Theoretical and Applied Genetics

, Volume 132, Issue 12, pp 3265–3276 | Cite as

Recombination between homoeologous chromosomes induced in durum wheat by the Aegilops speltoides Su1-Ph1 suppressor

  • Hao Li
  • Le Wang
  • Ming-Cheng Luo
  • Fang Nie
  • Yun Zhou
  • Patrick E. McGuire
  • Assaf Distelfeld
  • Xiongtao Dai
  • Chun-Peng Song
  • Jan DvorakEmail author
Original Article


Key message

Su1-Ph1, which we previously introgressed into wheat from Aegilops speltoides, is a potent suppressor of Ph1 and a valuable tool for gene introgression in tetraploid wheat.


We previously introgressed Su1-Ph1, a suppressor of the wheat Ph1 gene, from Aegilops speltoides into durum wheat cv Langdon (LDN). Here, we evaluated the utility of the introgressed suppressor for inducing introgression of alien germplasm into durum wheat. We built LDN plants heterozygous for Su1-Ph1 that simultaneously contained a single LDN chromosome 5B and a single Ae. searsii chromosome 5Sse, which targeted them for recombination. We genotyped 28 BC1F1 and 84 F2 progeny with the wheat 90-K Illumina single-nucleotide polymorphism assay and detected extensive recombination between the two chromosomes, which we confirmed by non-denaturing fluorescence in situ hybridization (ND-FISH). We constructed BC1F1 and F2 genetic maps that were 65.31 and 63.71 cM long, respectively. Recombination rates between the 5B and 5Sse chromosomes were double the expected rate computed from their meiotic pairing, which we attributed to selection against aneuploid gametes. Recombination rate between 5B and 5Sse was depressed compared to that between 5B chromosomes in the proximal region of the long arm. We integrated ND-FISH signals into the genetic map and constructed a physical map, which we used to map a 172,188,453-bp Ph1 region. Despite the location of the region in a low-recombination region of the 5B chromosome, we detected three crossovers in it. Our data show that Su1-Ph1 is a valuable tool for gene introgression and gene mapping based on recombination between homoeologous chromosomes in wheat.



We thank Moshe Feldman (Weizmann Institute of Science, Rehovot Area, Israel) for providing Ae. searsii accession TE10. We also thank anonymous reviewers for reading the manuscript and valuable suggestions.

Author Contribution statement

HL, JD, PEM, and AD conceived and designed the experiments. HL, LW, M-CL, constructed genetic maps, HL, FN, YZ, and CS performed HD-FISH and analyzed results, and JD, HL, M-CL, PEM, and AD discussed the findings and interpreted the results. JD and HL wrote the first draft of the paper. All authors have read and approved the final draft.


This work was supported in part by the China Scholarship Council, the US National Science Foundation (Grants IOS1212591 and IOS1238231), the USDA Grant 2006-01161, the USDA NIFA Hatch Program 1002302, and the US-Israel BARD Project (Grant IS-4829-15).

Complianace with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2019_3423_MOESM1_ESM.xlsx (41 kb)
Supplementary file1 (XLSX 41 kb)


  1. Akhunov ED, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theor Appl Genet 119:507–517PubMedPubMedCentralGoogle Scholar
  2. Aragon-Alcaide L, Miller T, Schwarzacher T, Reader S, Moore G (1996) A cereal centromeric sequence. Chromosoma 105:261–268PubMedGoogle Scholar
  3. Avni R, Nave M, Eilam T, Sela H, Alekperov C, Peleg Z, Dvorak J, Korol A, Distelfeld A (2014) Ultra-dense genetic map of durum wheat × wild emmer wheat developed using the 90K iSelect SNP genotyping assay. Mol Breed 34:1549–1562Google Scholar
  4. Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K, Jordan KW, Golan G, Deek J, Ben-Zvi B, Ben-Zvi G, Himmelbach A, MacLachlan RP, Sharpe AG, Fritz A, Ben-David R, Budak H, Fahima T, Korol A, Faris JD, Hernandez A, Mikel MA, Levy AA, Steffenson B, Maccaferri M, Tuberosa R, Cattivelli L, Faccioli P, Ceriotti A, Kashkush K, Pourkheirandish M, Komatsuda T, Eilam T, Sela H, Sharon A, Ohad N, Chamovitz DA, Mayer KFX, Stein N, Ronen G, Peleg Z, Pozniak CJ, Akhunov ED, Distelfeld A (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97PubMedGoogle Scholar
  5. Bhullar R, Nagarajan R, Bennypaul H, Sidhu GK, Sidhu G, Rustgi S, von Wettsteina D, Gill KS (2014) Silencing of a metaphase I-specific gene results in a phenotype similar to that of the Pairing homeologous 1 (Ph1) gene mutations. Proc Natl Acad Sci USA 111:14187–14192PubMedGoogle Scholar
  6. Cui Y, Zhang YP, Qi J, Wang HG, Wang RRC, Bao YG, Li XF (2018) Identification of chromosomes in Thinopyrum intermedium and wheat Th. intermedium amphiploids based on multiplex oligonucleotide probes. Genome 61:515–521PubMedGoogle Scholar
  7. Dennis ES, Gerlach WL, Peacock WJ (1980) Identical polypyrimidine-polypurine satellite DNAs in wheat and barley. Heredity 44:344–366Google Scholar
  8. Devi U, Grewal S, Yang CY, Hubbart-Edwards S, Scholefield D, Ashling S, Burridge A, King IP, King J (2019) Development and characterisation of interspecific hybrid lines with genome-wide introgressions from Triticum timopheevii in a hexaploid wheat background. BMC Plant Biol 19:183PubMedPubMedCentralGoogle Scholar
  9. Dvorak J, Gorham J (1992) Methodology of gene transfer by homoeologous recombination into Triticum turgidum: transfer of K+/Na+ discrimination from T. aestivum. Genome 35:639–646Google Scholar
  10. Dvorak J, Zhang HB (1990) Variation in repeated nucleotide sequences sheds light on the phylogeny of the wheat B and G genomes. Proc Natl Acad Sci USA 87:9640–9644PubMedGoogle Scholar
  11. Dvorak J, Zhang HB (1992) Reconstruction of the phylogeny of the genus Triticum from variation in repeated nucleotide sequences. Theor Appl Genet 84:419–429PubMedGoogle Scholar
  12. Dvorak J, di Terlizzi P, Zhang HB, Resta P (1993) The evolution of polyploid wheats: identification of the A genome donor species. Genome 36:21–31Google Scholar
  13. Dvorak J, Dubcovsky J, Luo MC, Devos KM, Gale MD (1995) Differentiation between wheat chromosomes 4B and 4D. Genome 38:1139–1147PubMedGoogle Scholar
  14. Dvorak J, Luo M-C, Yang Z-L (1998) Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 148:423–434PubMedPubMedCentralGoogle Scholar
  15. Dvorak J, Akhunov ED, Akhunov AR, Deal KR, Luo MC (2006a) Molecular characterization of a diagnostic DNA marker for domesticated tetraploid wheat provides evidence for gene flow from wild tetraploid wheat to hexaploid wheat. Mol Biol Evol 23:1386–1396PubMedGoogle Scholar
  16. Dvorak J, Deal KR, Luo MC (2006b) Discovery and mapping of the wheat Ph1 suppressors. Genetics 174:17–27PubMedPubMedCentralGoogle Scholar
  17. Dvorak J, Wang L, Zhu TT, Jorgensen CM, Deal KR, Dai XT, Dawson MW, Muller HG, Luo MC, Ramasamy RK, Dehghani H, Gu YQ, Gill BS, Distelfeld A, Devos KM, Qi P, You FM, Gulick PJ, McGuire PE (2018) Structural variation and rates of genome evolution in the grass family seen through comparison of sequences of genomes greatly differing in size. Plant J 95:487–503PubMedGoogle Scholar
  18. Feldman M, Kislev M (1977) Aegilops searsii, a new species of section Sitopsis (Platystachys). Isr J Bot 26:190–201Google Scholar
  19. Foote T, Roberts M, Kurata N, Sasaki T, Moore G (1997) Detailed comparative mapping of cereal chromosome regions corresponding to the Ph1 locus in wheat. Genetics 147:801–807PubMedPubMedCentralGoogle Scholar
  20. Friebe B, Tuleen NA, Gill BS (1995) Standard karyotype of Triticum searsii and its relationship with other S-genome species and common wheat. Theor Appl Genet 91:248–254PubMedGoogle Scholar
  21. Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acid Res 7:1869–1885PubMedGoogle Scholar
  22. Gill KS, Gill BS, Endo TR, Mukai Y (1993) Fine physical mapping of Ph1, a chromosome pairing regulator gene in polyploid wheat. Genetics 134:1231–1236PubMedPubMedCentralGoogle Scholar
  23. Grewal S, Yang CY, Edwards SH, 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 131:389–406PubMedGoogle Scholar
  24. Griffiths S, Sharp R, Foote TN, Bertin I, Wanous M, Reader S, Colas I, Moore G (2006) Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439:749–752PubMedGoogle Scholar
  25. Gyawali Y, Zhang W, Chao SM, Xu S, Cai XW (2019) Delimitation of wheat ph1b deletion and development of ph1b-specific DNA markers. Theor Appl Genet 132:195–204PubMedGoogle Scholar
  26. IWGSC (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191Google Scholar
  27. Jampates R, Dvorak J (1986) Location of the Ph1 locus in the metaphase chromosome map and the linkage map of the 5Bq arm of wheat. Can J Genet Cytol 28:511–519Google Scholar
  28. Jorgensen C, Luo M-C, Ramasamy R, Dawson M, Gill BS, Korol AB, Distelfeld A, Dvorak J (2017) A high-density genetic map of wild emmer wheat from the Karaca dag region provides new evidence on the structure and evolution of wheat chromosomes. Front Plant Sci 8:1798PubMedPubMedCentralGoogle Scholar
  29. Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare (Japanese). Agric Hort (Tokyo) 19:13–14Google Scholar
  30. Kimber G, Athwal RS (1972) A reassessment of the course of evolution of wheat. Proc Natl Acad Sci USA 69:912–915PubMedGoogle Scholar
  31. Komuro S, Endo R, Shikata K, Kato A (2013) Genomic and chromosomal distribution patterns of various repeated DNA sequences in wheat revealed by a fluorescence in situ hybridization procedure. Genome 56:131–137PubMedGoogle Scholar
  32. Li H, Wang CY, Fu SL, Guo X, Yang BJ, Chen CH, Zhang H, Wang YJ, Liu XL, Han FP, Ji WQ (2014) Development and discrimination of 12 double ditelosomics in tetraploid wheat cultivar DR147. Genome 57:89–95PubMedGoogle Scholar
  33. Li H, Deal KR, Luo MC, Ji WQ, Distelfeld A, Dvorak J (2017) Introgression of the Aegilops speltoides Su1-Ph1 suppressor into wheat. Front Plant Sci 8:2163PubMedPubMedCentralGoogle Scholar
  34. Luo MC, Gu YQ, Puiu D, Wang H, Twardziok SO, Deal KR, Huo NX, Zhu TT, Wang L, Wang Y, McGuire PE, Liu SY, Long H, Ramasamy RK, Rodriguez JC, Van SL, Yuan LX, Wang ZZ, Xia ZQ, Xiao LC, Anderson OD, Ouyang SH, Liang Y, Zimin AV, Pertea G, Qi P, Ennetzen JLB, Dai XT, Dawson MW, Muller HG, Kugler K, Rivarola-Duarte L, Spannagl M, Mayer KFX, Lu FH, Bevan MW, Leroy P, Li PC, You FM, Sun QX, Liu ZY, Lyons E, Wicker T, Salzberg SL, Devos KM, Dvorak J (2017) Genome sequence of the progenitor of the wheat D genome Aegilops tauschii. Nature 551:498–502Google Scholar
  35. McFadden ES, Sears ER (1946) The origin of Triticum spelta and its free-threshing hexaploid relatives. J Hered 37(81–89):107–116Google Scholar
  36. McIntyre CL, Clarke BC, Appels R (1988) Amplification and dispersion of repeated DNA sequences in the Triticeae. Plant Syst Evol 160:39–59Google Scholar
  37. Okamoto M (1957) Asynaptic effect of chromosome V. Wheat Inf Serv 5:6Google Scholar
  38. Rey MD, Martin AC, Higgins J, Swarbreck D, Uauy C, Shaw P, Moore G (2017) Exploiting the ZIP4 homologue within the wheat Ph1 locus has identified two lines exhibiting homoeologous crossover in wheat-wild relative hybrids. Mol Breed 37:95PubMedPubMedCentralGoogle Scholar
  39. Riley R (1960) The diploidization of polyploid wheat. Heredity 15:407–429Google Scholar
  40. Riley R, Chapman V (1958) Genetic control of the cytologically diploid behaviour of hexaploid wheat. Nature 182:713–715Google Scholar
  41. Salina EA, Lim KY, Badaeva ED, Shcherban AB, Adonina IG, Amosova AV, Samatadze TE, Vatolina TY, Zoshchuk SA, Leitch AR (2006) Phylogenetic reconstruction of Aegilops section Sitopsis and the evolution of tandem repeats in the diploids and derived wheat polyploids. Genome 49:1023–1035PubMedGoogle Scholar
  42. Sears ER (1973) Agropyron-wheat transfers induced by homeologous pairing. In: Proceedings of fourth international wheat genetics symposium, pp 191–200Google Scholar
  43. Sears ER (1977) An induced mutant with homoeologous pairing in common wheat. Can J Genet Cytol 19:585–593Google Scholar
  44. Sears ER, Okamoto M (1958) Intergenomic chromosome relationships in hexaploid wheat. In: Proceedings of international congress genetics, pp 258–259Google Scholar
  45. Tang ZX, Yang ZJ, Fu SL (2014) Oligonucleotides replacing the roles of repetitive sequences pAs1, pSc119.2, pTa-535, pTa71, CCS1, and pAWRC.1 for FISH analysis. J Appl Genet 55:313–318PubMedGoogle Scholar
  46. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78Google Scholar
  47. Wang SC, Wong DB, Forrest K, Allen A, Chao SM, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, 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 Biotech J 12:787–796Google Scholar
  48. Zhang W, Zhu XW, Zhang MY, Chao SM, Xu S, Cai XW (2018) Meiotic homoeologous recombination-based mapping of wheat chromosome 2B and its homoeologues in Aegilops speltoides and Thinopyrum elongatum. Theor Appl Genet 131:2381–2395PubMedGoogle Scholar
  49. Zhou SH, Zhang JP, Che YH, Liu WH, Lu YQ, Yang XM, Li XQ, Jia JZ, Liu X, Li LH (2018) Construction of Agropyron Gaertn. genetic linkage maps using a wheat 660K SNP array reveals a homoeologous relationship with the wheat genome. Plant Biotech J 16:818–827Google Scholar
  50. Zhu T, Wang L, Rodriguez JC, Deal KR, Avni R, Distelfeld A, McGuire PE, Dvorak J, Luo MC (2019) Improved genome sequence of wild emmer wheat Zavitan with the aid of optical maps. G3 Genes Genomes Genet 9:619–624Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019
corrected publication 2019

Authors and Affiliations

  • Hao Li
    • 1
    • 2
  • Le Wang
    • 2
  • Ming-Cheng Luo
    • 2
  • Fang Nie
    • 1
  • Yun Zhou
    • 1
  • Patrick E. McGuire
    • 2
  • Assaf Distelfeld
    • 3
  • Xiongtao Dai
    • 4
  • Chun-Peng Song
    • 1
  • Jan Dvorak
    • 2
    Email author
  1. 1.Key Laboratory of Plant Stress Biology, State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life SciencesHenan UniversityKaifengChina
  2. 2.Department of Plant SciencesUniversity of CaliforniaDavisUSA
  3. 3.School of Plant Sciences and Food SecurityTel Aviv UniversityTel AvivIsrael
  4. 4.Department of StatisticsIowa State UniversityAmesUSA

Personalised recommendations