Theoretical and Applied Genetics

, Volume 115, Issue 5, pp 721–733 | Cite as

A Pseudo-Response Regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.)

  • James Beales
  • Adrian Turner
  • Simon Griffiths
  • John W. Snape
  • David A. LaurieEmail author
Original Paper


Ppd-D1 on chromosome 2D is the major photoperiod response locus in hexaploid wheat (Triticum aestivum). A semi-dominant mutation widely used in the “green revolution” converts wheat from a long day (LD) to a photoperiod insensitive (day neutral) plant, providing adaptation to a broad range of environments. Comparative mapping shows Ppd-D1 to be colinear with the Ppd-H1 gene of barley (Hordeum vulgare) which is a member of the pseudo-response regulator (PRR) gene family. To investigate the relationship between wheat and barley photoperiod genes we isolated homologues of Ppd-H1 from a ‘Chinese Spring’ wheat BAC library and compared them to sequences from other wheat varieties with known Ppd alleles. Varieties with the photoperiod insensitive Ppd-D1a allele which causes early flowering in short (SD) or LDs had a 2 kb deletion upstream of the coding region. This was associated with misexpression of the 2D PRR gene and expression of the key floral regulator FT in SDs, showing that photoperiod insensitivity is due to activation of a known photoperiod pathway irrespective of day length. Five Ppd-D1 alleles were found but only the 2 kb deletion was associated with photoperiod insensitivity. Photoperiod insensitivity can also be conferred by mutation at a homoeologous locus on chromosome 2B (Ppd-B1). No candidate mutation was found in the 2B PRR gene but polymorphism within the 2B PRR gene cosegregated with the Ppd-B1 locus in a doubled haploid population, suggesting that insensitivity on 2B is due to a mutation outside the sequenced region or to a closely linked gene.


Photoperiod Response Photoperiod Insensitivity Photoperiod Insensitive Allele Single Chromosome Substitution Line Photoperiod Sensitive Allele 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by grant 208/D18107 from the UK Biotechnology and Biological Sciences Research Council and by grant-in-aid to the John Innes Centre from the same source.

Supplementary material

122_2007_603_MOESM1_ESM.pdf (95 kb)
Fig. S1 PCR amplification of a genome specific amplicon from the 3′ UTR of TaCO1 in ‘Chinese Spring’ nullisomic-tetrasomic lines. The respective nullisomic chromosome is indicated below each track and the arrow shows the expected band size. Absence of the band in the nullisomic 7B line shows that the product derives from this chromosome (PDF 95 kb)
122_2007_603_MOESM2_ESM.pdf (215 kb)
Fig. S2 PCR amplification of PRR gene amplicons from ‘Chinese Spring’ nullisomic-tetrasomic lines of the group 2 chromosomes. This shows that the amplicons used to measure the expression of the 2A, 2B and 2D PRR genes are specific to their respective chromosomes (PDF 216 kb)
122_2007_603_MOESM3_ESM.doc (38 kb)
Supplementary material (DOC 38 kb)


  1. Allouis S, Moore G, Bellec A, Sharp R, Faivre Rampant P, Mortimer K, Pateyron S, Foote TN, Griffiths S, Caboche M, Chalhoub B (2003) Construction and characterisation of a hexaploid wheat (Triticum aestivum L.) BAC library from the reference germplasm ‘Chinese Spring’. Cereal Res Commun 31:331–338Google Scholar
  2. Borlaug NE (1983) Contributions of conventional plant breeding to food production. Science 219:689–693CrossRefGoogle Scholar
  3. Börner A, Korzun V, Worland AJ (1998) Comparative genetic mapping of loci affecting plant height and development in cereals. Euphytica 100:245–248CrossRefGoogle Scholar
  4. Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder MS, Weber WE (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936PubMedCrossRefGoogle Scholar
  5. Butterworth KJ (2000) Flowering time genes of wheat and their influence on environmental adaptability. PhD Thesis, University of East AngliaGoogle Scholar
  6. 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 58:1231–1244PubMedCrossRefGoogle Scholar
  7. Feschotte C, Wessler SR (2002) Mariner-like transposases are widespread and diverse in flowering plants. Proc Natl Acad Sci USA 99:280–285PubMedCrossRefGoogle Scholar
  8. Feschotte C, Swamy L, Wessler SR (2003) Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with Stowaway miniature inverted repeat transposable elements (MITEs). Genetics 163:747–758PubMedGoogle Scholar
  9. Fu D, Szucs P, Yan L, Helguera M, Skinner JS, von Zitzewitz J, Hayes PM, Dubcovsky J (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol Genet Genom 273:54–65CrossRefGoogle Scholar
  10. Fujimori S, Washio T, Tomita M (2005) GC-compositional strand bias around transcription start sites in plants and fungi. BMC Genomics 6: Art. No. 26Google Scholar
  11. Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley (Hordeum vulgare), rice (Oryza sativa) and Arabidopsis thaliana. Plant Physiol 131:1855–1867PubMedCrossRefGoogle Scholar
  12. Hanocq E, Niarquin M, Heumez E, Rousset M, Le Gouis J (2004) Detection and mapping of QTL for earliness components in a bread wheat recombinant inbred lines population. Theor Appl Genet 110:106–115PubMedCrossRefGoogle Scholar
  13. Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722PubMedCrossRefGoogle Scholar
  14. Islam-Faridi MN (1988) Genetical studies of grain protein and developmental characters in wheat. PhD Thesis, University of CambridgeGoogle Scholar
  15. Kato K, Yokoyama H (1992) Geographical variation in heading characters among wheat landraces, Triticum aestivum L, and its implication for their adaptability. Theor Appl Genet 84:259–265CrossRefGoogle Scholar
  16. Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43:1096–1105PubMedCrossRefGoogle Scholar
  17. Laurie DA (1997) Comparative genetics of flowering time in cereals. Plant Mol Biol 35:167–177PubMedCrossRefGoogle Scholar
  18. Laurie DA, Pratchett N, Bezant JH, Snape JW (1995) RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter × spring barley (Hordeum vulgare L.) cross. Genome 38:575–585Google Scholar
  19. Law CN (1987) The genetic control of day-length response in wheat. In: Atherton JE (ed) Manipulation of flowering. Butterworths, London, pp 225–240Google Scholar
  20. Law CN, Sutka J, Worland AJ (1978) A genetic study of day-length response in wheat. Heredity 41:185–191Google Scholar
  21. Law CN, Worland AJ (1997) Genetic analysis of some flowering time and adaptive traits in wheat. New Phytol 137:19–28CrossRefGoogle Scholar
  22. Lin HX, Yamamoto T, Sasaki T, Yano M (2000) Characterization and detection of epistaic interactions of 3 QTLs, Hd1, Hd2, and Hd3, controlling heading date in rice using nearly isogenic lines. Theor Appl Genet 101:1021–1028CrossRefGoogle Scholar
  23. Matsushika A, Makino S, Kojima M, Mizuno T (2000) Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: Insight into the plant circadian clock. Plant Cell Physiol 41:1002–1012PubMedCrossRefGoogle Scholar
  24. McIntosh RA, Yamazaki Y, Devos KM, Dubcovsky J, Rogers WJ, Appels R (2003) Catalogue of gene symbols in wheat.
  25. Mizuno T, Nakamichi N (2005) Pseudo-response regulators (PRRs) or true oscillator components (TOCs). Plant Cell Physiol 46:677–685PubMedCrossRefGoogle Scholar
  26. 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 138:33–40CrossRefGoogle Scholar
  27. Murakami M, Ashikari M, Miura K, Yamashino T, Mizuno T (2003) The evolutionarily conserved OsPRR quintet: rice pseudo-response regulators implicated in circadian rhythm. Plant Cell Physiol 44:1229–1236PubMedCrossRefGoogle Scholar
  28. 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 69:410–414PubMedCrossRefGoogle Scholar
  29. Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66PubMedCrossRefGoogle Scholar
  30. Robson F, Costa MMR, Hepworth SR, Vizir I, Pineiro M, Reeves PH, Putterill J, Coupland G (2001) Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J 28:619–631PubMedCrossRefGoogle Scholar
  31. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616PubMedCrossRefGoogle Scholar
  32. Scarth R, Law CN (1983) The location of the photoperiodic gene, Ppd2, and an additional genetic factor for ear-emergence on chromosome 2B of wheat. Heredity 51:607–619Google Scholar
  33. Scarth R, Law CN (1984) The control of the day-length response in wheat by the group 2 chromosomes. Z Pflanzenzuchtg 92:140–150Google Scholar
  34. Sharp PJ, Kreis M, Shewry PR, Gale MD (1988) Location of B-amylase sequences in wheat and its relatives. Theor Appl Genet 75:286–290CrossRefGoogle Scholar
  35. Skøt L, Humphreys MO, Armstead I, Heywood S, Skot KP, Sanderson R, Thomas ID, Chorlton KH, Hamilton NRS (2005) An association mapping approach to identify flowering time genes in natural populations of Lolium perenne (L.) Mol Breed 15:233–245CrossRefGoogle Scholar
  36. Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289:768–771PubMedCrossRefGoogle Scholar
  37. Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1119PubMedCrossRefGoogle Scholar
  38. Thomas B, Vince-Prue D (1997) Photoperiodism in plants. 2nd edn. Academic, LondonGoogle Scholar
  39. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034PubMedCrossRefGoogle Scholar
  40. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006PubMedCrossRefGoogle Scholar
  41. Welsh JR, Keim DL, Pirasteh B, Richards RD (1973) Genetic control of photoperiod response in wheat. In: Proceedings of 4th International Wheat Genet Symposium. University of Missouri, Columbia, MO, USA, pp 879–884Google Scholar
  42. Worland AJ (1999) The importance of Italian wheats to worldwide varietal improvement. J Genet Breed 53:165–173Google Scholar
  43. Worland AJ, Law CN (1986) Genetic-analysis of chromosome 2D of wheat. 1. The location of genes affecting height, day-length insensitivity, hybrid dwarfism and yellow-rust resistance. Z Pflanzenzuchtung 96:331–345Google Scholar
  44. Worland T, Snape JW (2001) Genetic basis of worldwide wheat varietal improvement. In: Bonjean AP, Angus WJ (eds) The world wheat book: a history of wheat breeding. Lavoisier Publishing, Paris, pp 59–100Google Scholar
  45. Worland AJ, Appendino ML, Sayers EJ (1994) The distribution in European winter wheats of genes that influence ecoclimatic adaptability whilst determining photoperiodic insensitivity and plant height. Euphytica 80:219–228CrossRefGoogle Scholar
  46. Worland AJ, Börner A, Korzun V, Li WM, Petrovic S, Sayers EJ (1998) The influence of photoperiod genes to the adaptability of European winter wheats. Euphytica 100:385–394CrossRefGoogle Scholar
  47. Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268PubMedCrossRefGoogle Scholar
  48. Yan LL, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644PubMedCrossRefGoogle Scholar
  49. Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586PubMedCrossRefGoogle Scholar
  50. Yano M, Katayose Y, Ashikara M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2483PubMedCrossRefGoogle Scholar
  51. Zeilinger MN, Farre EM, Taylor SR, Kay SA, Doyle FJ (2006) A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Molecular Systems Biology 2: Art. No. 58Google Scholar
  52. Zhao XY, Liu MS, Li JR, Guan CM, Zhang XS (2005) The wheat TaGI1, involved in photoperiodic flowering, encodesan Arabidopsis GI ortholog. Plant Mol Biol 58:53–64PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • James Beales
    • 1
  • Adrian Turner
    • 1
  • Simon Griffiths
    • 1
  • John W. Snape
    • 1
  • David A. Laurie
    • 1
    Email author
  1. 1.Crop Genetics DepartmentJohn Innes CentreNorwichUK

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