HvFT1 polymorphism and effect—survey of barley germplasm and expression analysis

Frontiers in Plant Science

Volumn 5, Issue JUN, 2014, Pages

  Loscos, Jorge ^a   Igartua, Ernesto ^a   Contreras Moreir, Bruno ^a,b   Pilar Gracia, M ^a   Casas, Ana M ^a  

^a CSIC   (Spain)

^b FUNDACIÓN ARAID   (Spain)

Author keywords

Barley; Copy number variation; Flowering time; HvCEN; HvFT1

Indexed keywords

EID: 84979555753     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00251     Document Type: Article

References (68)

1. Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., et al. (2005). FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309, 1052-1056. doi: 10.1126/science.1115983
2. Ahn, J. H., Miller, D., Winter, V. J., Banfield, M. J., Lee, J. H., Yoo, S. Y., et al. (2006). A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J. 25, 605-614. doi: 10.1038/sj.emboj.7600950
3. Andrés, F., and Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639. doi: 10.1038/nrg3291
4. Baumer, M., and Cais, R. (2000). Abstammung der Gerstensorten. Freising: Bayerische Landesanstalt für Bodenkultur und Pflanzenbau.
5. Borràs-Gelonch, G., Denti, M., Thomas, W. T. B., and Romagosa, I. (2012). Genetic control of pre-heading phases in the Steptoe x Morex barley population under different conditions of photoperiod and temperature. Euphytica 183, 303-321. doi: 10.1007/s10681-011-0526-7
6. Borràs-Gelonch, G., Slafer, G. A., Casas, A. M., van Eeuwijk, F., and Romagosa, I. (2010). Genetic control of pre-heading phases and other traits related to development in a double-haploid barley (Hordeum vulgare L.) population. Field Crops Res. 119, 36-47. doi: 10.1016/j.fcr.2010.06.013
7. Boyd, W. J. R., Li, C. D., Grime, C. R., Cakir, M., Potipibool, S., Kaveeta, L., et al. (2003). Conventional and molecular genetic analysis of factors contributing to variation in the timing of heading among spring barley (Hordeum vulgare L) genotypes grown over a mild winter growing season. Aust. J. Agric. Res. 54, 1277-1301. doi: 10.1071/AR03014
8. Campoli, C., Drosse, B., Searle, I., Coupland, G., and von Korff, M. (2012). Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J. 69, 868-880. doi: 10.1111/j.1365-313X.2011.04839.x
9. Casao, M. C., Igartua, E., Karsai, I., Lasa, J. M., Gracia, M. P., and Casas, A. M. (2011). Expression analysis of vernalization and day-length response genes in barley (Hordeum vulgare L.) indicates that VRNH2 is a repressor of PPDH2 (HvFT3) under long days. J. Exp. Bot. 62, 1939-1949. doi: 10.1093/jxb/erq382
10. Casas, A. M., Djemel, A., Ciudad, F. J., Yahiaoui, S., Ponce, L. J., Contreras-Moreira, B., et al. (2011). HvFT1 (VrnH3) drives latitudinal adaptation in Spanish barleys. Theor. Appl. Genet. 122, 1293-1304. doi: 10.1007/s00122-011-1531-x
11. Chen, A., and Dubcovsky, J. (2012). Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering. PLoS Genet. 8:e1003134. doi: 10.1371/journal.pgen.1003134
12. Chiapparino, E., Donini, P., Reeves, J., Tuberosa, R., and O'Sullivan, D. M. (2006). Distribution of β-amylase I haplotypes among European cultivated barleys. Mol. Breeding 18, 341-354. doi: 10.1007/s11032-006-9035-0
13. Cockram, J., Chiapparino, E., Taylor, S., Stamati, K., Donini, P., Laurie, D., et al. (2007). Haplotype analysis of vernalization loci in European barley germplasm reveals novel VRN-H1 alleles and a predominant winter VRN-H1/VRN-H2 multi-locus haplotype. Theor. Appl. Genet. 115, 993-1001. doi: 10.1007/s00122-007-0626-x
14. Comadran, J., Kilian, B., Russell, J., Ramsay, L., Stein, N., Ganal, M., et al. (2012). Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat. Genet. 44, 1388-1392. doi: 10.1038/ng.2447
15. Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., et al. (2007). FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030-1033. doi: 10.1126/science.1141752
16. Cuesta-Marcos, A., Igartua, E., Ciudad, F. J., Codesal, P., Russell, J. R., Molina-Cano, J. L., et al. (2008). Heading date QTL in a spring x winter barley cross evaluated in Mediterranean environments. Mol. Breeding 21, 455-471. doi: 10.1007/s11032-007-9145-3
17. Cuesta-Marcos, A., Szucs, P., Close, T. J., Filichkin, T., Muehlbauer, G. J., Smith, K. P., et al. (2010). Genome-wide SNPs and re-sequencing of growth habit and inflorescence genes in barley: implications for association mapping in germplasm arrays varying in size and structure. BMC Genomics 11:707. doi: 10.1186/1471-2164-11-707
18. Díaz, A., Zikhali, M., Turner, A. S., Isaac, P., and Laurie, D. A. (2012). Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PLoS ONE 7:e33234. doi: 10.1371/journal.pone.0033234
19. Distelfeld, A., Li, C., and Dubcovsky, J. (2009). Regulation of flowering in temperate cereals. Curr. Opin. Plant Biol. 12, 178-184. doi: 10.1016/j.pbi.2008.12.010
20. Faure, S., Higgins, J., Turner, A., and Laurie, D. A. (2007). The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics 176, 599-609. doi: 10.1534/genetics.106.069500
21. Franckowiak, J. D., and Konishi, T. (1997). Stock number BGS213: spring growth habit 3. Barley Genet. Newsl. 26, 212.
22. Hayes, P. M., Liu, B. H., Knapp, S. J., Chen, F., Jones, B., Blake, T., et al. (1993). Quantitative trait locus effects and environmental interaction in a sample of North American barley germ plasm. Theor. Appl. Genet. 87, 392-401. doi: 10.1007/BF01184929
23. Hemming, M. N., Fieg, S., Peacock, W. J., Dennis, E. S., and Trevaskis, B. (2009). Regions associated with repression of the barley (Hordeum vulgare) VERNALIZATION1 gene are not required for cold induction. Mol. Genet. Genomics 282, 107-117. doi: 10.1007/s00438-009-0449-3
24. Hemming, M. N., Peacock, W. J., Dennis, E. S., and Trevaskis, B. (2008). Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol. 147, 355-366. doi: 10.1104/pp.108.116418
25. Higgins, J. A., Bailey, P. C., and Laurie, D. A. (2010). Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate grasses. PLoS ONE 5:e10065. doi: 10.1371/journal.pone.0010065
26. Himmelbach, A., Liu, L., Zierold, U., Altschmied, L., Maucher, H., Beier, F., et al. (2010). Promoters of the barley germin-like GER4 gene cluster enable strong transgene expression in response to pathogen attack. Plant Cell 22, 937-952. doi: 10.1105/tpc.109.067934
27. Hofmann, K., Silvar, C., Casas, A. M., Herz, M., Büttner, B., Gracia, M. P., et al. (2013). Fine mapping of the Rrs1 resistance locus against scald in two large populations derived from Spanish barley landraces. Theor. Appl. Genet. 126, 3091-3102. doi: 10.1007/s00122-013-2196-4
28. Igartua, E., Gracia, M. P., Lasa, J. M., Medina, B., Molina-Cano, J. L., Montoya, J. L., et al. (1998). The spanish barley core collection. Genet. Resour. Crop Evol. 45, 475-481. doi: 10.1023/A:1008662515059
29. Innan, H., and Kondrashov, F. (2010). The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11, 97-108. doi: 10.1038/nrg2689
30. Jaeger, K. E., Pullen, N., Lamzin, S., Morris, R. J., and Wigge, P. A. (2013). Interlocking feedback loops govern the dynamic behavior of the floral transition in Arabidopsis. Plant Cell 25, 820-833. doi: 10.1105/tpc.113.109355
31. Jiang, K., Liberatore, K. L., Park, S. J., Alvarez, J. P., and Lippman, Z. B. (2013). Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture. PLoS Genet. 9:e1004043. doi: 10.1371/journal.pgen.1004043
32. Karsai, I., Szucs, P., Meszaros, K., Filichkina, T., Hayes, P. M., Skinner, J. S., et al. (2005). The Vrn-H2 locus is a major determinant of flowering time in a facultative x winter growth habit barley (Hordeum vulgare L.) mapping population. Theor. Appl. Genet. 110, 1458-1466. doi: 10.1007/s00122-005-1979-7
33. Kikuchi, R., Kawahigashi, H., Ando, T., Tonooka, T., and Handa, H. (2009). Molecular and functional characterization of PEBP genes in barley reveal the diversification of their roles in flowering. Plant Physiol. 149, 1341-1353. doi: 10.1104/pp.108.132134
34. Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M., and Araki, T. (1999). A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960-1962. doi: 10.1126/science.286.5446.1960
35. Laurie, D. A. (2009). “Developmental and reproductive traits in the Triticeae,” in Genetics and Genomics of the Triticeae. Plant Genetics and Genomics: Crops and Models 7, eds C. Feuillet and G. J. Muehlbauer (Netherlands: Springer Science Business Media), 591-609. doi: 10.1007/978-0-387-77489-3_20
36. Laurie, D. A., Pratchett, N., Bezant, J. H., and Snape, J. W. (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. doi: 10.1139/g95-074
37. Li, C., Distelfeld, A., Comis, A., and Dubcovsky, J. (2011). Wheat flowering repressor VRN2 and promoter CO2 compete for interactions with NUCLEAR FACTOR-Y complexes. Plant J. 67, 763-773. doi: 10.1111/j.1365-313X.2011.04630.x
38. Li, C., and Dubcovsky, J. (2008). Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J. 55, 543-554. doi: 10.1111/j.1365-313X.2008.03526.x
39. Loukoianov, A., Yan, L., Blechl, A., Sanchez, A., and Dubcovsky, J. (2005). Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol. 138, 2364-2373. doi: 10.1104/pp.105.064287
40. Manninen, O., and Nissila, E. (1997). Genetic diversity among Finnish six-rowed barley cultivars based on pedigree information and DNA markers. Hereditas 126, 87-93. doi: 10.1111/j.1601-5223.1997.00087.x
41. Muñoz-Amatriaín, M., Eichten, S. R., Wicker, T., Richmond, T. A., Mascher, M., Steuernagel, B., et al. (2013). Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome. Genome Biol. 14, R58. doi: 10.1186/gb-2013-14-6-r58
42. Nitcher, R., Distelfeld, A., Tan, C., Yan, L., and Dubcovsky, J. (2013). Increased copy number at the HvFT1 locus is associated with accelerated flowering time in barley. Mol. Genet. Genomics 288, 261-275. doi: 10.1007/s00438-013-0746-8
43. Oliver, S. N., Finnegan, E. J., Dennis, E. S., Peacock, W. J., and Trevaskis, B. (2009). Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc. Natl. Acad. Sci. U.S.A. 106, 8386-8391. doi: 10.1073/pnas.0903566106
44. Pasquariello, M., Barabaschi, D., Himmelbach, A., Steuernagel, B., Ariyadasa, R., Stein, N., et al. (2014). The barley Frost resistance-H2 locus. Funct. Integr. Genomics 14, 85-100. doi: 10.1007/s10142-014-0360-9
45. Payne, R. W., Murray, D. A., Harding, S. A., Baird, D. B., and Soutar, D. M. (2009). GenStat for Windows, 12th Edn., Introduction. Hemel Hempstead: VSN International.
46. Piffanelli, P., Ramsay, L., Waugh, R., Benabdelmouna, A., D'Hont, A., Hollricher, K., et al. (2004). A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430, 887-891. doi: 10.1038/nature02781
47. Ponce-Molina, L. J., Casas, A. M., Gracia, M. P., Silvar, C., Mansour, E., Thomas, W. B. T., et al. (2012). Quantitative trait loci and candidate loci for heading date in a large population of a wide barley cross. Crop Sci. 52, 2469-2480. doi: 10.2135/cropsci2012.01.0029
48. Sasani, S., Hemming, M. N., Oliver, S. N., Greenup, A., Tavakkol-Afshari, R., Mahfoozi, S., et al. (2009). The influence of vernalization and daylength on expression of flowering-time genes in the shoot apex and leaves of barley (Hordeum vulgare). J. Exp. Bot. 60, 2169-2178. doi: 10.1093/jxb/erp098
49. Stracke, S., Haseneyer, G., Veyrieras, J. B., Geiger, H. H., Sauer, S., Graner, A., et al. (2009). Association mapping reveals gene action and interactions in the determination of flowering time in barley. Theor. Appl. Genet. 118, 259-273. doi: 10.1007/s00122-008-0896-y
50. Szűcs, P., Skinner, J. S., Karsai, I., Cuesta-Marcos, A., Haggard, K. G., Corey, A. E., et al. (2007). 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. Mol. Genet. Genomics 277, 249-261. doi: 10.1007/s00438-006-0195-8
51. Takahashi, R., and Yasuda, S. (1971). “Genetics of earliness and growth habit in barley,” in Barley Genetics II. Proceeding 2nd International Barley Genetics Symposium, ed R. A. Nilan (Pullman: Washington State University Press), 388-408.
52. Tamaki, S., Matsuo, S., Wong, H., Yokoi, S., and Shimamoto, K. (2007). Hd3a protein is a mobile flowering signal in rice. Science 316, 1033-1036. doi: 10.1126/science.1141753
53. Taoka, K. I., Ohki, I., Tsuji, H., Furuita, K., Hayashi, K., Yanase, T., et al. (2011). 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476, 332-335. doi: 10.1038/nature10272
54. Tiwari, S. B., Shen, Y., Chang, H.-C., Hou, Y., Harris, A., Ma, S. F., et al. (2010). The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol. 187, 57-66. doi: 10.1111/j.1469-8137.2010.03251.x
55. Trevaskis, B., Bagnall, D. J., Ellis, M. H., Peacock, W. J., and Dennis, E. S. (2003). MADS box genes control vernalization-induced flowering in cereals. Proc. Natl. Acad. Sci. U.S.A. 100, 13099-13104. doi: 10.1073/pnas.1635053100
56. Trevaskis, B., Hemming, M. N., Dennis, E. S., and Peacock, W. J. (2007). The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci. 12, 352-357. doi: 10.1016/j.tplants.2007.06.010
57. Trevaskis, B., Hemming, M. N., Peacock, W. J., and Dennis, E. S. (2006). HvVRN2 responds to day length, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol. 140, 1397-1405. doi: 10.1104/pp.105.073486
58. Turck, F., Fornara, F., and Coupland, G. (2008). Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573-594. doi: 10.1146/annurev.arplant.59.032607.092755
59. Turner, A., Beales, J., Faure, S., Dunford, R. P., and Laurie, D. A. (2005). The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310, 1031-1034. doi: 10.1126/science.1117619
60. van Harten, A. M. (1998). “Mutation breeding,” in Theory And Practical Applications, ed A. M. van Harten (Cambridge: Cambridge University Press), 353.
61. von Zitzewitz, J., Szűcs, P., Dubcovsky, J., Yan, L., Francia, E., Pecchioni, N., et al. (2005). Molecular and structural characterization of barley vernalization genes. Plant Mol. Biol. 59, 449-467. doi: 10.1007/s11103-005-0351-2
62. Weaver, S., Dube, S., Mir, A., Qin, J., Sun, G., Ramakrishnan, R., et al. (2010). Taking qPCR to a higher level: analysis of CNV reveals the power of high throughput qPCR to enhance quantitative resolution. Methods 50, 271-276. doi: 10.1016/j.ymeth.2010.01.003
63. Wigge, P. A., Kim, M. C., Jaeger, K. E., Busch, W., Schmid, M., Lohmann, J. U., et al. (2005). Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309, 1056-1059. doi: 10.1126/science.1114358
64. Yan, L., Echenique, V., Busso, C., SanMiguel, P., Ramakrishna, W., Bennetzen, J. L., et al. (2002). Cereal genes similar to Snf2 define a new subfamily that includes human and mouse genes. Mol. Genet. Genomics 268, 488-499. doi: 10.1007/s00438-002-0765-3
65. Yan, L., Fu, D., Li, C., Blechl, A., Tranquilli, G., Bonafede, M., et al. (2006). The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl. Acad. Sci. U.S.A. 103, 19851-19856. doi: 10.1073/pnas.0607142103
66. Yan, L., Loukoianov, A., Blechl, A., Tranquilli, G., Ramakrishna, W., SanMiguel, P., et al. (2004). The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303, 1640-1644. doi: 10.1126/science.1094305
67. Yan, L., Loukoianov, A., Tranquilli, G., Helguera, M., Fahima, T., and Dubcovsky, J. (2003). Positional cloning of the wheat vernalization gene VRN1. Proc. Natl. Acad. Sci. U.S.A. 100, 6263-6268. doi: 10.1073/pnas.0937399100
68. Zmieńko, A., Samelak, A., Kozłowski, P., and Figlerowicz, M. (2014). Copy number polymorphism in plant genomes. Theor. Appl. Genet. 127, 1-18. doi: 10.1007/s00122-013-2177-7