioinformatics 2014 30 1236 1240 10.1093/bioinformatics/btu031 24451626 PMC3998142 · DOI
  100. [105]Cantalapiedra CP eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale Mol. Biol. Evol. 2021 38 5825 5829 10.1093/molbev/msab293 34597405 PMC8662613 · DOI
  101. [108]Wang Y MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity Nucleic Acids Res. 2012 40 e49 10.1093/nar/gkr1293 22217600 PMC3326336 · DOI
  102. [109]Tang H An improved genome release (version Mt4.0) for the model legume Medicago truncatula BMC Genomics 2014 15 312 10.1186/1471-2164-15-312 24767513 PMC4234490 · DOI
  103. [111]Danecek P The variant call format and VCFtools Bioinformatics 2011 27 2156 2158 10.1093/bioinformatics/btr330 21653522 PMC3137218 · DOI
  104. [112]Cingolani P A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPsin the genome of Drosophila melanogaster strain w1118; iso-2; iso-3 Fly 2012 6 80 92 10.4161/fly.19695 22728672 PMC3679285 · DOI · Paper page
  105. [113]Rausch T DELLY: structural variant discovery by integrated paired-end and split-read analysis Bioinformatics 2012 28 333 339 10.1093/bioinformatics/bts378 PMC3436805 22962449 · DOI
  106. [114]Danecek P McCarthy SA BCFtools/csq: haplotype-aware variant consequences Bioinformatics 2017 33 2037 2039 10.1093/bioinformatics/btx100 28205675 PMC5870570 · DOI · Paper page
  107. [115]Price MN Dehal PS Arkin AP FastTree: computing large minimum evolution trees with profiles instead of a distance matrix Mol. Biol. Evol. 2009 26 1641 1650 10.1093/molbev/msp077 19377059 PMC2693737 · DOI · Paper page
  108. [116]Alexander DH Novembre J Lange K Fast model-based estimation of ancestry in unrelated individuals Genome Res. 2009 19 1655 1664 10.1101/gr.094052.109 19648217 PMC2752134 · DOI · Paper page
  109. [117]Purcell S PLINK: a tool set for whole-genome association and population-based linkage analyses Am. J. Hum. Genet. 2007 81 559 575 10.1086/519795 17701901 PMC1950838 · DOI · Paper page
  110. [118]Zhang C Dong SS Xu JY He WM Yang TL PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files Bioinformatics 2019 35 1786 1788 10.1093/bioinformatics/bty875 30321304 · DOI
  111. [119]Quinlan AR Hall IM BEDTools: a flexible suite of utilities for comparing genomic features Bioinformatics 2010 26 841 842 10.1093/bioinformatics/btq033 20110278 PMC2832824 · DOI · Paper page
  112. [120]Bradbury PJ TASSEL: software for association mapping of complex traits in diverse samples Bioinformatics 2007 23 2633 2635 10.1093/bioinformatics/btm308 17586829 · DOI
  113. [121]Broman KW Wu H Sen S Churchill GA R/qtl: QTL mapping in experimental crosses Bioinformatics 2003 19 889 890 10.1093/bioinformatics/btg112 12724300 · DOI
  114. [122]Gonda I Sequencing-based bin map construction of a tomato mapping population, facilitating high-resolution quantitative trait loci detection Plant Genome 2019 12 180010 10.3835/plantgenome2018.02.0010 PMC12809921 30951101 · DOI
  115. [123]Churchill GA Doerge RW Empirical threshold values for quantitative trait mapping Genetics 1994 138 963 971 10.1093/genetics/138.3.963 7851788 PMC1206241 · DOI
  116. [124]Ouellette LA Reid RW Blanchard SG Brouwer CR LinkageMapView-rendering high-resolution linkage and QTL maps Bioinformatics 2018 34 306 307 10.1093/bioinformatics/btx576 28968706 PMC5860205 · DOI
  117. [125]Li D Liu CM Luo R Sadakane K Lam TW MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Bioinformatics 2015 31 1674 1676 10.1093/bioinformatics/btv033 25609793 · DOI
  118. [126]Zimin AV The MaSuRCA genome assembler Bioinformatics 2013 29 2669 2677 10.1093/bioinformatics/btt476 23990416 PMC3799473 · DOI
  119. [127]Fu L Niu B Zhu Z Wu S Li W CD-HIT: accelerated for clustering the next-generation sequencing data Bioinformatics 2012 28 3150 3152 10.1093/bioinformatics/bts565 23060610 PMC3516142 · DOI · Paper page
  120. [128]Alonge M RaGOO: fast and accurate reference-guided scaffolding of draft genomes Genome Biol. 2019 20 224 10.1186/s13059-019-1829-6 31661016 PMC6816165 · DOI
  121. [129]Glick L Mayrose I Panoramic: A package for constructing eukaryotic pan-genomes Mol. Ecol. Resour. 2021 21 1393 1403 10.1111/1755-0998.13344 33533167 · DOI
  122. [130]Marçais G MUMmer4: A fast and versatile genome alignment system PLoS Comput. Biol. 2018 14 e1005944 10.1371/journal.pcbi.1005944 29373581 PMC5802927 · DOI · Paper page
  123. [132]Li H The Sequence Alignment/Map format and SAMtools Bioinformatics 2009 25 2078 2079 10.1093/bioinformatics/btp352 19505943 PMC2723002 · DOI · Paper page
  124. [133]Page AJ Roary: rapid large-scale prokaryote pan genome analysis Bioinformatics 2015 31 3691 3693 10.1093/bioinformatics/btv421 26198102 PMC4817141 · DOI · Paper page
  125. [134]Huerta-Cepas J eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses Nucleic Acids Res. 2019 47 D309 D314 10.1093/nar/gky1085 30418610 PMC6324079 · DOI
  126. [135]Tian T agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update Nucleic Acids Res. 2017 45 W122 W129 10.1093/nar/gkx382 28472432 PMC5793732 · DOI
  127. [136]Chen C TBtools: An integrative toolkit developed for interactive analyses of big biological data Mol. Plant 2020 13 1194 1202 10.1016/j.molp.2020.06.009 32585190 · DOI

Cited by

Sorted by citations

Authors
Yang, T., Liu, R., Luo, Y., Hu, S., Wang, D., Wang, C., Pandey, M. K., Ge, S., Xu, Q., Li, N., Li, G., Huang, Y., Saxena, R. K., Ji, Y., Li, M., Yan, X., He, Y., Liu, Y., Wang, X., Xiang, C., Varshney, R. K., Ding, H., Gao, S., & Zong, X.
Affiliations
  • Chinese Academy of Agricultural Sciences (CN)
  • Chinese Academy of Sciences (CN)
  • Shandong Academy of Agricultural Sciences (CN)
  • International Crops Research Institute for the Semi-Arid Tropics (IN)
  • Northwest A&F University (CN)
  • Shandong Normal University (CN)
  • Yunnan Academy of Agricultural Sciences (CN)
  • Qinghai University (CN)
  • Sichuan Academy of Agricultural Sciences (CN)
  • Murdoch University (AU)
Corresponding author
  • Varshney, Rajeev K.
  • Ding, Hanfeng
  • Gao, Shenghan
  • Zong, Xuxiao
Venue
Nature Genetics
Published
2022-09-22
Volume
54
Issue
10
Pages
1553-1563
ISSN
  • 1061-4036 (ISSN-L)
  • 1546-1718
OpenAlex
W4296683311
Cited by
191
References
4
Citations by year
2026: 46 · 2025: 56 · 2024: 53 · 2023: 33 · 2022: 3
FWCI
21.13
Type
journal article
Language
en
Open access
Locations
  • Nature Genetics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Open Access Repository of ICRISAT (International Crops Research Institute for the Semi-Arid Tropics) (acceptedVersion)
  • Murdoch University Research Portal (submittedVersion, cc-by)
  • Murdoch University Research Portal (submittedVersion)
  • Institute of Botany, CAS Institutional Repository (submittedVersion)
Funders
  • Murdoch University
  • National Natural Science Foundation of China (2018YFD1000701, CARS-08, 2130135, 31801428, 2018YFD1000700)
  • Chinese Academy of Agricultural Sciences
  • Shandong Academy of Agricultural Sciences
  • Agricultural Variety Improvement Project of Shandong Province (2019LZGC017, SDAIT-15-01, CARS-08)
  • Agricultural Science and Technology Innovation Program
  • Youth Innovation Promotion Association
  • Modern Agricultural Technology Industry System of Shandong province
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetic and Environmental Crop Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
Keywords
pea, Pisum, de novo genome assembly, genome annotation, pan-genome, Pisum abyssinicum, Pisum fulvum, Pisum sativum, genomic diversity, quantitative trait loci, Mendelian inheritance, stem length, seed shape, crop breeding
MeSH terms
Plant Breeding, Biological Evolution, Pisum sativum, Genomics, Quantitative Trait Loci

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