, 214:3 | Cite as

Natural variation in photoperiodic flowering pathway and identification of photoperiod-insensitive accessions in wild wheat, Aegilops tauschii

  • Kayo Koyama
  • Yurika Okumura
  • Emi Okamoto
  • Ryo Nishijima
  • Shigeo Takumi


The D-genome progenitor of hexaploid wheat, Aegilops tauschii Coss., has a wide natural species range in central Eurasia and possesses wide natural variation in heading and flowering time. Here, we report identification of two Ae. tauschii accessions insensitive to short day length. Similarly to a loss or reduced degree of vernalization requirement, the photoperiod-insensitive mutations were found only in the early flowering sublineage (TauL1b) of Ae. tauschii. Quantitative trait locus (QTL) analyses using two F2 mapping populations showed that a QTL for heading time on the long arm of chromosome 5D was related to the early heading phenotype of the photoperiod-insensitive accessions under short-day conditions. In the photoperiod-insensitive accession, expression patterns of two flowering-related genes were altered under short-day conditions compared with the patterns in photoperiod-sensitive accessions. This study indicates that analysis of natural variations in the Ae. tauschii population is useful to find novel genetic loci controlling agronomically important traits.


Flowering time Natural variation Photoperiod sensitivity Quantitative trait locus Wheat 



This work was financially supported by Grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grants-in-Aid for Scientific Research (B) Nos. 21380005 and 16H04862).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (DOCX 3006 kb)


  1. Arora S, Singh N, Kaur S, Bains NS, Uauy C, Poland J, Chhuneja P (2017) Genome-wide association study of grain architecture in wild wheat Aegilops tauschii. Front Plant Sci 8:886CrossRefPubMedPubMedCentralGoogle Scholar
  2. Beales J, Turner A, Griffiths S, Snape JW, Laurie DA (2007) A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115:721–733CrossRefPubMedGoogle Scholar
  3. Bendix C, Marshall CM, Harmon FG (2015) Circadian clock genes universally control key agricultural traits. Mol Plant 8:1135–1152CrossRefPubMedGoogle Scholar
  4. Chen A, Li C, Hu W, Lau MY, Lin H, Rockwell NC, Martin SS, Jernstedt JA, Lagarias JC, Dubcovsky J (2014) Phytochrome C plays a major role in the acceleration of wheat flowering under long-day photoperiod. Proc Natl Acad Sci USA 111:10037–10044CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cockram J, Jones H, Leigh FJ, O’Sullivan D, Powell W, Laurie DA, Greenland AJ (2007) Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. J Exp Bot 58:1231–1244CrossRefPubMedGoogle Scholar
  6. Golovnina KA, Kondratenko EY, Blinov AG, Goncharov NP (2010) Molecular characterization of vernalization loci VRN1 in wild and cultivated wheats. BMC Plant Biol 10:168CrossRefPubMedPubMedCentralGoogle Scholar
  7. Huang L, Wang Q, Zhang LQ, Yuan ZW, Wang JR, Zhang HG, Zheng YL, Liu DC (2012) Haplotype variations of gene Ppd-D1 in Aegilops tauschii and their implications on wheat origin. Genet Resour Crop Evol 59:1027–1032CrossRefGoogle Scholar
  8. Jackson SD (2009) Plant responses to photoperiod. New Phytol 181:517–531CrossRefPubMedGoogle Scholar
  9. Jones H, Gosman N, Horsnell R, Rose GA, Everst LA, Bentley AR, Tha S, Uauy C, Kowalski A, Novoselovic D, Simek R, Kobiljski B, Kondic-Spika A, Brbaklic L, Mitrofanova O, Chesnokov Y, Bonnett D, Greenland A (2013) Strategy for exploiting exotic germplasm using genetic, morphological, and environmental diversity: the Aegilops tauschii Coss. example. Theor Appl Genet 126:1793–1808CrossRefPubMedGoogle Scholar
  10. Kajimura T, Murai K, Takumi S (2011) Distinct genetic regulation of flowering time and grain-filling period based on empirical study of D-genome diversity in synthetic hexaploid wheat lines. Breed Sci 61:130–141CrossRefGoogle Scholar
  11. Kippes N, Chen A, Zhang X, Lukaszewski AJ, Dubcovsky J (2016) Development and characterization of a spring hexaploid wheat line with no functional VRN2 genes. Theor Appl Genet 129:1417–1428CrossRefPubMedPubMedCentralGoogle Scholar
  12. Kobayashi F, Takumi S, Kume S, Ishibashi M, Ohno R, Murai K, Nakamura C (2005) Regulation by Vrn-1/Fr-1 chromosomal intervals of CBF-mediated Cor/Lea gene expression and freezing tolerance in common wheat. J Exp Bot 56:887–895CrossRefPubMedGoogle Scholar
  13. Koyama K, Hatano H, Nakamura J, Takumi S (2012) Characterization of three VERNALIZATION INSENSITIVE3-like (VIL) homologs in wild wheat, Aegilops tauschii Coss. Hereditas 149:62–71CrossRefPubMedGoogle Scholar
  14. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181CrossRefPubMedGoogle Scholar
  15. Law CN, Sutka J, Worland AJ (1978) A genetic study of day length response in wheat. Heredity 41:185–191CrossRefGoogle Scholar
  16. Lewandowska-Sabat AM, Fjellheim S, Rognli OA (2012) The continental-oceanic climate gradient impose clinal variation in vernalization response in Arabidopsis thaliana. Environ Exp Bot 78:109–116CrossRefGoogle Scholar
  17. Lewandowska-Sabat AM, Fjellheim S, Olsen JE, Rognli OA (2017) Local populations of Arabidopsis thaliana show clear relationship between photoperiodic sensitivity of flowering time and altitude. Front Plant Sci 8:1046CrossRefPubMedPubMedCentralGoogle Scholar
  18. Liu Y, Wang L, Mao S, Liu K, Lu Y, Wang J, Wei Y, Zheng Y (2015) Genome-wide association study of 29 morphological traits in Aegilops tauschii. Sci Rep 5:15562CrossRefPubMedPubMedCentralGoogle Scholar
  19. Matsuoka Y (2011) Evolution of polyploid Triticum wheats under cultivation: the role of domestication, natural hybridization and allopolyploid speciation in their diversification. Plant Cell Physiol 52:750–764CrossRefPubMedGoogle Scholar
  20. Matsuoka Y, Nasuda S (2004) Durum wheat as a candidate for the unknown female progenitor of bread wheat: an empirical study with a highly fertile F1 hybrid with Aegilops tauschii Coss. Theor Appl Genet 109:1710–1717CrossRefPubMedGoogle Scholar
  21. Matsuoka Y, Takumi S, Kawahara T (2008) Flowering time diversification and dispersal in central Eurasian wild wheat Aegilops tauschii Coss.: genealogical and ecological framework. PLoS ONE 3:e3138CrossRefPubMedPubMedCentralGoogle Scholar
  22. Matsuoka Y, Nasuda S, Ashida Y, Nitta M, Tsujimoto H, Takumi S, Kawahara T (2013) Genetic basis for spontaneous hybrid genome doubling during allopolyploid speciation of common wheat shown by natural variation analyses of the paternal species. PLoS ONE 8:e68310CrossRefPubMedPubMedCentralGoogle Scholar
  23. Matsuoka Y, Kawahara T, Takumi S (2015) Intraspecific lineage divergence and its association with reproductive trait change during species range expansion in central Eurasian wild wheat Aegilops tauschii Coss. (Poaceae). BMC Evol Biol 15:213CrossRefPubMedPubMedCentralGoogle Scholar
  24. Mizuno N, Yamasaki M, Matsuoka Y, Kawahara T, Takumi S (2010) Population structure of wild wheat progenitor Aegilops tauschii Coss.: implications for intraspecific lineage diversification and evolution of common wheat. Mol Ecol 19:999–1013CrossRefPubMedGoogle Scholar
  25. Mizuno N, Kinoshita M, Kinoshita S, Nishida H, Fujita M, Kato K, Murai K, Nasuda S (2016) Loss-of-function mutations in three homoeologous PHYTOCLOCK 1 genes in common wheat are associated with the extra-early flowering phenotype. PLoS ONE 11:e0165618CrossRefPubMedPubMedCentralGoogle Scholar
  26. Mujeeb-Kazi A, Rosas V, Roldan S (1996) Conservation of the genetic variation of Triticum tauschii (Coss.) Schmalh. (Aegilops squarrosa auct. non L.) in synthetic hexaploid wheats (T. turgidum L. x T. tauschii; 2n = 6x = 42, AABBDD) and its potential utilization for wheat improvement. Genet Res Crop Evol 43:129–134CrossRefGoogle Scholar
  27. Murai K, Ikari C, Shitsukawa N (2005) Pathways that promote the floral transition in wheat. In: Tsunewaki K (ed) Frontiers of wheat bioscience, Memorial Issue of Wheat Information Service. Kihara Memorial Foundation, Yokohama, pp 119–128Google Scholar
  28. Nguyen AT, Iehisa JCM, Kajimura T, Murai K, Takumi S (2013) Identification of quantitative trait loci for flowering-related traits in the D genome of synthetic hexaploid wheat lines. Euphytica 192:401–412CrossRefGoogle Scholar
  29. Nguyen AT, Nishijima R, Kajimura T, Murai K, Takumi S (2015) Quantitative trait locus analysis for flowering-related traits using two F2 populations derived from crosses between Japanese common wheat cultivars and synthetic hexaploids. Genes Genet Syst 90:89–98CrossRefPubMedGoogle Scholar
  30. Saisho D, Ishii M, Hori K, Sato K (2011) Natural variation of barley vernalization requirements: implication of quantitative variation of winter growth habit as an adaptive trait in East Asia. Plant Cell Physiol 52:775–784CrossRefPubMedGoogle Scholar
  31. Saisho D, Takumi S, Matsuoka Y (2016) Salt tolerance during germination and seedling growth of wild wheat Aegilops tauschii and its impact on the species range expansion. Sci Rep 6:38554CrossRefPubMedPubMedCentralGoogle Scholar
  32. Scarth R, Law CN (1983) The location of the photoperiod gene, Ppd2, and an additional genetic factor for ear-emergence time on chromosome 2B of wheat. Heredity 51:607–619CrossRefGoogle Scholar
  33. Snape JW, Quarrie SA, Laurie DA (1996) Comparative mapping and its use for the genetic analysis of agronomic characters in wheat. Euphytica 89:27–31CrossRefGoogle Scholar
  34. Takumi S, Koyama K, Fujiwara K, Kobayashi F (2011) Identification of a large deletion in the first intron of a Vrn-D1 locus associated with loss of vernalization requirement in wild wheat progenitor Aegilops tauschii Coss. Genes Genet Syst 86:183–195CrossRefPubMedGoogle Scholar
  35. Tsunewaki K (1966) Comparative gene analysis of common wheat and its ancestral species. II. Waxiness, growth habit and awnedness. Jpn J Bot 19:175–229Google Scholar
  36. Van Slageren MW (1994) Wild wheats: A monograph of Aegilops L. and Amblyopyrum (Jaub. & Spach) Eig (Poaceae). Wageningen Agricultural University, Wageningen, pp 326–344Google Scholar
  37. Wang S, Basten CJ, Zeng ZB (2011) Windows QTL cartographer 2.5. Department of Statics, North Carolina State University, Raleigh, NC.
  38. Xiang ZG, Zhang LQ, Ning SZ, Zheng YL, Liu DC (2008) Evaluation of Aegilops tauschii for heading date and its gene location in a re-synthesized hexaploid wheat. Agric Sci China 8:1–7CrossRefGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  1. 1.Graduate School of Agricultural ScienceKobe UniversityKobeJapan

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