BAC- and oligo-FISH mapping reveals chromosome evolution among Vigna angularis, V. unguiculata, and Phaseolus vulgaris

Abstract

Cytogenomic resources have accelerated synteny and chromosome evolution studies in plant species, including legumes. Here, we established the first cytogenetic map of V. angularis (Va, subgenus Ceratotropis) and compared this new map with those of V. unguiculata (Vu, subgenus Vigna) and P. vulgaris (Pv) by BAC-FISH and oligopainting approaches. We mapped 19 Vu BACs and 35S rDNA probes to the 11 chromosome pairs of Va, Vu, and Pv. Vigna angularis shared a high degree of macrosynteny with Vu and Pv, with five conserved syntenic chromosomes. Additionally, we developed two oligo probes (Pv2 and Pv3) used to paint Vigna orthologous chromosomes. We confirmed two reciprocal translocations (chromosomes 2 and 3 and 1 and 8) that have occurred after the Vigna and Phaseolus divergence (~9.7 Mya). Besides, two inversions (2 and 4) and one translocation (1 and 5) have occurred after Vigna and Ceratotropis subgenera separation (~3.6 Mya). We also observed distinct oligopainting patterns for chromosomes 2 and 3 of Vigna species. Both Vigna species shared similar major rearrangements compared to Pv: one translocation (2 and 3) and one inversion (chromosome 3). The sequence synteny identified additional inversions and/or intrachromosomal translocations involving pericentromeric regions of both orthologous chromosomes. We propose chromosomes 2 and 3 as hotspots for chromosomal rearrangements and de novo centromere formation within and between Vigna and Phaseolus. Our BAC- and oligo-FISH mapping contributed to physically trace the chromosome evolution of Vigna and Phaseolus and its application in further studies of both genera.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data availability

All data generated during this study are available in this published paper and its Supplementary Information files.

References

  1. Albert PS, Zhang T, Semrau K, Rouillard JM, Kao YH, Wang CJR, Danilova TV, Jiang J, Birchler JA (2019) Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships. Proc Natl Acad Sci 116:1679–1685. https://doi.org/10.1073/pnas.1813957116

    CAS  Article  PubMed  Google Scholar 

  2. Almeida C, Pedrosa-Harand A (2013) High macro-collinearity between lima bean (Phaseolus lunatus L.) and the common bean (P. vulgaris L.) as revealed by comparative cytogenetic mapping. Theor Appl Genet 126:1909–1916. https://doi.org/10.1007/s00122-013-2106-9

    Article  PubMed  Google Scholar 

  3. Beliveau BJ, Joyce EF, Apostolopoulos N, Yilmaz F, Fonseka CY, McCole RB, Chang Y, Li JB, Senaratne TN, Williams BR, Rouillard JM, Wu CT (2012) Versatile design and synthesis platform for visualizing genomes with Oligopaint FISH probes. Proc Natl Acad Sci 109:21301–21306. https://doi.org/10.1073/pnas.1213818110

    Article  PubMed  Google Scholar 

  4. Betekhtin A, Jenkins G, Hasterok R (2014) Reconstructing the evolution of Brachypodium genomes using comparative chromosome painting. PLoS One 9:e115108. https://doi.org/10.1371/journal.pone.0115108

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Bi Y, Zhao Q, Yan W et al (2019) Flexible chromosome painting based on multiplex PCR of oligonucleotides and its application for comparative chromosome analyses in Cucumis. Plant J. https://doi.org/10.1111/tpj.14600

  6. Bonifácio EM, Fonsêca A, Almeida C, dos Santos KG, Pedrosa-Harand A (2012) Comparative cytogenetic mapping between the lima bean (Phaseolus lunatus L.) and the common bean (P. vulgaris L.). Theor Appl Genet 124:1513–1520. https://doi.org/10.1007/s00122-012-1806-x

    Article  PubMed  Google Scholar 

  7. Braz GT, He L, Zhao H, Zhang T, Semrau K, Rouillard JM, Torres GA, Jiang JM (2018) Comparative oligo-FISH mapping: an efficient and powerful methodology to reveal karyotypic and chromosomal evolution. Genetics 208:513–523. https://doi.org/10.1534/genetics.117.300344

    CAS  Article  PubMed  Google Scholar 

  8. Braz GT, do Vale Martins L, Zhang T, Albert PS, Birchler JA, Jiang J (2020) A universal chromosome identification system for maize and wild Zea species. Chromosom Res 28:183–194. https://doi.org/10.1007/s10577-020-09630-5

    CAS  Article  Google Scholar 

  9. Chèvre AM, Mason AS, Coriton O, Grandont L, Jenczewski E, Lysak M (2018) Cytogenetics, a science linking genomics and breeding: the Brassica model. In: Liu S, Snowdon R, Chalhoub B (eds) The Brassica napus Genome. Compendium of Plant Genomes. Springer Nature, Switzerland, pp 21–39. https://doi.org/10.1007/978-3-319-43694-4_2

    Google Scholar 

  10. Coghlan A, Eichler EE, Oliver SG, Paterson AH, Stein L (2005) Chromosome evolution in eukaryotes: a multi-kingdom perspective. Trends Genet 21:673–682. https://doi.org/10.1016/j.tig.2005.09.009

    CAS  Article  PubMed  Google Scholar 

  11. de Carvalho CR, Saraiva LS (1993) An air drying technique for maize chromosomes without enzymatic maceration. Biotech Histochem 68:142–145. https://doi.org/10.3109/10520299309104684

    Article  PubMed  Google Scholar 

  12. Delgado-Salinas A, Thulin M, Pasquet R, Weeden N, Lavin M (2011) Vigna (Leguminosae) sensu lato: the names and identities of the American segregate genera. Am J Bot 98:1694–1715. https://doi.org/10.3732/ajb.1100069

    Article  PubMed  Google Scholar 

  13. do Vale Martins L, Yu F, Zhao H et al (2019) Meiotic crossovers characterized by haplotype-specific chromosome painting in maize. Nat Commun 10:4604. https://doi.org/10.1038/s41467-019-12646-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Fonsêca A, Pedrosa-Harand A (2013) Karyotype stability in the genus Phaseolus evidenced by the comparative mapping of the wild species Phaseolus microcarpus. Genome 56:335–343. https://doi.org/10.1139/gen-2013-0025

    CAS  Article  PubMed  Google Scholar 

  15. Fonsêca A, Ferreira J, dos Santos TR et al (2010) Cytogenetic map of common bean (Phaseolus vulgaris L.). Chromosom Res 18:487–502. https://doi.org/10.1007/s10577-010-9129-8

    CAS  Article  Google Scholar 

  16. Fonsêca A, Ferraz ME, Pedrosa-Harand A (2016) Speeding up chromosome evolution in Phaseolus: multiple rearrangements associated with a one-step descending dysploidy. Chromosoma 125:413–421. https://doi.org/10.1007/s00412-015-0548-3

    CAS  Article  PubMed  Google Scholar 

  17. Galasso I, Schmidt T, Pignone D, Heslop-Harrison JS (1995) The molecular cytogenetics of Vigna unguiculata (L.) Walp: the physical organization and characterization of 18s-5.8s-25s rRNA genes, 5s rRNA genes, telomere-like sequences, and a family of centromeric repetitive DNA sequences. Theor Appl Genet 91:928–935. https://doi.org/10.1007/BF00223902

    CAS  Article  PubMed  Google Scholar 

  18. Han OK, Kaga A, Isemura T, Wang XW, Tomooka N, Vaughan DA (2005) A genetic linkage map for azuki bean [Vigna angularis (Willd.) Ohwi & Ohashi]. Theor Appl Genet 111:1278–1287. https://doi.org/10.1007/s00122-005-0046-8

    CAS  Article  PubMed  Google Scholar 

  19. Han Y, Zhang Z, Liu C, Liu J, Huang S, Jiang J, Jin W (2009) Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation. Proc Natl Acad Sci 106:14937–14941. https://doi.org/10.1073/pnas.0904833106

    Article  PubMed  Google Scholar 

  20. Han Y, Zhang T, Thammapichai P, Weng Y, Jiang J (2015) Chromosome-specific painting in Cucumis species using bulked oligonucleotides. Genetics 200:771–779. https://doi.org/10.1534/genetics.115.177642

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. He L, Braz GT, Torres GA, Jiang J (2018) Chromosome painting in meiosis reveals pairing of specific chromosomes in polyploid Solanum species. Chromosoma 127:505–513. https://doi.org/10.1007/s00412-018-0682-9

    Article  PubMed  Google Scholar 

  22. He L, Zhao H, He J, Yang Z, Guan B, Chen K, Hong Q, Wang J, Liu J, Jiang J (2020) Extraordinarily conserved chromosomal synteny of Citrus species revealed by chromosome-specific painting. Plant J 103:2225–2235. https://doi.org/10.1111/tpj.14894

    CAS  Article  PubMed  Google Scholar 

  23. Heslop-Harrison JS, Harrison GE, Leitch IJ (1992) Reprobing of DNA: DNA in situ hybridization preparations. Trends Genet 8:372–373. https://doi.org/10.1016/0168-9525(92)90287-e

    CAS  Article  PubMed  Google Scholar 

  24. Hou L, Xu M, Zhang T, Xu Z, Wang W, Zhang J, Yu M, Ji W, Zhu C, Gong Z, Gu M, Jiang J, Yu H (2018) Chromosome painting and its applications in cultivated and wild rice. BMC Plant Biol 18:110. https://doi.org/10.1186/s12870-018-1325-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Hougaard BK, Madsen LH, Sandal N, de Carvalho Moretzsohn M, Fredslund J, Schauser L, Nielsen AM, Rohde T, Sato S, Tabata S, Bertioli DJ, Stougaard J (2008) Legume anchor markers link syntenic regions between Phaseolus vulgaris, Lotus japonicus, Medicago truncatula and Arachis. Genetics 179:2299–2312. https://doi.org/10.1534/genetics.108.090084

    Article  PubMed  PubMed Central  Google Scholar 

  26. Idziak D, Hazuka I, Poliwczak B, Wiszynska A, Wolny E, Hasterok R (2014) Insight into the karyotype evolution of Brachypodium species using comparative chromosome barcoding. PLoS One 9:e93503. https://doi.org/10.1371/journal.pone.0093503

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Ishii T, Juranic M, Maheshwari S et al (2020) Unequal contribution of two paralogous CENH3 variants in cowpea centromere function. Commun Biol 3:775. https://doi.org/10.1038/s42003-020-01507-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Iwata A, Tek AL, Richard MMS, Abernathy B, Fonsêca A, Schmutz J, Chen NWG, Thareau V, Magdelenat G, Li Y, Murata M, Pedrosa-Harand A, Geffroy V, Nagaki K, Jackson SA (2013) Identification and characterization of functional centromeres of the common bean. Plant J 76:47–60. https://doi.org/10.1111/tpj.12269

    CAS  Article  PubMed  Google Scholar 

  29. Iwata-Otsubo A, Lin JY, Gill N, Jackson SA (2016a) Highly distinct chromosomal structures in cowpea (Vigna unguiculata), as revealed by molecular cytogenetic analysis. Chromosom Res 24:197–216. https://doi.org/10.1007/s10577-015-9515-3

    CAS  Article  Google Scholar 

  30. Iwata-Otsubo A, Radke B, Findley S, Abernathy B, Vallejos E, Jackson SA (2016b) Fluorescence in situ hybridization (FISH)-based karyotyping reveals rapid evolution of centromeric and subtelomeric repeats in common bean (Phaseolus vulgaris) and relatives. G3 (Bethesda) 6:1013–1022. https://doi.org/10.1534/g3.115.024984

    CAS  Article  PubMed Central  Google Scholar 

  31. Javadi F, Tun YT, Kawase M, Guan K, Yamaguchi H (2011) Molecular phylogeny of the subgenus Ceratotropis (genus Vigna, Leguminosae) reveals three eco-geographical groups and Late Pliocene-Pleistocene diversification: evidence from four plastid DNA region sequences. Ann Bot 108:367–380. https://doi.org/10.1093/aob/mcr141

    Article  PubMed  PubMed Central  Google Scholar 

  32. Jiang J (2019) Fluorescence in situ hybridization in plants: recent developments and future applications. Chromosom Res 27:153–165. https://doi.org/10.1007/s10577-019-09607-z

    CAS  Article  Google Scholar 

  33. Jiang J, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068. https://doi.org/10.1139/g06-076

    CAS  Article  PubMed  Google Scholar 

  34. Jiao W, Schneeberger K (2020) Chromosome-level assemblies of multiple Arabidopsis genomes reveal hotspots of rearrangements with altered evolutionary dynamics. Nat Commun 11:989. https://doi.org/10.1038/s41467-020-14779

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Kang YJ, Satyawan D, Shim S, Lee T, Lee J, Hwang WJ, Kim SK, Lestari P, Laosatit K, Kim KH, Ha TJ, Chitikineni A, Kim MY, Ko JM, Gwag JG, Moon JK, Lee YH, Park BS, Varshney RK, Lee SH (2015) Draft genome sequence of adzuki bean, Vigna angularis. Sci Rep 5:8069. https://doi.org/10.1038/srep08069

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645. https://doi.org/10.1101/gr.092759.109

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL (2004) Versatile and open software for comparing large genomes. Genome Biol 5:R12. https://doi.org/10.1186/gb-2004-5-2-r12

    Article  PubMed  PubMed Central  Google Scholar 

  38. Lewis GP (2005) Tribe Caesalpinieae. In: Lewis G, Schrire B, Mackinder B, Lock M (eds) Legumes of the world. Royal Botanic Gardens, Kew

    Google Scholar 

  39. Li H, Wang W, Lin L, Zhu X, Li J, Zhu X, Chen Z (2013) Diversification of the phaseoloid legumes: effects of climate change, range expansion and habit shift. Front Plant Sci 4:386. https://doi.org/10.3389/fpls.2013.00386

    Article  PubMed  PubMed Central  Google Scholar 

  40. Liu X, Sun S, Wu Y, Zhou Y, Gu S, Yu H, Yi C, Gu M, Jiang J, Liu B, Zhang T, Gong Z (2019) Dual-color oligo-FISH can reveal chromosomal variations and evolution in Oryza species. Plant J 101:112–121. https://doi.org/10.1111/tpj.14522

    CAS  Article  PubMed  Google Scholar 

  41. Liu Y, Wang X, Wei Y, Liu Z, Lu Q, Liu F, Zhang T, Peng R (2020) Chromosome painting based on bulked oligonucleotides in cotton. Front Plant Sci 11:802. https://doi.org/10.3389/fpls.2020.00802

    Article  PubMed  PubMed Central  Google Scholar 

  42. Lonardi S, Muñoz-Amatriaín M, Liang Q, Shu S, Wanamaker SI, Lo S, Tanskanen J, Schulman AH, Zhu T, Luo MC, Alhakami H, Ounit R, Hasan AM, Verdier J, Roberts PA, Santos JRP, Ndeve A, Doležel J, Vrána J, Hokin SA, Farmer AD, Cannon SB, Close TJ (2019) The genome of cowpea (Vigna unguiculata [L.] Walp.). Plant J 98:767–782. https://doi.org/10.1111/tpj.14349

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. LPWG (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: the Legume Phylogeny Working Group (LPWG). Taxon 66:44–77. https://doi.org/10.12705/661.3

    Article  Google Scholar 

  44. Lusinska J, Majka J, Betekhtin A, Susek K, Wolny E, Hasterok R (2018) Chromosome identification and reconstruction of evolutionary rearrangements in Brachypodium distachyon, B. stacei and B. hybridum. Ann Bot 122:445–459. https://doi.org/10.1093/aob/mcy086

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Lysak MA, Fransz PF, Ali HB, Schubert I (2001) Chromosome painting in Arabidopsis thaliana. Plant J 28:689–697. https://doi.org/10.1046/j.1365-313x.2001.01194.x

    CAS  Article  PubMed  Google Scholar 

  46. Lysak MA, Koch MA, Pecinka A, Schubert I (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res 15:516–525. https://doi.org/10.1101/gr.3531105

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I (2006) Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci 103:5224–5229. https://doi.org/10.1073/pnas.0510791103

    CAS  Article  PubMed  Google Scholar 

  48. Mandáková T, Lysak MA (2008) Chromosomal phylogeny and karyotype evolution in x=7 crucifer species (Brassicaceae). Plant Cell 20:2559–2570. https://doi.org/10.1105/tpc.108.062166

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Mandáková T, Joly S, Krzywinski M, Mummenhoff K, Lysak MA (2010) Fast diploidization in close mesopolyploid relatives of Arabidopsis. Plant Cell 22:2277–2290. https://doi.org/10.1105/tpc.110.074526

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Mandáková T, Hlousková P, Koch MA, Lysak MA (2020) Genome evolution in Arabideae was marked by frequent centromere repositioning. Plant Cell 32:650–665. https://doi.org/10.1105/tpc.19.00557

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Meng Z, Zhang Z, Yan T, Lin Q, Wang Y, Huang W, Huang Y, Li Z, Yu Q, Wang J, Wang K (2018) Comprehensively characterizing the cytological features of Saccharum spontaneum by the development of a complete set of chromosome-specific oligo probes. Front Plant Sci 9:1624. https://doi.org/10.3389/fpls.2018.01624

    Article  PubMed  PubMed Central  Google Scholar 

  52. Meng Z, Han J, Lin Y, Zhao Y, Lin Q, Ma X, Wang J, Zhang M, Zhang L, Yang Q, Wang K (2020) Characterization of a Saccharum spontaneum with a basic chromosome number of x=10 provides new insights on genome evolution in genus Saccharum. Theor Appl Genet 133:187–199. https://doi.org/10.1007/s00122-019-03450-w

    Article  PubMed  Google Scholar 

  53. Mercado-Ruaro P, Delgado-Salinas A (1996) Karyological studies in several Mexican species of Phaseolus L. and Vigna Savi (Phaseolinae, Fabaceae). In: Pickersgill B, Lock JM (eds) Advances in legumes systematics. 8: Legumes of economic importance. Royal Botanic Gardens, Kew, pp 83–87

    Google Scholar 

  54. Muchero W, Diop NN, Bhat PR, Fenton RD, Wanamaker S, Pottorff M, Hearne S, Cisse N, Fatokun C, Ehlers JD, Roberts PA, Close TJ (2009) A consensus genetic map of cowpea [Vigna unguiculata (L) Walp] and synteny based on EST-derived SNPs. Proc Natl Acad Sci 106:18159–18164. https://doi.org/10.1073/pnas.0905886106

    CAS  Article  PubMed  Google Scholar 

  55. Nasuda S, Hudakova S, Schubert I, Houben A, Endo TR (2005) Stable barley chromosomes without centromeric repeats. Proc Natl Acad Sci 102:9842–9847. https://doi.org/10.1073/pnas.0504235102

    CAS  Article  PubMed  Google Scholar 

  56. Oliveira ARS, Martins LV, Bustamante FO, Muñoz-Amatriaín M, Close T, Costa AF, Benko-Iseppon AM, Pedrosa-Harand A, Brasileiro-Vidal AC (2020) Breaks of macrosynteny and collinearity among moth bean (Vigna aconitifolia), cowpea (V. unguiculata), and common bean (Phaseolus vulgaris). Chromosom Res. https://doi.org/10.1007/s10577-020-09635-0

  57. Qu M, Li K, Han Y, Chen L, Li Z, Han Y (2017) Integrated karyotyping of woodland strawberry (Fragaria vesca) with oligopaint FISH probes. Cytogenet Genome Res 153:158–164. https://doi.org/10.1159/000485283

    CAS  Article  PubMed  Google Scholar 

  58. Raskina O, Barber JC, Nevo E, Belyayev A (2008) Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenet Genome Res 120:351–357. https://doi.org/10.1159/000121084

    CAS  Article  PubMed  Google Scholar 

  59. Ribeiro T, Vasconcelos E, Santos KGB, Vaio M, Brasileiro-Vidal AC, Pedrosa-Harand A (2019) Diversity of repetitive sequences within compact genomes of Phaseolus L. beans and allied genera Cajanus L. and Vigna Savi. Chromosom Res 28:139–153. https://doi.org/10.1007/s10577-019-09618-w

    CAS  Article  Google Scholar 

  60. Sakai H, Naito K, Ogiso-Tanaka E, Takahashi Y, Iseki K, Muto C, Satou K, Teruya K, Shiroma A, Shimoji M, Hirano T, Itoh T, Kaga A, Tomooka N (2015) The power of single molecule real-time sequencing technology in the de novo assembly of a eukaryotic genome. Sci Rep 5:16780. https://doi.org/10.1038/srep16780

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, Fujishiro T, Katoh M, Kohara M, Kishida Y, Minami C, Nakayama S, Nakazaki N, Shimizu Y, Shinpo S, Takahashi C, Wada T, Yamada M, Ohmido N, Hayashi M, Fukui K, Baba T, Nakamichi T, Mori H, Tabata S (2008) Genome structure of the legume, Lotus japonicus. DNA Res 15:227–239. https://doi.org/10.1093/dnares/dsn008

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. https://doi.org/10.1038/nature08670

    CAS  Article  Google Scholar 

  63. Schmutz J, McClean PE, Mamidi S et al (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713. https://doi.org/10.1038/ng.3008

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Schubert I (2018) What is behind “centromere repositioning”? Chromosoma 127:229–234. https://doi.org/10.1007/s00412-018-0672-y

    CAS  Article  PubMed  Google Scholar 

  65. Šimoníková D, Němečková A, Karafiátová M, Uwimana B, Swennen R, Doležel J, Hřibová E (2019) Chromosome painting facilitates anchoring reference genome sequence to chromosomes in situ and integrated karyotyping in banana (Musa spp.). Front Plant Sci 10:1503. https://doi.org/10.3389/fpls.2019.01503

    Article  PubMed  PubMed Central  Google Scholar 

  66. Song X, Song R, Zhou J, Yan W, Zhang T, Sun H, Xiao J, Wu Y, Xi M, Lou Q, Wang H, Wang X (2020) Development and application of oligonucleotide-based chromosome painting for chromosome 4D of Triticum aestivum L. Chromosom Res 28:171–182. https://doi.org/10.1007/s10577-020-09627-0

    CAS  Article  Google Scholar 

  67. Tang H, Krishnakumar V, Bidwell S et al (2014) An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genomics 15:312. https://doi.org/10.1186/1471-2164-15-312

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. Vallejos CE, Sakiyama NS, Chase CD (1992) A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 131:733–740

    CAS  Article  Google Scholar 

  69. Valliyodan B, Cannon SB, Bayer PE, Shu S, Brown AV, Ren L, Jenkins J, Chung CYL, Chan TF, Daum CG, Plott C, Hastie A, Baruch K, Barry KW, Huang W, Patil G, Varshney RK, Hu H, Batley J, Yuan Y, Song Q, Stupar RM, Goodstein DM, Stacey G, Lam HM, Jackson SA, Schmutz J, Grimwood J, Edwards D, Nguyen HT (2019) Construction and comparison of three reference-quality genome assemblies for soybean. Plant J 100:1066–1082. https://doi.org/10.1111/tpj.14500

    CAS  Article  PubMed  Google Scholar 

  70. Vasconcelos EV, Fonsêca AFA, Pedrosa-Harand A, Bortoleti KCA, Benko-Iseppon AM, da Costa AF, Brasileiro-Vidal AC (2015) Intra- and interchromosomal rearrangements between cowpea [Vigna unguiculata (L.) Walp.] and common bean (Phaseolus vulgaris L.) revealed by BAC-FISH. Chromosom Res 23:253–266. https://doi.org/10.1007/s10577-014-9464-2

    CAS  Article  Google Scholar 

  71. Wang L, Kikuchi S, Muto C, Naito K, Isemura T, Ishimoto M, Cheng X, Kaga A, Tomooka N (2015) Reciprocal translocation identified in Vigna angularis dominates the wild population in East Japan. J Plant Res 128:653–663. https://doi.org/10.1007/s10265-015-0720-0

    CAS  Article  PubMed  Google Scholar 

  72. Wanzenböck EM, Schöfer C, Schweizer D, Bachmair A (1997) Ribosomal transcription units integrated via T-DNA transformation associate with the nucleolus and do not require upstream repeat sequences for activity in Arabidopsis thaliana. Plant J 11:1007–1016. https://doi.org/10.1046/j.1365-313x.1997.11051007.x

    Article  PubMed  Google Scholar 

  73. Wellenreuther M, Bernatchez L (2018) Eco-evolutionary genomics of chromosomal inversions. Trends Ecol Evol 33:427–440. https://doi.org/10.1016/j.tree.2018.04.002

    Article  PubMed  Google Scholar 

  74. Xin H, Zhang T, Han Y, Wu Y, Shi J, Xi M, Jiang J (2018) Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides. Chromosoma 127:313–321. https://doi.org/10.1007/s00412-018-0664-y

    CAS  Article  PubMed  Google Scholar 

  75. Xin H, Zhang T, Wu Y, Zhang W, Zhang P, Xi M, Jiang J (2019) An extraordinarily stable karyotype of the woody Populus species revealed by chromosome painting. Plant J 101:253–264. https://doi.org/10.1111/tpj.14536

    CAS  Article  PubMed  Google Scholar 

  76. Young ND, Debellé F, Oldroyd GE et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524. https://doi.org/10.1038/nature10625

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  77. Zhao H, Zeng Z, Koo DH, Gill BS, Birchler JA, Jiang J (2017) Recurrent establishment of de novo centromeres in the pericentromeric region of maize chromosome 3. Chromosom Res 25:299–311. https://doi.org/10.1007/s10577-017-9564-x

    CAS  Article  Google Scholar 

  78. Zhao Q, Wang Y, Bi Y, Zhai Y, Yu X, Cheng C, Wang P, Li J, Lou Q, Chen J (2019) Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypes. BMC Plant Biol 19:471. https://doi.org/10.1186/s12870-019-2060-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Embrapa Arroz e Feijão, Embrapa Meio-Norte, and IPK for providing the seeds. We also thank Timothy Close (University of California, Riverside) for providing the V. unguiculata BAC clones and Claudio César Montenegro Júnior for positioning the BAC H074C16 on the sequence map. We thank CNPq, CAPES, and FACEPE for fellowships and financial support.

Funding

This research was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) (Grant nos. 442019/2019-0, 421968/2018-4, 433931/2018-3, 310804/2017-5, 310871/2014-0, and 313527/2017-2) and FACEPE (Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco) APQ-0409-2.02/16. The doctorate scholarship and a doctorate-abroad scholarship were provided by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), Finance Code 001 and Project no. 88881.189152/2018-01, respectively.

Author information

Affiliations

Authors

Contributions

LVM performed the BAC- and oligo-FISH experiments and wrote the paper. FOB and ARSO helped to perform the experiments. AFC performed seed multiplication. QL analyzed the sequence synteny data. HZ designed the oligo-FISH probes. APH and FOB conceived the oligo probes. MMA and TC maintained and provided V. unguiculata BAC clones. JJ provided the resources for the oligo-FISH experiments. APH, LLF, AMBI, and JJ planed the experiments and discussed the results. ACBV was doctorate supervisor of LVM, designed and directed the research, and helped to write the paper. All authors read, discussed, and approved the final version of the paper.

Corresponding author

Correspondence to Ana Christina Brasileiro-Vidal.

Ethics declarations

Ethics approval

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Fig. S1
figure5

Detailed sequence synteny between Vigna angularis (Va) and V. unguiculata (Vu) pseudomolecules 2 using V. unguiculata sequences but colored in accordance with Pv2 (green) and Pv3 (red). The pericentric inversion, previously identified by our BAC-FISH analysis, was confirmed by our sequence analysis: H074C16 Vu BAC is located at 5.6 Mb and 18.7 Mb region of Va2 and Vu2, respectively, that corresponds to a red region in both species. Lateral black squares on Va2 and Vu2 represent the centromere positions. Bar =5 Mb (PNG 808 kb).

High Resolution Image (TIF 3.16 kb).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

do Vale Martins, L., de Oliveira Bustamante, F., da Silva Oliveira, A.R. et al. BAC- and oligo-FISH mapping reveals chromosome evolution among Vigna angularis, V. unguiculata, and Phaseolus vulgaris. Chromosoma (2021). https://doi.org/10.1007/s00412-021-00758-9

Download citation

Keywords

  • BAC-FISH
  • Beans
  • Chromosomal rearrangements
  • Karyotype evolution
  • Macrosynteny
  • Oligopainting