Skip to main content
Log in

Structural variation in the 5′ upstream region of photoperiod-insensitive alleles Ppd-A1a and Ppd-B1a identified in hexaploid wheat (Triticum aestivum L.), and their effect on heading time

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

For genetic analysis of Ppd-1 homoeologs controlling photoperiodic response of wheat (Triticum aestivum L.), bulk segregant analysis was performed using a doubled haploid (DH) population derived from a cross of Japanese wheat genotypes Winter-Abukumawase and Chihokukomugi. Based on the segregation of simple sequence repeat markers linked to the Ppd-1 homoeologs, Winter-Abukumawase carried insensitive alleles Ppd-B1a and Ppd-D1a and Chihokukomugi carried a single insensitive allele (Ppd-A1a) that was first found in common wheat. The genomic sequence of Ppd-1 homoeologs including the 5′ upstream region was determined and compared between the two genotypes. Ppd-D1a of Winter-Abukumawase had a deletion of 2,089 bp that was already reported for Ciano 67. Critical sequence polymorphism causing photoperiod insensitivity was not detected from the translation start codon to the 3′ untranslated region of Ppd-A1 and Ppd-B1. However, novel mutations were found in the 5′ upstream region. Ppd-A1a of Chihokukomugi had a deletion of 1,085 bp and Ppd-B1a of Winter-Abukumawase had an insertion of 308 bp. A total of 80 DH lines were classified into eight genotypes by PCR-based genotyping using specific primer sets to detect the In/Dels in the 5′ upstream region of three Ppd-1 genes. The heading dates of the DH lines differed significantly between the eight genotypes, showing that each of the three insensitive alleles accelerates heading by 7–9 days compared with the photoperiod-sensitive genotype. Interaction between the three genes was also significant.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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 115:721–733

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarti B, Singh SD, Nagarajan S, Aggarwal PK (2011) Impact of temperature on phenology and pollen sterility of wheat varieties. Aust J Crop Sci 5:1039–1043

    Google Scholar 

  • Cockram J, Mackay IJ, O’Sullivan DM (2007) The role of double-stranded break repair in the creation of phenotypic diversity at cereal VRN1 loci. Genetics 177:2535–2539

    Article  PubMed  CAS  Google Scholar 

  • Dunford RP, Yano M, Kurata N, Sasaki T, Huestis G, Rocheford T, Laurie DA (2002) Comparative mapping of the barley Ppd-H1 photoperiod response gene region, which lies close to a junction between two rice linkage segments. Genetics 161:825–834

    PubMed  CAS  Google Scholar 

  • Fujita M, Taniguchi Y, Ujihara K, Sasaki A (1995) Ear primordia development and stem elongation of near-isogenic lines for vernalization requirement in extremely-early maturing wheat cultivars (Triticum aestivum L.). Breed Sci 45:97–104 (in Japanese with English summary)

    Google Scholar 

  • Gonzalez FG, Slafer GA, Miralles DJ (2005) Pre-anthesis development and number of fertile florets in wheat as affected by photoperiod sensitivity genes Ppd-D1 and Ppd-B1. Euphytica 146:253–269

    Article  Google Scholar 

  • Hanocq E, Laperche A, Jaminon O, Lainé AL, Le Gouis J (2007) Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis. Theor Appl Genet 114:569–584

    Article  PubMed  CAS  Google Scholar 

  • Hoogendoorn J (1985) A reciprocal F1 monosomic analysis of the genetic control of the time of ear emergence, number of leaves and number of spikelets in wheat (Triticum aestivum L.). Euphytica 34:545–558

    Article  Google Scholar 

  • Hoshino T, Kato K, Ueno K (2000) Japanese wheat pool. In: Bonjean A, Clavel K, Angus B (eds) World wheat book. Tec & Doc/Intercept Ltd., Paris, pp 703–726

    Google Scholar 

  • Hudson ME, Quail PH (2003) Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol 133:1605–1616

    Article  PubMed  CAS  Google Scholar 

  • Kato K, Yamagata H (1988) Method for evaluation of chilling requirement and narrow-sense earliness of wheat cultivars. Jpn J Breed 38:172–186

    Google Scholar 

  • Kato K, Yamashita S (1991) Varietal variation in photoperiodic response, chilling requirement and narrow-sense earliness and their relation to heading time in wheat (Triticum aestivum L.). Jpn J Breed 41:475–484

    Google Scholar 

  • Kato K, Nakamura W, Tabiki T, Miura H (2001) Detection of loci controlling seed dormancy on group 4 chromosomes of wheat and comparative mapping with rice and barley genomes. Theor Appl Genet 102:980–985

    Article  CAS  Google Scholar 

  • Keim DL, Welsh JR, Mcconnell RL (1973) Inheritance of photoperiodic heading response in winter and spring cultivars of bread wheat. Can J Plant Sci 53:247–250

    Article  Google Scholar 

  • Klaimi YY, Qualset CO (1973) Genetics of heading time in wheat (Triticum aestivum L.). I. The inheritance of photoperiodic response. Genetics 74:139–156

    PubMed  CAS  Google Scholar 

  • Laurie DA, Pratchett N, Snape JW, Bezant JH (1995) RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter x spring barley (Hordeum vulgare L.) cross. Genome 38:575–585

    Article  PubMed  CAS  Google Scholar 

  • Lupton FGH (1987) History of wheat breeding. In: Lupton FGH (ed) Wheat breeding. Chapman and Hall, London, pp 51–70

    Google Scholar 

  • Marcellos H, Single WK (1984) Frost injury in wheat ears after ear emergence. Aust J Plant Physiol 11:7–15

    Article  Google Scholar 

  • Michael TP, McClung CR (2003) Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. Plant Physiol 132:629–639

    Article  PubMed  CAS  Google Scholar 

  • Michael TP, Mockler TC, Breton G, McEntee C, Byer A, Trout JD, Hazen SP, Shen R, Priest HD, Sullivan CM, Givan SA, Yanovsky M, Hong F, Kay SA, Chory J (2008) Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet 4:e14

    Article  PubMed  Google Scholar 

  • Mohler V, Lukman R, Ortiz-Islas S, William M, Worland AJ, van Beem J, Wenzel G (2004) Genetic and physical mapping of photoperiod insensitive gene Ppd-B1 in common wheat. Euphytica 138:33–40

    Article  CAS  Google Scholar 

  • Murakami M, Matsushika A, Ashikari M, Yamashino T, Mizuno T (2005) Circadian-associated rice pseudo response regulators (OsPRRs): insight into the control of flowering time. Biosci Biotechnol Biochem 69:410–414

    Article  PubMed  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  PubMed  CAS  Google Scholar 

  • Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua NH, Sakakibara H (2010) PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22:594–605

    Article  PubMed  CAS  Google Scholar 

  • Nam JH, Kim HS (2000) Korean wheat pool. In: Bonjean A, Clavel K, Angus B (eds) World wheat book. Tec & Doc/Intercept Ltd., Paris, pp 727–752

    Google Scholar 

  • Pirasteh B, Welsh JR (1975) Monosomic analysis of photoperiod response in wheat. Crop Sci 15:503–505

    Article  Google Scholar 

  • Pruneda-Paz JL, Breton G, Para A, Kay SA (2009) A functional genomic approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323:1481–1485

    Article  PubMed  CAS  Google Scholar 

  • Pugsley AT (1965) Inheritance of a correlated day-length response in spring wheat. Nature 207:108

    Article  Google Scholar 

  • 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 51:607–619

    Article  Google Scholar 

  • Scarth R, Law CN (1984) The control of the day-length responses in wheat by the group 2 chromosomes. Z Pflanzenzüchtg 92:140–150

    Google Scholar 

  • Schindler U, Beckmann H, Cashmore AR (1992) TGA1 and G-box binding factors: two distinct classes of Arabidopsis leucine zipper proteins compete for the G-box-like element TGACGTGG. Plant Cell 4:1309–1319

    PubMed  CAS  Google Scholar 

  • Seki M, Chono M, Matsunaka H, Fujita M, Oda S, Kubo K, Kiribuchi-Otobe C, Kojima H, Nishida H, Kato K (2011) Distribution of photoperiod-insensitive alleles Ppd-B1a and Ppd-D1a and their effect on heading time in Japanese wheat cultivars. Breed Sci 61:405–412

    Article  PubMed  CAS  Google Scholar 

  • Shindo C, Tsujimoto H, Sasakuma T (2003) Segregation analysis of heading traits in hexaploid wheat utilizing recombinant inbred lines. Heredity 90:56–63

    Article  PubMed  CAS  Google Scholar 

  • Snape JW, Butterworth K, Whitechurch E, Worland AJ (2001) Waiting for fine times: genetics of flowering time in wheat. Euphytica 119:185–190

    Article  CAS  Google Scholar 

  • Spensley M, Kim J-Y, Picot E, Reid J, Ott S, Helliwell C, Carré IA (2009) Evolutionarily conserved regulatory motifs in the promoter of the Arabidopsis clock gene LATE ELONGATED HYPOCOTYL. Plant Cell 21:2606–2623

    Article  PubMed  CAS  Google Scholar 

  • Tanio M, Kato K (2007) Development of near-isogenic lines for photoperiod-insensitive genes, Ppd-B1 and Ppd-D1, carried by the Japanese wheat cultivars and their effect on apical development. Breed Sci 57:65–72

    Article  Google Scholar 

  • Tanio M, Kato K, Ishikawa N, Tamura Y, Sato M, Takagi H, Matsuoka M (2005) Genetic analysis of photoperiod response in wheat and its relation with the earliness of heading in the Southwestern part of Japan. Breed Sci 55:327–334

    Article  Google Scholar 

  • Welsh JR, Keim DL, Pirasteh B, Richards RD (1973) Genetic control of photoperiod response in wheat. In: Proceedings of 4th International Wheat Genetics Symposium, Columbia, USA, pp 879–884

  • Wilhelm EP, Turner AS, Laurie DA (2009) Photoperiod insensitive Ppd-A1a mutations in tetraploid wheat (Triticum durum Desf.). Theor Appl Genet 118:285–294

    Article  PubMed  CAS  Google Scholar 

  • Worland AJ (1996) The influence of flowering time genes on environmental adaptability in European wheats. Euphytica 89:49–57

    Article  Google Scholar 

  • Worland AJ, Petrovic S, Law CN (1988) Genetic analysis of chromosome 2D of wheat II. The importance of this chromosome to Yugoslavian varieties. Plant Breed 100:247–259

    Article  Google Scholar 

  • Yasuda S, Shimoyama H (1965) Analysis of internal factors influencing the heading time of wheat varieties. Ber Ohara Inst Landw Biol Okayama Univ 13:23–38

    Google Scholar 

Download references

Acknowledgments

This study was partly supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Green Technology Project GD-3005) and the Japan Society for the Promotion of Science (JSPS) Asian CORE Program entitled “Cooperative Research and Educational Center for Important Plant Genetic Resources in East Asia”.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kenji Kato.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 10 kb)

11032_2012_9765_MOESM2_ESM.ppt

Supplementary Fig. S1 PCR assays to identify the Ppd-1 genotype of cultivars Winter-Abukumawase (W-AB), Chihokukomugi (CK), Chinese Spring (CS) and Haruhikari (HH), using diagnostic PCR primers shown in Supplementary Table S1 and Fig. 2. a Ppd-A1a.1 allele of CK (338-bp) is clearly distinguished by multiplex PCR to amplify the 5′ upstream region of Ppd-A1. b Ppd-B1a.1 allele of W-AB (620 bp) is clearly distinguished by amplifying the 5′ upstream region of Ppd-B1. c Ppd-D1a.1 allele of W-AB (415 bp) is clearly distinguished by multiplex PCR to amplify the 5′ upstream region of Ppd-D1. M 100-bp DNA ladder (PDF 51 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nishida, H., Yoshida, T., Kawakami, K. et al. Structural variation in the 5′ upstream region of photoperiod-insensitive alleles Ppd-A1a and Ppd-B1a identified in hexaploid wheat (Triticum aestivum L.), and their effect on heading time. Mol Breeding 31, 27–37 (2013). https://doi.org/10.1007/s11032-012-9765-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-012-9765-0

Keywords

Navigation