Skip to main content
SpringerLink
Log in

A genetic system on chromosome arm 1BL of wild emmer causes distorted segregation in common wheat

  • Research Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Nonrandom segregation ratios of alleles ‘segregation distortion’ can have a striking impact on transmission genetics, and with widespread availability of genetic markers has been shown to be a frequent phenomenon. To investigate the possible effect of genetic interaction on segregation distortion and genetic map construction, the segregation and mapping of genetic markers located on wheat chromosomes 1A and 1B were followed in four recombinant substitution line (RSL) populations, produced using four chromosome-arm substitution lines (CASLs 1AS, 1AL, 1BS and 1BL) of wild emmer (Triticum turgidum var. dicoccoides, accession TTD140) in the background of the common wheat (T. aestivum) cultivar Bethlehem (BLH), each crossed to BLH itself. Using these four RSL populations, four genetic maps of chromosome 1 arms were constructed. A total of 22 genetic markers representing 19 loci were assigned to chromosome 1A, and 32 markers representing 30 loci were assigned to 1B. For chromosome 1B, two linkage maps were also constructed using RFLP data of an \(\hbox {F}_{2}\) population derived from the same cross combination as the RSLs. The RSL and \(\hbox {F}_{2}\) maps varied in genetic distances, but showed the same linear order of DNA markers. Segregation analysis revealed strong selection against BLH alleles on chromosome 1B, skewing the allelic frequency distribution in favour of TTD in both \(\hbox {F}_{2}\) and RSL populations at all marker loci. On the contrary, strong selection against TTD alleles on chromosome 1A was detected for some loci in the BLH \(\times \) CASL1AL RSLs, and their distribution was significantly skewed to BLH. \(\hbox {F}_{2}\) populations always showed more segregation distortion than the corresponding RSLs. More markers near the region of chromosome 1B shared by both CASL1BS and 1BL (\(\sim \)55 cM on chromosome 1B across the centromere) showed significantly distorted segregation in the \(\hbox {BLH}\times \hbox {CASL1BL}\) population than in the corresponding \(\hbox {BLH}\times \hbox {CASL1BS}\) populations. Six markers located on chromosome 1A region shared by CASL1AS and 1AL showed significantly distorted segregation in 1AL-RSL, while no marker showed distorted segregation in 1AS-RSL. These results indicated that genetic factor(s) in the centromere region cause the distorted segregation of genetic markers on wheat chromosome 1B.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bauer H., Schindler S., Charron Y., Willert J., Kusecek B. and Herrmann B. G. 2012 The nucleoside diphosphate kinase gene Nme3 acts as quantitative trait locus promoting non-Mendelian inheritance. PLoS Genet. 8, e1002567.

    Article  CAS  Google Scholar 

  • Baumbach J., Rogers J. P., Slattery R. A., Narayanan N. N., Xu M., Palmer R. G. et al. 2012 Segregation distortion in a region containing a malesterility, female-sterility locus in soybean. Plant Sci. 195, 151–156.

    Article  CAS  Google Scholar 

  • Bennett D. 1978 Population genetics of \(T/t\) complex mutations. In NIH workshop on Origins of Inbred Mice, (ed. H. C. Morse), pp. 615–632. Academic Press, New York.

    Chapter  Google Scholar 

  • Dunn L. C. 1957 Studies of the genetic variability in populations of wild house mice II. Analysis of additional alleles at locus \(T\). Genetics 42, 299–311.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dvorák J., Dubcovsky J., Luo M. M., Devos K. M. and Gale M. D. 1995 Differentiation between wheat chromosomes 4B and 4D. Genome 38, 1139–1147.

    Article  Google Scholar 

  • Faris J. D., Laddomada B. and Gill B. S. 1998 Molecular mapping of segregation distortion loci in Aegilops tauschii. Genetics 149, 319–327.

  • Feldmann K. A., Coury D. A. and Christianson M. L. 1997 Exceptional segregation of a selectable marker (KanR) in Arabidopsis identifies genes important for gametophytic growth and development. Genetics 147, 1411–1422.

  • Galili G. and Feldman M. 1983 Genetic control of endosperm proteins in wheat: 1. The use of high resolution one-dimensional gel electrophoresis for the allocation of genes coding for endosperm protein subunits in the common wheat cultivar chinese spring. Theor. Appl. Genet. 64, 97–101.

    Article  CAS  Google Scholar 

  • Hiraizumi Y. 1990 Negative segregation distortion in the SD system of Drosophila melanogaster: a challenge to the concept of differential sensitivity of Rsp alleles. Genetics 125, 515–525.

  • Jiang Y. R., He M. D., Ding M. Q. and Rong J. K. 2016 Chromosome elimination of hexaploid common wheat mediated by interaction between Chinese spring cytoplasm and a genetic factor(s) on chromosome arm 1BL of wild emmer. Euphytica 209, 1–11.

    Article  Google Scholar 

  • Kam-Morgan L. N. W., Gill B. S. and Muthukrishnan S. 1989 DNA restriction fragment length polymorphism: a strategy for genetic mapping of D genome of wheat. Genome 32, 724–732.

    Article  CAS  Google Scholar 

  • Kinoshita T. 1993 Report of the committee on gene symbolization, nomenclature and linkage group. Rice Genet. News 10, 7–39.

    Google Scholar 

  • Kosambi D. D. 2011 The estimation of map distance from recombination values. Ann. Eugen. 12, 172–175.

    Article  Google Scholar 

  • Kumar S., Gill B. S. and Faris J. D. 2007 Identification and characterization of segregation distortion loci along chromosome 5B in tetraploid wheat. Mol. Genet. Genomics 278, 187–196.

    Article  CAS  Google Scholar 

  • Lander E. S., Green P., Abrahamson J., Barlow A., Daly M. J., Lincoln S. E. et al. 1987 MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1, 174–181.

    Article  CAS  Google Scholar 

  • Larracuente A. M. and Presgraves D. C. 2012 The selfish segregation distorter gene complex of Drosophila melanogaster. Genetics 192, 33–53.

  • Lavery P. and James S. H. 1987 Complex hybridity in Isotoma petraea VI. Distorted segregation gametic lethal systems and population divergence. Heredity 58, 401–408.

  • Liedl B. and Anderson N. O. 1993 Reproductive barriera: identification, uses and circumvention. Plant Breed Rev. 11, 11–154.

    Google Scholar 

  • Liharska T., Wordragen M., Kammen A., Zabel P. and Koornneef M. 1996 Tomato chromosome 6: effect of alien chromosomal segments on recombinant frequencies. Genome 39, 485–491.

    Article  CAS  Google Scholar 

  • Lyon M. F. 1984 Transmission ratio distortion in mouse t-haplotypes is due to multiple distorter genes acting on a responder locus. Cell 37, 621–628

  • Lyon M. F. 2003 Transmission ratio distortion in mice. Annu. Rev. Genet. 37, 393–408.

    Article  CAS  Google Scholar 

  • Lyttle T. W. 1991 Segregation distorters. Annu. Rev. Genet. 25, 511–557.

    Article  CAS  Google Scholar 

  • Manrique-Carpintero N. C., Coombs J. J., Veilleux R. E., Buell C. R. and Douches D. S. 2016 Comparative analysis of regions with distorted segregation in three diploid populations of Potato. Genes Genom. 6, 2617–2628.

    Google Scholar 

  • Millet E., Rong J. K., Qualset C. O., McGuire P. E., Bernard M., Sourdille P. et al. 2013 Production of chromosome-arm substitution lines of wild emmer in common wheat. Euphytica 190, 1–17.

    Article  Google Scholar 

  • Moschetti R., Caizzi R. and Pimpinelli S. 1996 Segregation distortion in Drosophila melanogaster: Genomic organization of Responder sequences. Genetics 144, 1665–1671.

  • Peng J. H., Zadeh H., Lazo J. R., Gustafson J. P., Chao S., Anderson O. D. et al. 2004 Chromosome bin map of expressed sequence tags in homoeologous group 1 of hexaploid wheat and homoeology with rice and Arabidopsis. Genetics 168, 609–623.

    Article  CAS  Google Scholar 

  • Pennisi E. 2003 Gene evolution. Cannibalism and prion disease may have been rampant in ancient humans. Science 300, 227–228.

    Article  CAS  Google Scholar 

  • Röder M. S., Korzun V., Wendehake K., Plaschke J., Tixier M. H., Leroy P. et al. 1998 A microsatellite map of wheat. Genetics 149, 2007–2023.

    PubMed  PubMed Central  Google Scholar 

  • Schmidt R., West J., Love K., Lenehan Z., Lister C. and Thompson H. 1995 Physical map and organization of Arabidopsis thaliana chromosome 4. Science 270, 480–483.

    Article  CAS  Google Scholar 

  • Silver L. M. 1985 Mouse \(t\) haplotypes. Annu. Rev. Genet. 19, 179–208.

    Article  CAS  Google Scholar 

  • Temin R. G. 1991 The independent distorting ability of the enhancer of segregation distortion, E(SD), in Drosophila melanogaster. Genetics 128, 339–356.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Temin R. G., Ganetzky B., Powers P. A., Lyttle T. W., Pimpinelli S., Dimitri P. et al. 1991 Segregation distortion in Drosophila melanogaster: genetic and molecular analyses. Am. Nat. 137, 287–331.

    Article  Google Scholar 

  • Tsujimoto H. 1995 Gametocidal genes in wheat and its relatives. IV. Functional relationships between six gametocidal genes. Genome 38, 283–289.

    Article  CAS  Google Scholar 

  • Van Deynze A. E., Nelson J. C., Yglesias E. S., Harrington S. E., Braga D. P., McCouch S. R. et al. 1995a Comparative mapping in grasses. Wheat relationships. Mol. Gen. Genet. 248, 744–754.

    Article  Google Scholar 

  • Van Deynze A. E., Nelson J. C., O’donoughue L. S., Ahn S. N., Siripoonwiwat W., Harrington S. E. et al. 1995b Comparative mapping in grasses. Oat relationships. Mol. Gen. Genet. 249, 349–356.

  • Van Wordragen M. F., Weide R. L., Coppoolse E., Zabel P. and Koornneef M. 1996 Tomato chromosome 6: a high resolution map of the long arm and construction of a composite integrated marker-order map. Theor. Appl. Genet. 92, 1065–1072.

    Article  Google Scholar 

  • Xu X., Hsia A. P., Zhang L., Nikolau B. J. and Schnable P. S. 1995 Meiotic recombination break points resolve at high rates at the 5’ end of a maize coding sequence. Plant Cell 7, 215–261.

    Google Scholar 

  • Xu X., Li L., Dong X., Jin W., Melchinger A. E. and Chen S. 2013 Gametophytic and zygotic selection leads to segregation distortion through in vivo induction of a maternal haploid in maize. J. Exp. Bot. 64, 1083–1096.

    Article  CAS  Google Scholar 

  • Xu Y., Zhu L., Xiao J., Huang N. and McCouch S. R. 1997 Chromosomal regions associated with segregation distortion of molecular markers in F\(_2\), backcross, doubled haploid, and recombinant inbred populations of rice (Oryza sativa L.). Mol. Gen. Gent. 253, 535–545.

  • Yanagihara S., McCouch S. R., Ishikawa K., Ogi Y., Maruyama K. and Ikehashi H. 1995 Molecular analysis of the inheritance of the S-5 locus, conferring wide compatility in Indical Japonica hybrids of rice (O. sativa L.). Theor. Appl. Genet. 90, 182–188.

  • Yang J., Zhao X., Cheng K., Du H., Ouyang Y., Chen J. et al. 2012 A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337, 1336–1340.

    Article  CAS  Google Scholar 

  • Zhang H. B. and Dvorak J. 1990 Characterization and distribution of an interspersed repeated nucleotide sequence from Lophopyrum elongatum and mapping of a segregation-distortion factor with it. Genome 33, 927–936.

Download references

Acknowledgements

This research was completed in Professor Moshe Feldman’s laboratory at Weizmann Institute of Science, Israel. Many thanks to him for sharing the data with us. The manuscript was prepared in our current laboratory in Hangzhou, China, which was supported jointly by the National Key Research and Development Programme of China (2016YFD0102000) and the National Natural Science Foundation of China (grant no. 31671684) to Junkang Rong, and the Public Project of Science Technology Department of Zhejiang Province (grant no. 2016C02050-9-9) to Yurong Jiang.

Author information

Authors and Affiliations

  1. The Key Laboratory for Quality Improvement of Agricultural Products of Zhejiang Province, School of Agriculture and Food Science, Zhejiang A&F University, Linan, Hangzhou, 311300, Zhejiang, People’s Republic of China

    Yunzheng Miao, Siqing Yang, Yurong Jiang, Junkang Rong & Jinsheng Yu

  2. Department of Plant Sciences, The Weizmann Institute of Science, 76100, Rehovot, Israel

    Junkang Rong

Authors
  1. Yunzheng Miao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Siqing Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yurong Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Junkang Rong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinsheng Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jinsheng Yu.

Additional information

Corresponding editor: H. A. Ranganath

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (xlsx 26 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miao, Y., Yang, S., Jiang, Y. et al. A genetic system on chromosome arm 1BL of wild emmer causes distorted segregation in common wheat. J Genet 97, 1421–1431 (2018). https://doi.org/10.1007/s12041-018-1041-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-018-1041-6

Keywords

Search

Navigation