Distinct patterns of genetic variation alter flowering responses of Arabidopsis accessions to different daylengths

Plant Physiology

Volumn 152, Issue 1, 2010, Pages 177-191

  Giakountis, Antonis ^a   Cremer, Frederic ^a   Sim, Sheina ^b   Reymond, Matthieu ^a   Schmitt, Johanna ^b   Coupland, George ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 73249145459     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.109.140772     Document Type: Article

References (60)

1. Alonso-Blanco C, El-Assal SED, Coupland G, Koornneef M (1998) Analysis of natural allelic variation at flowering time loci in the Landsberg erecta and Cape Verde Islands ecotypes of Arabidopsis thaliana. Genetics 149: 749-764
2. Balasubramanian S, Sureshkumar S, Agrawal M, Michael TP, Wessinger C, Maloof JN, Clark R, Warthmann N, Chory J, Weigel D (2006) The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nat Genet 38: 711-715
3. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427: 164-167
4. Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040-1043
5. Borthwick HA, Parker MW (1939) Photoperiodic responses of several varieties of soybean. Bot Gaz 101: 341-365
6. Burn JE, Smyth DR, Peacock WJ, Dennis ES (1993) Genes conferring late flowering in Arabidopsis thaliana. Genetica 90: 147-155
7. Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD (2004) Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc Natl Acad Sci USA 101: 15670-15675
8. Chen XM, Meyerowitz EM (1999) HUA1 and HUA2 are two members of the floral homeotic AGAMOUS pathway. Mol Cell 3: 349-360
9. Clarke JH, Dean C (1994) Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol Gen Genet 242: 81-89
10. Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309: 630-633
11. Doyle MR, Bizzell CM, Keller MR, Michaels SD, Song JD, Noh YS, Amasino RM (2005) HUA2 is required for the expression of floral repressors in Arabidopsis thaliana. Plant J 41: 376-385
12. El-Assal SED, Alonso-Blanco C, Peeters AJM, Raz V, Koornneef M (2001) A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet 29: 435-440
13. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18: 4679-4688
14. Fujiwara S, Oda A, Yoshida R, Niinuma K, Miyata K, Tomozoe Y, Tajima T, Nakagawa M, Hayashi K, Coupland G, et al (2008) Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell 20: 2960-2971
15. Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 132: 1107-1114
16. Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA (2005) FKF1F-BOX protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309: 293-297
17. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347
18. Kania T, Russenberger D, Peng S, Apel K, Melzer S (1997) FPF1 promotes flowering in Arabidopsis. Plant Cell 9: 1327-1338
19. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286: 1962-1965
20. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286: 1960-1962
21. Kobayashi Y, Weigel D (2007) Move on up, it's time for change: mobile signals controlling photoperiod-dependent flowering. Genes Dev 21: 2371-2384
22. Koornneef M, Blankestijn-de Vries H, Hanhart C, Soppe W, Peeters T (1994) The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant J 6: 911-919
23. Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229: 57-66
24. Laibach F (1951) Uber sommer und winterannuelle Rasse von Arabidopsis thaliana (L.) Heynh: Ein Beitrag zur Atiologie der Blutenbildung. Beitr Biol Pflanz 28: 173-210
25. Le Corre V, Roux F, Reboud X (2002) DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Mol Biol Evol 19: 1261-1271
26. Lee I, Michaels SD, Masshardt AS, Amasino RM (1994) The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J 6: 903-909
27. Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D (2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet 1: 109-118
28. Li Y, Roycewicz P, Smith E, Borevitz JO (2006) Genetics of local adaptation in the laboratory: flowering time quantitative trait loci under geographic and seasonal conditions in Arabidopsis. PLoS One 1: e105
29. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956
30. Michaels SD, Bezerra IC, Amasino RM (2004) FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proc Natl Acad Sci USA 101: 3281-3285
31. Michaels SD, He YH, Scortecci KC, Amasino RM (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci USA 100: 10102-10107
32. Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song HR, Carre IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2: 629-641
33. Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H, Putterill J, et al (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17: 2255-2270
34. Nakamichi N, Kita M, Niinuma K, Ito S, Yamashino T, Mizoguchi T, Mizuno T (2007) Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol 48: 822-832
35. Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B (2000) FKF1, a clock- controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101: 331-340
36. Onouchi H, Igeno MI, Perilleux C, Graves K, Coupland G (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12: 885-900
37. Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG (1999) Control of circadian rhythms and photoperiodic flowering by the GIGANTEA gene. Science 285: 1579-1582
38. Pouteau S, Carre I, Gaudin V, Ferret V, Lefebvre D, Wilson M (2008) Diversification of photoperiodic response patterns in a collection of early-flowering mutants of Arabidopsis. Plant Physiol 148: 1465-1473
39. Purugganan MD, Fuller DQ (2009) The nature of selection during plant domestication. Nature 457: 843-848
40. Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80: 847-857
41. Ratcliffe OJ, Nadzan GC, Reuber TL, Riechmann JL (2001) Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol 126: 122-132
42. Ray PM, Alexander WE (1966) Photoperiodic adaptation to latitude in Xanthium strumarium. Am J Bot 53: 806-816
43. Redei GP (1962) Supervital mutants of Arabidopsis. Genetics 47: 443-460
44. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre IA, Coupland G (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93: 1219-1229
45. Scortecci KC, Michaels SD, Amasino RM (2001) Identification of a MADS- box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26: 229-236
46. Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11: 445-458
47. Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol 138: 1163-1173
48. Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci USA 101: 4712-4717
49. Suarez-Lopez 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: 1116-1120
50. Sung SB, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427: 159-164
51. Thomas B, Vince-Prue B (1997) Photoperiodism in Plants, Ed 2. Academic Press, San Diego
52. 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
53. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudoresponse regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310: 1031-1034
54. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein and the mechanism of photoperiodic flowering. Science 303: 1003-1006
55. Wang Q, Sajja U, Rosloski S, Humphrey T, Kim MC, Bomblies K, Weigel D, Grbic V (2007) HUA2 caused natural variation in shoot morphology of A. thaliana. Curr Biol 17: 1513-1519
56. Wang ZY, Tobin EM (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93: 1207-1217
57. Werner JD, Borevitz JO, Uhlenhaut NH, Ecker JR, Chory J, Weigel D (2005a) FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170: 1197-1207
58. Werner JD, Borevitz JO, Warthmann N, Trainer GT, Ecker JR, Chory J, Weigel D (2005b) Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation. Proc Natl Acad Sci USA 102: 2460-2465
59. Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, Muir CD, Sim S, Walker A, Anderson J, et al (2009) Effects of genetic perturbation on seasonal life history plasticity. Science 323: 930-934
60. Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, et al (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12: 2473-2484