Skip to main content
Log in

Meiotic homoeologous recombination-based mapping of wheat chromosome 2B and its homoeologues in Aegilops speltoides and Thinopyrum elongatum

Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

We physically dissected and mapped wheat chromosome 2B and its homoeologues in Aegilops speltoides and Thinopyrum elongatum based on meiotic homoeologous recombination, providing a unique physical framework for genome studies.

Abstract

Common wheat has a large and complex genome with narrow genetic diversity and various degrees of recombination between the A, B, and D subgenomes. This has limited the homologous recombination-based genome studies in wheat. Here, we exploited meiotic homoeologous recombination for molecular mapping of wheat chromosome 2B and its homoeologue 2S from Aegilops speltoides and 2E from Thinopyrum elongatum. The 2B–2S and 2B–2E recombination was induced by the ph1b mutant, and recovered using molecular markers and fluorescent genomic in situ hybridization (FGISH). A total of 112 2B–2S and 87 2B–2E recombinants involving different chromosome regions were developed and physically delineated by FGISH. The 2B–2S and 2B–2E recombination hotspots mapped to the subterminal regions on both arms. Recombination hotspots with the highest recombination rates mapped to the short arms. Eighty-three 2B–2S and 67 2B–2E recombinants were genotyped using the wheat 90 K SNP arrays. Based on the genotyping results and FGISH patterns of the recombinants, chromosomes 2B, 2S, and 2E were partitioned into 93, 66, and 46 bins, respectively. In total, 1037 SNPs physically mapped onto distinct bins of these three homoeologous chromosomes. A homoeologous recombination-based bin map was constructed for chromosome 2B, providing a unique physical framework for genome studies in wheat and its relatives. Meiotic homoeologous recombination also facilitates gene introgression to diversify the wheat genome for germplasm development. Therefore, homoeologous recombination-based studies enhance understanding of the wheat genome and its homoeologous counterparts from wild grasses, and expand the genetic variability of the wheat genome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • Cai X (1994) Chromosome translocations in the common wheat variety ‘Amigo’. Hereditas 121:199–202

    Article  Google Scholar 

  • Cai X, Jones S, Murray T (1998) Molecular cytogenetic characterization of Thinopyrum and wheat–Thinopyrum translocated chromosomes in a wheat Thinopyrum amphiploid. Chromosome Res 6:183–189

    Article  CAS  Google Scholar 

  • Dvorak J, Terlizzi P, Zhang HB, Resta P (1993) The evolution of polyploidy wheats: identification of the A genome donor species. Genome 36:21–31

    Article  CAS  Google Scholar 

  • Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307

    Article  CAS  Google Scholar 

  • Erayman M, Sandhu D, Sidhu D, Dilbirligi M, Baenziger PS, Gill KS (2004) Demarcating the gene-rich regions of the wheat genome. Nucleic Acids Res 32:3546–3565

    Article  CAS  Google Scholar 

  • Faris JD, Xu SS, Cai X, Friesen TL, Jin Y (2008) Molecular and cytogenetic characterization of a durum wheat-Aegilops speltoides chromosome translocation conferring resistance to stem rust. Chromosome Res 16:1097–1105

    Article  CAS  Google Scholar 

  • Friebe B, Jiang J, Raupp WJ, McIntosh RA, Gill BS (1996) Characterization of wheat–alien translocations conferring resistance to diseases and pests: current status. Euphytica 91:59–87

    Article  Google Scholar 

  • Friebe B, Zhang P, Linc G, Gill BS (2005) Robertsonian translocations in wheat arise by centric misdivision of univalents at anaphase I and rejoining of broken centromeres during interkinesis of meiosis II. Cytogenet Genome Res 109:293–297

    Article  CAS  Google Scholar 

  • Friebe B, Qi LL, Liu C, Gill BS (2011) Genetic compensation abilities of Aegilops speltoides chromosomes for homoeologous B-genome chromosomes of polyploid wheat in disomic S(B) chromosome substitution lines. Cytogenet Genome Res 134:144–150

    Article  CAS  Google Scholar 

  • Gill BS, Morris R, Schmidt JW, Maan SS (1963) Meiotic studies on chromosome morphology in the Wichita wheat variety by means of monosomics. Can J Genet Cytol 5:326–337

    Article  Google Scholar 

  • Gill BS, Friebe B, Endo TR (1991) Standard karyotype and nomenclature system for description of chromosome bands and structural aberrations in wheat (Triticum aestivum). Genome 34:830–839

    Article  Google Scholar 

  • Grewal S, Yang C, Hubbart Edwards S, Scholefield D, Ashling S, Burridge AJ, King IP, King J (2018) Characterisation of Thinopyrum bessarabicum chromosomes through genome-wide introgressions into wheat. Theor Appl Genet 131:389–406

    Article  CAS  Google Scholar 

  • Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P (2002) Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploidy wheat. Proc Natl Acad Sci USA 99:8133–8138

    Article  CAS  Google Scholar 

  • Jiang J, Friebe B, Gill BS (1994) Recent advances in alien gene transfer in wheat. Euphytica 73:199–212

    Article  Google Scholar 

  • Kalavacharla V, Hossain K, Gu Y, Riera-Lizarazu O, Vales MI, Bhamidimarri S, Gonzalez-Hernandez JL, Maan SS, Kianian SF (2006) High-resolution radiation hybrid map of wheat chromosome 1D. Genetics 173:1089–1099

    Article  CAS  Google Scholar 

  • Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare wheat. Agric Hortic (Tokyo) 19:889–890

    Google Scholar 

  • King J, Grewal S, Yang CY, Hubbart Edwards S, Scholefield D, Ashling S, Harper JA, Allen AM, Edwards KJ, Burridge AJ, King IP (2018) Introgression of Aegilops speltoides segments in Triticum aestivum and the effect of the gametocidal genes. Ann Bot 121:229–240

    Article  Google Scholar 

  • Klindworth DL, Niu Z, Chao S, Friesen TL, Jin Y, Faris JD, Cai X, Xu SS (2012) Introgression and characterization of a goatgrass gene for a high level of resistance to Ug99 stem rust in tetraploid wheat. G3 2:665–673

    Article  CAS  Google Scholar 

  • Liu W, Jin Y, Rouse M, Friebe B, Gill B, Pumphrey MO (2011) Development and characterization of wheat-A. searsii Robertsonian translocations and a recombinant chromosome conferring resistance to stem rust. Theor Appl Genet 122:1537–1545

    Article  Google Scholar 

  • Long Y, Chao WS, Ma G, Xu SS, Qi L (2017) An innovative SNP genotyping method adapting to multiple platforms and throughputs. Theor Appl Genet 130:597–607

    Article  CAS  Google Scholar 

  • Lukaszewski AJ, Curtis CA (1993) Physical distribution of recombination in B-genome chromosomes of tetraploid wheat. Theor Appl Genet 86:121–127

    Article  CAS  Google Scholar 

  • Marcussen T, Sandve SR, Heier L, Spannagl M, Pfeifer M, Jakobesn KS, IWGSC, Wulff BBH, Steuernagel B, Mayer KFX, Olsen OA (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science 345:1250092-1–1250092-4

    Article  Google Scholar 

  • Morris R, Sears ER (1967) The cytogenetics of wheat and its relatives. In: Quisenberry KS, Reitz LP (eds) Wheat and wheat improvement. American Society of Agronomy, Madison, WI, pp 19–87

    Google Scholar 

  • Niu Z, Klindworth DL, Friesen TL, Chao S, Jin Y, Cai X, Xu SS (2011) Targeted introgression of a wheat stem rust resistance gene by DNA marker-assisted chromosome engineering. Genetics 187:1011–1021

    Article  CAS  Google Scholar 

  • Patokar C, Sepsi A, Schwarzacher T, Kishii M, Heslop-Harrison JS (2016) Molecular cytogenetic characterization of novel wheat-Thinopyrum bessarabicum recombinant lines carrying intercalary translocations. Chromosoma 125:163–172

    Article  CAS  Google Scholar 

  • Qi L, Echalier B, Friebe B, Gill B (2003) Molecular characterization of a set of wheat deletion stocks for use in chromosome bin mapping of ESTs. Funct Integr Genomics 3:39–55

    CAS  PubMed  Google Scholar 

  • Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvorak J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, La Rota CM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Erayman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma XF, Miftahudin Gustafson JP, Conley EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NLV, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    Article  CAS  Google Scholar 

  • Qi LL, Friebe B, Zhang P, Gill BS (2007) Homoeologous recombination, chromosome engineering and crop improvement. Chromosome Res 15:3–19

    Article  CAS  Google Scholar 

  • Rey M, Martín AC, Smedley M, Hayta S, Harwood W, Shaw P, Moore G (2018) Magnesium increases homoeologous crossover frequency during meiosis in ZIP4 (Ph1 gene) mutant wheat-wild relative hybrids. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00509

    Article  PubMed  PubMed Central  Google Scholar 

  • Riley R, Chapman V (1958) Genetic control of cytologically diploid behaviour of hexaploid wheat. Nature 182:713–715

    Article  Google Scholar 

  • Riley R, Chapman V, Kimber G (1959) Genetic control of chromosome pairing in intergeneric hybrids with wheat. Nature 183:1244–1246

    Article  CAS  Google Scholar 

  • Roberts MA, Reader SM, Dalgliesh C, Miller TE, Foote TN, Fish LJ, Snape JW, Moore G (1999) Induction and characterization of Ph1 wheat mutants. Genetics 153:1909–1918

    CAS  PubMed  PubMed Central  Google Scholar 

  • Šafář J, Šimková H, Kubaláková M, Číhalíková J, Suchánková P, Bartoš J, Doležel J (2010) Development of chromosome-specific BAC resources for genomics of bread wheat. Cytogenet Genome Res 129:211–223

    Article  Google Scholar 

  • Saintenac C, Falque M, Martin OC, Paux E, Feuillet C, Sourdille P (2009) Detailed recombination studies along chromosome 3B provide new insights on crossover distribution in wheat (Triticum aestivum L.). Genetics 181:393–403

    Article  CAS  Google Scholar 

  • Sears ER (1954) The aneuploids of common wheat. Mo Agric Exp Stn Res Bull 572:1–59

    Google Scholar 

  • Sears ER (1966) Nullisomic-tetrasomic combinations in hexaploid wheat. In: Riley R, Lewis KR (eds) Chromosome manipulation and plant genetics. Oliver and Boyd, Edinburgh, pp 29–45

    Chapter  Google Scholar 

  • Sears ER (1977) An induced mutant with homoeologous pairing in common wheat. Can J Genet Cytol 19:585–593

    Article  Google Scholar 

  • Sidhu D, Gill KS (2004) Distribution of genes and recombination in wheat and other eukaryotes. Plant Cell Tissue Organ Cult 79:257–270

    Article  Google Scholar 

  • Takumi S, Nasuda S, Liu YG, Tsunewaki K (1993) Wheat phylogeny determined by RFLP analysis of nuclear DNA. I. Einkorn wheat. Jpn J Genet 68:73–79

    Article  Google Scholar 

  • Wang S, Wong D, Forrest K, Allen A, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, International Wheat Genome Sequencing Consortium, Lillemo M, Mather D, Appels R, Dolferus R, Brown-Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo MC, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796

    Article  CAS  Google Scholar 

  • Werner JE, Endo TR, Gill BS (1992) Toward a cytogenetically based physical map of the wheat genome. Proc Natl Acad Sci USA 89:11307–11311

    Article  CAS  Google Scholar 

  • Zhang W, Cao Y, Zhang M, Zhu X, Ren S, Long Y, Gyawali Y, Chao S, Xu S, Cai X (2017) Meiotic homoeologous recombination-based alien gene introgression in the genomics era of wheat. Crop Sci 57:1189–1198

    Article  CAS  Google Scholar 

  • Zhang W, Zhang M, Zhu X, Cao Y, Sun Q, Ma G, Chao S, Yan C, Xu S, Cai X (2018) Molecular cytogenetic and genomic analyses reveal new insights into the origin of the wheat B genome. Theor Appl Genet 131:365–375

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank members of the laboratories involved for their help to this research and Drs. Lili Qi and Rebekah Oliver for their critical review of the manuscript. This project is supported by Agriculture and Food Research Initiative Competitive Grant no. 2013-67013-21121 from the USDA National Institute of Food and Agriculture.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiwen Cai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by P. Heslop-Harrison.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, W., Zhu, X., Zhang, M. et al. Meiotic homoeologous recombination-based mapping of wheat chromosome 2B and its homoeologues in Aegilops speltoides and Thinopyrum elongatum. Theor Appl Genet 131, 2381–2395 (2018). https://doi.org/10.1007/s00122-018-3160-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-018-3160-0

Navigation