Journal of Genetics

, Volume 97, Issue 5, pp 1421–1431 | Cite as

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

  • Yunzheng Miao
  • Siqing Yang
  • Yurong Jiang
  • Junkang Rong
  • Jinsheng YuEmail author
Research Article


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.


wheat DNA marker distorted segregation genetic map 



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.

Supplementary material

12041_2018_1041_MOESM1_ESM.xlsx (26 kb)
Supplementary material 1 (xlsx 26 KB)


  1. 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.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.PubMedPubMedCentralGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. Faris J. D., Laddomada B. and Gill B. S. 1998 Molecular mapping of segregation distortion loci in Aegilops tauschii. Genetics 149, 319–327.Google Scholar
  7. 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.Google Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.Google Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Kinoshita T. 1993 Report of the committee on gene symbolization, nomenclature and linkage group. Rice Genet. News 10, 7–39.Google Scholar
  13. Kosambi D. D. 2011 The estimation of map distance from recombination values. Ann. Eugen. 12, 172–175.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. Larracuente A. M. and Presgraves D. C. 2012 The selfish segregation distorter gene complex of Drosophila melanogaster. Genetics 192, 33–53.Google Scholar
  17. 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.Google Scholar
  18. Liedl B. and Anderson N. O. 1993 Reproductive barriera: identification, uses and circumvention. Plant Breed Rev. 11, 11–154.Google Scholar
  19. 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.CrossRefGoogle Scholar
  20. Lyon M. F. 1984 Transmission ratio distortion in mouse t-haplotypes is due to multiple distorter genes acting on a responder locus. Cell 37, 621–628Google Scholar
  21. Lyon M. F. 2003 Transmission ratio distortion in mice. Annu. Rev. Genet. 37, 393–408.CrossRefGoogle Scholar
  22. Lyttle T. W. 1991 Segregation distorters. Annu. Rev. Genet. 25, 511–557.CrossRefGoogle Scholar
  23. 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
  24. 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.CrossRefGoogle Scholar
  25. Moschetti R., Caizzi R. and Pimpinelli S. 1996 Segregation distortion in Drosophila melanogaster: Genomic organization of Responder sequences. Genetics 144, 1665–1671.Google Scholar
  26. 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.CrossRefGoogle Scholar
  27. Pennisi E. 2003 Gene evolution. Cannibalism and prion disease may have been rampant in ancient humans. Science 300, 227–228.CrossRefGoogle Scholar
  28. 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.PubMedPubMedCentralGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. Silver L. M. 1985 Mouse \(t\) haplotypes. Annu. Rev. Genet. 19, 179–208.CrossRefGoogle Scholar
  31. Temin R. G. 1991 The independent distorting ability of the enhancer of segregation distortion, E(SD), in Drosophila melanogaster. Genetics 128, 339–356.PubMedPubMedCentralGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. Tsujimoto H. 1995 Gametocidal genes in wheat and its relatives. IV. Functional relationships between six gametocidal genes. Genome 38, 283–289.CrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.Google Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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
  38. 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.CrossRefGoogle Scholar
  39. 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.Google Scholar
  40. 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.Google Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.Google Scholar

Copyright information

© Indian Academy of Sciences 2018

Authors and Affiliations

  • Yunzheng Miao
    • 1
  • Siqing Yang
    • 1
  • Yurong Jiang
    • 1
  • Junkang Rong
    • 1
    • 2
  • Jinsheng Yu
    • 1
    Email author
  1. 1.The Key Laboratory for Quality Improvement of Agricultural Products of Zhejiang Province, School of Agriculture and Food ScienceZhejiang A&F UniversityLinan, HangzhouPeople’s Republic of China
  2. 2.Department of Plant SciencesThe Weizmann Institute of ScienceRehovotIsrael

Personalised recommendations