Table of Contents
International Journal of Plant Genomics
Volume 2015, Article ID 874361, 17 pages
http://dx.doi.org/10.1155/2015/874361
Research Article

Genome-Wide Comparative Analysis of Flowering-Related Genes in Arabidopsis, Wheat, and Barley

1Feed Crops Branch, Alberta Agriculture and Forestry, 7000-113 Street, Edmonton, AB, Canada T6H 5T6
2Department of Agricultural, Food and Nutritional Science, University of Alberta, 410 Agriculture/Forestry Centre, Edmonton, AB, Canada T6G 2P5

Received 4 June 2015; Revised 24 July 2015; Accepted 10 August 2015

Academic Editor: Peter Langridge

Copyright © 2015 Fred Y. Peng et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Dvořák, P. di Terlizzi, H.-B. Zhang, and P. Resta, “The evolution of polyploid wheats: identification of the A genome donor species,” Genome, vol. 36, no. 1, pp. 21–31, 1993. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Dvořák and H.-B. Zhang, “Variation in repeated nucleotide sequences sheds light on the phylogeny of the wheat B and G genomes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 24, pp. 9640–9644, 1990. View at Publisher · View at Google Scholar · View at Scopus
  3. T. Naranjo and E. Corredor, “Clustering of centromeres precedes bivalent chromosome pairing of polyploid wheats,” Trends in Plant Science, vol. 9, no. 5, pp. 214–217, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. K. M. Devos, J. Doležel, and C. Feuillet, “Genome organization and comparative genomics,” Wheat Science and Trade, pp. 327–367, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. G. Moore, “Cereal genome evolution: Pastoral pursuits with “Lego” genomes,” Current Opinion in Genetics and Development, vol. 5, no. 6, pp. 717–724, 1995. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Brenchley, M. Spannagl, M. Pfeifer et al., “Analysis of the bread wheat genome using whole-genome shotgun sequencing,” Nature, vol. 491, no. 7426, pp. 705–710, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. The International Barley Genome Sequencing Consortium, “A physical, genetic and functional sequence assembly of the barley genome,” Nature, vol. 491, no. 7426, pp. 711–716, 2012. View at Publisher · View at Google Scholar
  8. The International Wheat Genome Sequencing Consortium, “A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome,” Science, vol. 345, no. 6194, Article ID 1251788, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. A. N. Dodd, N. Salathia, A. Hall et al., “Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage,” Science, vol. 309, no. 5734, pp. 630–633, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Cockram, H. Jones, F. J. Leigh et al., “Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity,” Journal of Experimental Botany, vol. 58, no. 6, pp. 1231–1244, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Nitcher, S. Pearce, G. Tranquilli, X. Zhang, and J. Dubcovsky, “Effect of the hope FT-B1 allele on wheat heading time and yield components,” Journal of Heredity, vol. 105, no. 5, pp. 666–675, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Thepot, G. Restoux, I. Goldringer et al., “Efficiently tracking selection in a multiparental population: the case of earliness in wheat,” Genetics, vol. 199, no. 2, pp. 609–623, 2015. View at Publisher · View at Google Scholar
  13. R.-C. Yang and B. J. Ham, “Stability of genome-wide QTL effects on malt α-amylase activity in a barley doubled-haploid population,” Euphytica, vol. 188, no. 1, pp. 131–139, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. I. R. Henderson and C. Dean, “Control of Arabidopsis flowering: the chill before the bloom,” Development, vol. 131, no. 16, pp. 3829–3838, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. A. S. Turner, S. Faure, Y. Zhang, and D. A. Laurie, “The effect of day-neutral mutations in barley and wheat on the interaction between photoperiod and vernalization,” Theoretical and Applied Genetics, vol. 126, no. 9, pp. 2267–2277, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Fjellheim, S. Boden, and B. Trevaskis, “The role of seasonal flowering responses in adaptation of grasses to temperate climates,” Frontiers in Plant Science, vol. 5, 2014. View at Publisher · View at Google Scholar
  17. F. Fornara, A. de Montaigu, and G. Coupland, “SnapShot: control of flowering in Arabidopsis,” Cell, vol. 141, no. 3, pp. 550–550.e2, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Nakamichi, T. Kiba, R. Henriques, T. Mizuno, N.-H. Chua, and H. Sakakibara, “PSEUDO-RESPONSE ReGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock,” The Plant Cell, vol. 22, no. 3, pp. 594–605, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. P. A. Salomé, D. Weigel, and C. R. McClunga, “The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation,” The Plant Cell, vol. 22, no. 11, pp. 3650–3661, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. F. Valverde, “CONSTANS and the evolutionary origin of photoperiodic timing of flowering,” Journal of Experimental Botany, vol. 62, no. 8, pp. 2453–2463, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. F. Andrés and G. Coupland, “The genetic basis of flowering responses to seasonal cues,” Nature Reviews Genetics, vol. 13, no. 9, pp. 627–639, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. C.-H. Jung, C. E. Wong, M. B. Singh, and P. L. Bhalla, “Comparative genomic analysis of soybean flowering genes,” PLoS ONE, vol. 7, no. 6, Article ID e38250, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. X. Gu, C. Le, Y. Wang et al., “Arabidopsis FLC clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues,” Nature Communications, vol. 4, article 2947, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Amasino, “Seasonal and developmental timing of flowering,” The Plant Journal, vol. 61, no. 6, pp. 1001–1013, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. R. M. Amasino and S. D. Michaels, “The timing of flowering,” Plant Physiology, vol. 154, no. 2, pp. 516–520, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Johansson and D. Staiger, “Time to flower: interplay between photoperiod and the circadian clock,” Journal of Experimental Botany, vol. 66, no. 3, pp. 719–730, 2015. View at Publisher · View at Google Scholar
  27. J. Beales, A. Turner, S. Griffiths, J. W. Snape, and D. A. Laurie, “A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.),” Theoretical and Applied Genetics, vol. 115, no. 5, pp. 721–733, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Cane, H. A. Eagles, D. A. Laurie et al., “Ppd-B1 and Ppd-D1 and their effects in southern Australian wheat,” Crop and Pasture Science, vol. 64, no. 2, pp. 100–114, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Nishida, T. Yoshida, K. Kawakami 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,” Molecular Breeding, vol. 31, no. 1, pp. 27–37, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. L. M. Shaw, A. S. Turner, L. Herry, S. Griffiths, and D. A. Laurie, “Mutant alleles of Photoperiod-1 in Wheat (Triticum aestivum L.) that confer a late flowering phenotype in long days,” PLoS ONE, vol. 8, no. 11, Article ID e79459, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. X. Y. Zhao, M. S. Liu, J. R. Li, and et al, “The wheat TaGI1, involved in photoperiodic flowering, encodes an Arabidopsis GI ortholog,” Plant Molecular Biology, vol. 58, no. 1, pp. 53–64, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Dubcovsky, A. Loukoianov, D. Fu, M. Valarik, A. Sanchez, and L. Yan, “Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2,” Plant Molecular Biology, vol. 60, no. 4, pp. 469–480, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Chen and J. Dubcovsky, “Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering,” PLoS Genetics, vol. 8, no. 12, Article ID e1003134, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Gomez, L. Vanzetti, M. Helguera, L. Lombardo, J. Fraschina, and D. J. Miralles, “Effect of Vrn-1, Ppd-1 genes and earliness per se on heading time in Argentinean bread wheat cultivars,” Field Crops Research, vol. 158, pp. 73–81, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Turner, J. Beales, S. Faure, R. P. Dunford, and D. A. Laurie, “The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley,” Science, vol. 310, no. 5750, pp. 1031–1034, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. R. P. Dunford, S. Griffiths, V. Christodoulou, and D. A. Laurie, “Characterisation of a barley (Hordeum vulgare L.) homologue of the Arabidopsis flowering time regulator GIGANTEA,” Theoretical and Applied Genetics, vol. 110, no. 5, pp. 925–931, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. B. Trevaskis, M. N. Hemming, W. J. Peacock, and E. S. Dennis, “HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status,” Plant Physiology, vol. 140, no. 4, pp. 1397–1405, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Campoli, B. Drosse, I. Searle, G. Coupland, and M. Von Korff, “Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS,” Plant Journal, vol. 69, no. 5, pp. 868–880, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Faure, A. S. Turner, D. Gruszka et al., “Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 21, pp. 8328–8333, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. S. A. Boden, D. Weiss, J. J. Ross et al., “EARLY FLOWERING3 regulates flowering in spring barley by mediating Gibberellin production and FLOWERING LOCUS T expression,” The Plant Cell, vol. 26, no. 4, pp. 1557–1569, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. A. M. Alqudah, R. Sharma, R. K. Pasam, A. Graner, B. Kilian, and T. Schnurbusch, “Genetic dissection of photoperiod response based on gwas of pre-anthesis phase duration in spring barley,” PLoS ONE, vol. 9, no. 11, Article ID e113120, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Distelfeld, C. Li, and J. Dubcovsky, “Regulation of flowering in temperate cereals,” Current Opinion in Plant Biology, vol. 12, no. 2, pp. 178–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Greenup, W. J. Peacock, E. S. Dennis, and B. Trevaskis, “The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals,” Annals of Botany, vol. 103, no. 8, pp. 1165–1172, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Trevaskis, “The central role of the VERNALIZATION1 gene in the vernalization response of cereals,” Functional Plant Biology, vol. 37, no. 6, pp. 479–487, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Trevaskis, M. N. Hemming, E. S. Dennis, and W. J. Peacock, “The molecular basis of vernalization-induced flowering in cereals,” Trends in Plant Science, vol. 12, no. 8, pp. 352–357, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. C. R. McClung, “A modern circadian clock in the common angiosperm ancestor of monocots and eudicots,” BMC Biology, vol. 8, article 55, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. C. R. McClung and R. A. Gutiérrez, “Network news: prime time for systems biology of the plant circadian clock,” Current Opinion in Genetics and Development, vol. 20, no. 6, pp. 588–598, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Blümel, N. Dally, and C. Jung, “Flowering time regulation in crops-what did we learn from Arabidopsis?” Current Opinion in Biotechnology, vol. 32, pp. 121–129, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. Y. H. Song, J. S. Shim, H. A. Kinmonth-Schultz, and T. Imaizumi, “Photoperiodic flowering: time measurement mechanisms in leaves,” Annual Review of Plant Biology, vol. 66, pp. 441–464, 2015. View at Publisher · View at Google Scholar
  50. J. Colasanti and V. Coneva, “Mechanisms of floral induction in grasses: something borrowed, something new,” Plant Physiology, vol. 149, no. 1, pp. 56–62, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. C. P. G. Calixto, R. Waugh, and J. W. S. Brown, “Evolutionary relationships among barley and Arabidopsis core circadian clock and clock-associated genes,” Journal of Molecular Evolution, vol. 80, no. 2, pp. 108–119, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Faure, J. Higgins, A. Turner, and D. A. Laurie, “The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare),” Genetics, vol. 176, no. 1, pp. 599–609, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Nitcher, A. Distelfeld, C. Tan, L. Yan, and J. Dubcovsky, “Increased copy number at the HvFT1 locus is associated with accelerated flowering time in barley,” Molecular Genetics and Genomics, vol. 288, no. 5-6, pp. 261–275, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Yan, D. Fu, C. Li et al., “The wheat and barley vernalization gene VRN3 is an orthologue of FT,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 51, pp. 19581–19586, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. V. Hecht, F. Foucher, C. Ferrándiz et al., “Conservation of Arabidopsis flowering genes in model legumes,” Plant Physiology, vol. 137, no. 4, pp. 1420–1434, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Y. Kim, Y. J. Kang, T. Lee, and S.-H. Lee, “Divergence of flowering-related genes in three legume species,” The Plant Genome, vol. 6, no. 3, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. S. K. Kim, T. Lee, Y. J. Kang et al., “Genome-wide comparative analysis of flowering genes between Arabidopsis and mungbean,” Genes & Genomics, vol. 36, no. 6, pp. 799–808, 2014. View at Publisher · View at Google Scholar · View at Scopus
  58. C. E. Grover, J. P. Gallagher, and J. F. Wendel, “Candidate gene identification of flowering time genes in Cotton,” The Plant Genome, 2015. View at Publisher · View at Google Scholar
  59. M. Murakami, Y. Tago, T. Yamashino, and T. Mizuno, “Comparative overviews of clock-associated genes of Arabidopsis thaliana and Oryza sativa,” Plant and Cell Physiology, vol. 48, no. 1, pp. 110–121, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. H. Tsuji, K.-I. Taoka, and K. Shimamoto, “Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation,” Current Opinion in Plant Biology, vol. 14, no. 1, pp. 45–52, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. J. A. Higgins, P. C. Bailey, and D. A. Laurie, “Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate Grasses,” PLoS ONE, vol. 5, no. 4, Article ID e10065, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Brkljacic, E. Grotewold, R. Scholl et al., “Brachypodium as a model for the grasses: today and the future,” Plant Physiology, vol. 157, no. 1, pp. 3–13, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. L. A. J. Mur, J. Allainguillaume, P. Catalán et al., “Exploiting the brachypodium tool box in cereal and grass research,” New Phytologist, vol. 191, no. 2, pp. 334–347, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Griffiths, R. P. Dunford, G. Coupland, and D. A. Laurie, “The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis,” Plant Physiology, vol. 131, no. 4, pp. 1855–1867, 2003. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Campoli, M. Shtaya, S. J. Davis, and M. von Korff, “Expression conservation within the circadian clock of a monocot: natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs,” BMC Plant Biology, vol. 12, article 97, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. J. Cockram, T. Thiel, B. Steuernagel et al., “Genome dynamics explain the evolution of flowering time CCT domain gene families in the Poaceae,” PLoS ONE, vol. 7, no. 9, Article ID e45307, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Campoli, A. Pankin, B. Drosse, C. M. Casao, S. J. Davis, and M. Von Korff, “HvLUX1 is a candidate gene underlying the early maturity 10 locus in barley: phylogeny, diversity, and interactions with the circadian clock and photoperiodic pathways,” New Phytologist, vol. 199, no. 4, pp. 1045–1059, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. S. F. Altschul, T. L. Madden, A. A. Schäffer et al., “Gapped BLAST and PSI-BLAST: a new generation of protein database search programs,” Nucleic Acids Research, vol. 25, no. 17, pp. 3389–3402, 1997. View at Publisher · View at Google Scholar · View at Scopus
  69. L. Li, C. J. Stoeckert Jr., and D. S. Roos, “OrthoMCL: identification of ortholog groups for eukaryotic genomes,” Genome Research, vol. 13, no. 9, pp. 2178–2189, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. F. Chen, A. J. Mackey, C. J. Stoeckert Jr., and D. S. Roos, “OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups,” Nucleic Acids Research, vol. 34, pp. D363–D368, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Hunter, P. Jones, A. Mitchell et al., “InterPro in 2011: new developments in the family and domain prediction database (vol 40, pg D306, 2011),” Nucleic Acids Research, vol. 40, no. 10, p. 4725, 2012. View at Google Scholar
  72. P. Jones, D. Binns, H.-Y. Chang et al., “InterProScan 5: genome-scale protein function classification,” Bioinformatics, vol. 30, no. 9, pp. 1236–1240, 2014. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Schmid, T. S. Davison, S. R. Henz et al., “A gene expression map of Arabidopsis thaliana development,” Nature Genetics, vol. 37, no. 5, pp. 501–506, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Druka, G. Muehlbauer, I. Druka et al., “An atlas of gene expression from seed to seed through barley development,” Functional & Integrative Genomics, vol. 6, no. 3, pp. 202–211, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. A. W. Schreiber, T. Sutton, R. A. Caldo et al., “Comparative transcriptomics in the Triticeae,” BMC Genomics, vol. 10, article 285, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Dash, J. Van Hemert, L. Hong, R. P. Wise, and J. A. Dickerson, “PLEXdb: gene expression resources for plants and plant pathogens,” Nucleic Acids Research, vol. 40, no. 1, pp. D1194–D1201, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. P. Lamesch, T. Z. Berardini, D. Li et al., “A gene expression map of Arabidopsis thaliana development,” Nucleic Acids Research, vol. 40, no. 1, pp. D1202–D1210, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. F. Cunningham, M. R. Amode, D. F. Cunningham et al., “Ensembl 2015,” Nucleic Acids Research, vol. 43, no. 1, pp. D662–D669, 2015. View at Publisher · View at Google Scholar · View at Scopus
  79. M. A. Larkin, G. Blackshields, N. P. Brown et al., “Clustal W and Clustal X version 2.0,” Bioinformatics, vol. 23, no. 21, pp. 2947–2948, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. A. M. Waterhouse, J. B. Procter, D. M. A. Martin, M. Clamp, and G. J. Barton, “Jalview Version 2-A multiple sequence alignment editor and analysis workbench,” Bioinformatics, vol. 25, no. 9, pp. 1189–1191, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. A. J. Drummond, M. A. Suchard, D. Xie, and A. Rambaut, “Bayesian phylogenetics with BEAUti and the BEAST 1.7,” Molecular Biology and Evolution, vol. 29, no. 8, pp. 1969–1973, 2012. View at Publisher · View at Google Scholar · View at Scopus
  82. R. C. Gentleman, V. J. Carey, D. M. Bates et al., “Bioconductor: open software development for computational biology and bioinformatics,” Genome Biology, vol. 5, R80, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. R Core Team, R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, 2014, http://www.R-project.org/.
  84. C. L. Wilson and C. J. Miller, “Simpleaffy: a BioConductor package for affymetrix quality control and data analysis,” Bioinformatics, vol. 21, no. 18, pp. 3683–3685, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. Z. Wu, R. A. Irizarry, R. Gentleman, F. Martinez-Murillo, and F. Spencer, “A model-based background adjustment for oligonucleotide expression arrays,” Journal of the American Statistical Association, vol. 99, no. 468, pp. 909–917, 2004. View at Publisher · View at Google Scholar · View at Zentralblatt MATH · View at MathSciNet · View at Scopus
  86. M. O. Winfield, C. Lu, I. D. Wilson, J. A. Coghill, and K. J. Edwards, “Cold- and light-induced changes in the transcriptome of wheat leading to phase transition from vegetative to reproductive growth,” BMC Plant Biology, vol. 9, article 55, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. N. Yamaguchi, C. M. Winter, M.-F. Wu et al., “Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis,” Science, vol. 344, no. 6184, pp. 638–641, 2014. View at Publisher · View at Google Scholar · View at Scopus
  88. E. Spanudakis and S. Jackson, “The role of microRNAs in the control of flowering time,” Journal of Experimental Botany, vol. 65, no. 2, pp. 365–380, 2014. View at Publisher · View at Google Scholar · View at Scopus
  89. L. Hategan, B. Godza, L. Kozma-Bognar, G. J. Bishop, and M. Szekeres, “Differential expression of the brassinosteroid receptor-encoding BRI1 gene in Arabidopsis,” Planta, vol. 239, no. 5, pp. 989–1001, 2014. View at Publisher · View at Google Scholar · View at Scopus
  90. A. G. Greenup, S. Sasani, S. N. Oliver et al., “ODDSOC2 is a MADS box floral repressor that is down-regulated by vernalization in temperate cereals,” Plant Physiology, vol. 153, no. 3, pp. 1062–1073, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. P. Ruelens, R. A. de Maagd, S. Proost, G. Theißen, K. Geuten, and K. Kaufmann, “FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box genes,” Nature Communications, vol. 4, article 2280, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. O. J. Ratcliffe, R. W. Kumimoto, B. J. Wong, and J. L. Riechmann, “Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold,” The Plant Cell, vol. 15, no. 5, pp. 1159–1169, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. L. Pingault, F. Choulet, A. Alberti et al., “Deep transcriptome sequencing provides new insights into the structural and functional organization of the wheat genome,” Genome Biology, vol. 16, no. 1, article 29, 2015. View at Publisher · View at Google Scholar
  94. P. Szucs, J. S. Skinner, I. Karsai et al., “Validation of the VRN-H2/VRN-H1 epistatic model in barley reveals that intron length variation in VRN-H1 may account for a continuum of vernalization sensitivity,” Molecular Genetics and Genomics, vol. 277, no. 3, pp. 249–261, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. R. Kikuchi, H. Kawahigashi, T. Ando, T. Tonooka, and H. Handa, “Molecular and functional characterization of PEBP genes in barley reveal the diversification of their roles in flowering,” Plant Physiology, vol. 149, no. 3, pp. 1341–1353, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Karlgren, N. Gyllenstrand, T. Källman et al., “Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution,” Plant Physiology, vol. 156, no. 4, pp. 1967–1977, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. T. J. Close, S. I. Wanamaker, R. A. Caldo et al., “A new resource for cereal genomics: 22K barley GeneChip comes of age,” Plant Physiology, vol. 134, no. 3, pp. 960–968, 2004. View at Publisher · View at Google Scholar · View at Scopus
  98. A. Becker and G. Theissen, “The major clades of MADS-box genes and their role in the development and evolution of flowering plants,” Molecular Phylogenetics and Evolution, vol. 29, no. 3, pp. 464–489, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. Y. Nemoto, M. Kisaka, T. Fuse, M. Yano, and Y. Ogihara, “Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice,” The Plant Journal, vol. 36, no. 1, pp. 82–93, 2003. View at Publisher · View at Google Scholar · View at Scopus
  100. B. Trevaskis, D. J. Bagnall, M. H. Ellis, W. J. Peacock, and E. S. Dennis, “MADS box genes control vernalization-induced flowering in cereals,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 22, pp. 13099–13104, 2003. View at Publisher · View at Google Scholar · View at Scopus
  101. C. Smaczniak, R. G. H. Immink, G. C. Angenent, and K. Kaufmann, “Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies,” Development, vol. 139, no. 17, pp. 3081–3098, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. C. Smaczniak, R. G. H. Immink, J. M. Muiño et al., “Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 5, pp. 1560–1565, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. S. Torti, F. Fornara, C. Vincent et al., “Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucine-rich repeat protein that promotes flowering,” The Plant Cell, vol. 24, no. 2, pp. 444–462, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. S. N. Gangappa and J. F. Botto, “The BBX family of plant transcription factors,” Trends in Plant Science, vol. 19, no. 7, pp. 460–470, 2014. View at Publisher · View at Google Scholar · View at Scopus
  105. A. G. Greenup, S. Sasani, S. N. Oliver, S. A. Walford, A. A. Millar, and B. Trevaskis, “Transcriptome analysis of the vernalization response in barley (Hordeum vulgare) seedlings,” PLoS ONE, vol. 6, no. 3, Article ID e17900, 2011. View at Publisher · View at Google Scholar · View at Scopus
  106. L. J. Leach, E. J. Belfield, C. Jiang, C. Brown, A. Mithani, and N. P. Harberd, “Patterns of homoeologous gene expression shown by RNA sequencing in hexaploid bread wheat,” BMC Genomics, vol. 15, no. 1, article 276, 2014. View at Publisher · View at Google Scholar · View at Scopus
  107. D. B. Fowler, G. Breton, A. E. Limin, S. Mahfoozi, and F. Sarhan, “Photoperiod and temperature interactions regulate low-temperature-induced gene expression in barley,” Plant Physiology, vol. 127, no. 4, pp. 1676–1681, 2001. View at Publisher · View at Google Scholar · View at Scopus
  108. M. F. Covington, J. N. Maloof, M. Straume, S. A. Kay, and S. L. Harmer, “Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development,” Genome Biology, vol. 9, no. 8, article R130, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. S. Sasani, M. N. Hemming, S. N. Oliver et al., “The influence of vernalization and daylength on expression of flowering-time genes in the shoot apex and leaves of barley (Hordeum vulgare),” Journal of Experimental Botany, vol. 60, no. 7, pp. 2169–2178, 2009. View at Publisher · View at Google Scholar · View at Scopus
  110. A. F. Stelmakh, “Genetic systems regulating flowering response in wheat (reprinted from wheat: prospects for global improvement, 1998),” Euphytica, vol. 100, no. 1–3, pp. 359–369, 1998. View at Google Scholar
  111. M. Iqbal, A. Navabi, R.-C. Yang, D. F. Salmon, and D. Spaner, “Molecular characterization of vernalization response genes in Canadian spring wheat,” Genome, vol. 50, no. 5, pp. 511–516, 2007. View at Publisher · View at Google Scholar · View at Scopus