Increased copy number at the HvFT1 locus is associated with accelerated flowering time in barley

Molecular Genetics and Genomics

Volumn 288, Issue 5-6, 2013, Pages 261-275

  Nitcher, Rebecca ^a   Distelfeld, Assaf ^a,b   Tan, Chortee ^c   Yan, Liuling ^c   Dubcovsky, Jorge ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

^c OKLAHOMA STATE UNIVERSITY   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Barley; Flowering; FT; Hordeum vulgare; Vernalization

Indexed keywords

ALLELE; ARTICLE; BARLEY; CONTROLLED STUDY; COPY NUMBER VARIATION; EPISTASIS; FLOWERING; GENE EXPRESSION PROFILING; GENE LOCUS; HAPLOTYPE; INTRON; NONHUMAN; PLANT GROWTH; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SPRING; TRANSCRIPTION REGULATION; UPREGULATION; VERNALIZATION; WINTER;

ALLELES; DNA COPY NUMBER VARIATIONS; FLOWERS; GENE EXPRESSION REGULATION, PLANT; HAPLOTYPES; HORDEUM; TIME FACTORS;

DICOTYLEDONEAE; HORDEUM; HORDEUM VULGARE; HORDEUM VULGARE SUBSP. VULGARE; TRITICUM AESTIVUM;

EID: 84878759957     PISSN: 16174615     EISSN: 16174623     Source Type: Journal    
DOI: 10.1007/s00438-013-0746-8     Document Type: Article

References (56)

1. Adrian J, Farrona S, Reimer JJ, Albani MC, Coupland G, Turck F (2010) cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22:1425-1440
2. Campoli C, Drosse B, Searle I, Coupland G, von Korff M (2012) Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J 69:868-880
3. Casao MC, Karsai I, Igartua E, Gracia MP, Veisz O, Casas AM (2011) Adaptation of barley to mild winters: a role for PPD-H2. BMC Plant Biol 11:164
4. Casas AM, Djemel A, Ciudad FJ, Yahiaoui S, Ponce LJ, Contreras-Moreira B, Gracia MP, Lasa JM, Igartua E (2011) HvFT1 (VrnH3) drives latitudinal adaptation in Spanish barleys. Theor Appl Genet 122:1293-1304
5. Chen A, 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
6. Corbesier L, Coupland G (2005) Photoperiodic flowering of Arabidopsis: integrating genetic and physiological approaches to characterization of the floral stimulus. Plant Cell Environ 28:54-66
7. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030-1033
8. Cuesta-Marcos A, Szucs P, Close TJ, Filichkin T, Muehlbauer GJ, Smith KP, Hayes PM (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
9. Danyluk J, Kane NA, Breton G, Limin AE, Fowler DB, Sarhan F (2003) TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol 132:1849-1860
10. Díaz A, Zikhali M, Turner AS, Isaac P, Laurie DA (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
11. Distelfeld A, Tranquilli G, Li C, Yan L, Dubcovsky J (2009) Genetic and molecular characterization of the VRN2 loci in tetraploid wheat. Plant Physiol 149:245-257
12. Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316:1862-1866
13. Dubcovsky J, Chen CL, Yan LL (2005) Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Mol Breed 15:395-407
14. Faure S, Higgins J, Turner A, Laurie DA (2007) The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics 176:599-609
15. Franckowiak JD, Konishi T (1997) Barley Genetic Stock 213: spring growth habit 3. Barley Genet Newsl 26:212
16. Fu D, Szücs 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 Genomics 273:54-65
17. Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, Kahles A, Bohnert R, Jean G, Derwent P, Kersey P, Belfield EJ, Harberd NP, Kemen E, Toomajian C, Kover PX, Clark RM, Raetsch G, Mott R (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477:419-423
18. Helliwell CA, Wood CC, Robertson M, James Peacock W, Dennis ES (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J 46:183-192
19. Hemming MN, Peacock WJ, Dennis ES, Trevaskis B (2008) Low-temperature and day length cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol 147:355-366
20. Hemming MN, Fieg S, Peacock WJ, Dennis ES, 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
21. Kikuchi R, Kawahigashi H, Ando T, Tonooka T, 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
22. Knox AK, Dhillon T, Cheng H, Tondelli A, Pecchioni N, Stockinger EJ (2010) CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals. Theor Appl Genet 121:21-35
23. Li C, Dubcovsky J (2008) Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J 55:543-554
24. Li C, Distelfeld A, Comis A, Dubcovsky J (2011) Wheat flowering repressor VRN2 and promoter CO2 compete for interactions with NUCLEAR FACTOR-Y complexes. Plant J 67:763-773
25. Li Y, Xiao J, Wu J, Duan J, Liu Y, Ye X, Zhang X, Guo X, Gu Y, Zhang L, Jia J, Kong X (2012) A tandem segmental duplication (TSD) in green revolution gene Rht-D1b region underlies plant height variation. New Phytol 196:282-291
26. Loukoianov A, Yan L, Blechl A, Sanchez A, Dubcovsky J (2005) Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol 138:2364-2373
27. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321-4325
28. Oliver SN, Finnegan EJ, Dennis ES, Peacock WJ, Trevaskis B (2009) Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc Natl Acad Sci USA 106:8386-8391
29. Pan A, Hayes PM, Chen F, Chen THH, Blake T, Wright S, Karsai I, Bedo Z (1994) Genetic-analysis of the components of winterhardiness in barley (Hordeum vulgare L.). Theor Appl Genet 89:900-910
30. Ponce-Molina LJ, María Casas A, Pilar Gracia M, Silvar C, Mansour E, Thomas WBT, Schweizer G, Herz M, Igartua E (2012) Quantitative trait loci and candidate loci for heading date in a large population of a wide barley cross. Crop Sci 52:2469-2480
31. Ragupathy R, Naeem HA, Reimer E, Lukow OM, Sapirstein HD, Cloutier S (2008) Evolutionary origin of the segmental duplication encompassing the wheat GLU-B1 locus encoding the overexpressed Bx7 (Bx7OE) high molecular weight glutenin subunit. Theor Appl Genet 116:283-296
32. Read BJ, Raman H, McMichael G, Chalmers KJ, Ablett GA, Platz GJ, Raman R, Genger RK, Boyd WJR, Li CD, Grime CR, Park RF, Wallwork H, Prangnell R, Lance RCM (2003) Mapping and QTL analysis of the barley population Sloop × Halcyon. Aust J Agric Res 54:1145-1153
33. Saintenac C, Jiang D, Akhunov ED (2011) Targeted analysis of nucleotide and copy number variation by exon capture in allotetraploid wheat genome. Genome Biol 12:R88
34. Sasani S, Hemming MN, Oliver SN, Greenup A, Tavakkol-Afshari R, Mahfoozi S, Poustini K, Sharifi HR, Dennis ES, Peacock WJ, Trevaskis B (2009) The influence of vernalization and day length on expression of flowering-time genes in the shoot apex and leaves of barley (Hordeum vulgare). J Exp Bot 60:2169-2178
35. Schwartz C, Balasubramanian S, Warthmann N, Michael TP, Lempe J, Sureshkumar S, Kobayashi Y, Maloof JN, Borevitz JO, Chory J, Weigel D (2009) Cis-regulatory changes at FLOWERING LOCUS T mediate natural variation in flowering responses of Arabidopsis thaliana. Genetics 183:723-732
36. Stockinger EJ, Skinner JS, Gardner KG, Francia E, Pecchioni N (2007) Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J 51:308-321
37. Takahashi R (1983) Catalogue of the barley germplasm preserved in Okayama University. Institute of Agricultural and Biological Sciences. Okayama University, Kurashiki, p 217
38. Takahashi R, Yasuda S (1971) Genetics of earliness and growth habit in barley. In: Nilan RA (ed) Proceedings of the 2nd International Barley Genetics Symposium. Washington State University Press, Washington, pp 388-408
39. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033-1036
40. Taoka K, Ohki I, Tsuji H, Furuita K, Hayashi K, Yanase T, Yamaguchi M, Nakashima C, Purwestri YA, Tamaki S, Ogaki Y, Shimada C, Nakagawa A, Kojima C, Shimamoto K (2011) 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476:332-335
41. Tiwari SB, Shen Y, Chang H-C, Hou Y, Harris A, Ma SF, McPartland M, Hymus GJ, Adam L, Marion C, Belachew A, Repetti PP, Reuber TL, Ratcliffe OJ (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol 187:57-66
42. Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci USA 100:13099-13104
43. Trevaskis B, Hemming MN, Peacock WJ, Dennis ES (2006) HvVRN2 responds to day length, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol 140:1397-1405
44. Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352-357
45. Tsuji H, K-i Taoka, Shimamoto K (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr Opin Plant Biol 14:45-52
46. Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573-594
47. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031-1034
48. von Zitzewitz J, Szücs P, Dubcovsky J, Yan L, Francia E, Pecchioni N, Casas A, Chen TH, Hayes PM, Skinner JS (2005) Molecular and structural characterization of barley vernalization genes. Plant Mol Biol 59:449-467
49. Weaver S, Dube S, Mir A, Qin J, Sun G, Ramakrishnan R, Jones RC, Livak KJ (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
50. Wicker T, Mayer KF, Gundlach H, Martis M, Steuernagel B, Scholz U, Šimková H, Kubaláková M, Choulet F, Taudien S, Platzer M, Feuillet C, Fahima T, Budak H, Doležel J, Keller B, Stein N (2011) Frequent gene movement and pseudogene evolution is common to the large and complex genomes of wheat, barley, and their relatives. Plant Cell 23:1706-1718
51. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056-1059
52. Yan L, Echenique V, Busso C, SanMiguel P, Ramakrishna W, Bennetzen JL, Harrington S, Dubcovsky J (2002) Cereal genes similar to Snf2 define a new subfamily that includes human and mouse genes. Mol Genet Genomics 268:488-499
53. 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 100:6263-6268
54. Yan L, 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 303:1640-1644
55. Yan L, von Zitzewitz J, Skinner JS, Hayes PM, Dubcovsky J (2005) Molecular characterization of the duplicated meristem identity genes HvAP1a and HvAP1b in barley. Genome 48:905-912
56. 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 103:19581-19586