Comparative biology comes into bloom: Genomic and genetic comparison of flowering pathways in rice and Arabidopsis

Current Opinion in Plant Biology

Volumn 6, Issue 2, 2003, Pages 113-120

  Izawa, Takeshi ^a   Takahashi, Yuji ^b   Yano, Masahiro ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b Institute of the Society for Techno innovation of Agriculture   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; EMBRYOPHYTA; MAGNOLIOPHYTA;

EID: 0344080487     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(03)00014-1     Document Type: Review

References (66)

1. Yu J, Hu S, Wang J, Wong GK-S, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X et al.: A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 2002, 296:79-92. This study used the whole-genome shotgun method to sequence the rice genome. The indica rice cultivar '93-11', the parent of the super-hybrid rice 'Liang-You-Pei-Jiu', was selected for this large project. In total, around 120 000 contigs were registered in the public sequence databases. The assembled sequence covers 92.0% of the genome. Free access to the database is essential to allow plant scientists to use the sequence information for the benefit of everyone.
2. Goff SA, Ricke D, Lan T-H, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H et al.: A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 2002, 296:92-100. This study also used the whole-genome shotgun method to sequence the rice genome. This project used the japonica cultivar 'Nipponbare', which is also being sequenced by the International Rice Genome Sequencing Project. The assembled sequence covers 93% of the genome. The resulting database, containing around 40 000 contigs in total, can be searched only by registration with the Torrey Mesa Research Institute.
3. Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-815.
4. Mouradov A, Cremer F, Coupland G: Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 2002 (Suppl):S111-S130.
5. Simpson GG, Dean C: Arabidopsis, the Rosetta stone of flowering time? Science 2002, 296:285-289.
6. Lin C: Photoreceptor and regulation of flowering time. Plant Physiol 2000, 123:39-50.
7. Quail PH: The phytochrome family: dissection of functional roles and signaling pathways among family members. Phil Trans R Soc Lond B 1998, 353:1399-1403.
8. Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA: Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 2000, 289:768-771.
9. Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG: Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 1999, 285:1579-1582.
10. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J: GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 1999, 18:4679-4688.
11. Hayama R, Izawa T, Shimamoto K: Isolation of rice genes possibly involved in the photoperiodic control of flowering by a differential display method. Plant Cell Physiol 2002, 43:494-504. The authors performed a fluorescent differential display using a phytochrome-deficient mutant of rice, photoperiod sensitivity5 (se5), which has no response to photoperiod. Isolated cDNAs were analyzed further by detailed mRNA expression analysis. One of the clones to be analyzed in this way was OsGl, an orthologue of Arabidopsis Gl. The expression pattern of OsGl was basically the same as that of Gl.
12. Makino S, Kiba T, Imamura A, Hanaki N, Nakamura A, Suzuki T, Taniguchi M, Uesugi C, Sugiyama T, Mizuno T: Genes encoding pseudo-response regulators: insight into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol 2000, 41:791-803.
13. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre IA, Coupland G: The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 1998, 93:1219-1229.
14. Wang ZY, Tobin EM: Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 1998, 93:1207-1217.
15. Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K: Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev 2002, 16:2006-2020. This is the first report to explain how the short-day plant rice recognizes daylength at the molecular level. The evidence presented supports the external coincidence model, one of the most popular models for photoperiodism. Daylengths other than 24 hours, such as 36 h light/12 h dark, were used to evaluate flowering-time mutants of rice.
16. Hicks KA, Albertson TM, Wagner DR: EARLY FLOWERING 3 encodes a novel protein that regulates circadian clock function and flowering in Arabidopsis. Plant Cell 2001, 13:1281-1292.
17. Doyle MR, Davis SJ, Bastow RM, McWatters HG, Kozma-Bogar L, Nagy F, Millar A, Amasino RM: The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 2002, 419:74-77. Interestingly, the elf4 mutant exhibits rhythmic gene expression that has larger deviations than that of the wild-type. This suggests an important role for ELF4 in maintaining the circadian clock. This gene could be a central component of the circadian clock.
18. Somers DE, Schultz TF, Milnamow M, Kay SA: ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 2000, 101:319-329.
19. Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B: FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 2000, 101:331-340.
20. Putterill J, Robson F, Lee K, Simon R, Coupland G: The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 1995, 80:847-857.
21. Ledger S, Strayer C, Ashton F, Kay SA, Putterill J: Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J 2001, 26:15-22.
22. Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T: Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 2000, 12:2473-2484.
23. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chow J, Harrison MJ, Weigel D: Activation tagging of the floral inducer FT. Science 1999, 286:1962-1965.
24. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T: A pair of related genes with antagonistic roles in mediating flowering signals. Science 1999, 286:1960-1962.
25. Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M: Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day condition. Plant Cell Physiol 2002, 43:1096-1105. A QTL for heading date, Hd3a, was isolated in rice by a map-based strategy. Hd3a shows a high level of similarity to the Arabidopsis flowering-time gene FT. Using expression analysis, the authors showed that the amount of Hd3a mRNA is upregulated by Hd1 under short days, suggesting that Hd3a promotes heading under the control of Hd1. This work clearly demonstrates that photoperiod-response genes are highly conserved between long- and short-day plants.
26. Onouchi H, Igeno MI, Périlleux C, Graves K, Coupland G: Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 2000, 12:885-900.
27. Kyozuka J, Konishi S, Nemoto K, Izawa T, Shimamoto K: Down-regulation of RFL, the FLO/LFY homolog of rice, accompanied with panicle branch initiation. Proc Natl Acad Sci USA 1998, 95:1979-1982.
28. Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES: The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 1999, 11:445-458.
29. Michaels SD, Amasino RM: FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 1999, 11:949-956.
30. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C: Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 2000, 290:344-347.
31. Gendall AR, Levy YY, Wilson A, Dean C: The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 2001, 107:525-535. VRN2, which is required for vernalization in Arabidopsis, encodes a protein that is homologous to Drosophila Su(z)12, Arabidopsis FERTILIZATION INDEPENDENT SEED2 (FIS2), and EMF2. These genes are members of the Polycomb group. VRN2 maintains the repression of a floral repressor, FLC, but is not involved in initiating this repression. This evidence implies that FLC expression is epigenetically regulated through chromatin remodeling.
32. Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C: Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 2002, 297:243-246.
33. Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love K, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C: FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 1997, 89:737-745.
34. Yoshida N, Yanai Y, Chen L, Kato Y, Hiratsuka J, Miwa T, Sung ZR, Takahashi S: EMBRYONIC FLOWER 2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 2001, 13:2471-2481.
35. Kinoshita T, Harada JJ, Goldberg RB, Fischer RL: Polycomb repression of flowering during early plant development. Proc Natl Acad Sci USA 2001, 98:14156-14161. Weak alleles of fie mutants were produced by expressing a fusion protein of FIE in the fie mutant. The phenotype of these mutants suggests that FIE represses flowering during the early development of Arabidopsis. FIE encodes a protein that is homologous to Drosophila Extra Sex Combs, a member of the Polycomb group.
36. Gaudin V, Libault M, Pouteau S, Juul T, Zhao G, Lefebvre D, Grandjean O: Mutations in LIKE HETEROCHROMATIN PROTEIN I affect flowering time and plant architecture in Arabidopsis. Development 2001, 128:4847-4858. This study suggests that heterochromatin formation is involved in floral induction and flower architecture in Arabidopsis. This is the first genetic evidence that heterochromatin structure is involved in biological functions in plants. LHP1 can affect the expression of CO mRNA.
37. Izawa T, Oikawa T, Tokutomi S, Okuno K, Shimamoto K: Phytochromes confer the photoperiodic control of flowering in rice, a short-day plant. Plant J 2000, 22:391-399.
38. Goto N, Kumagai T, Koornneef M: Flowering responses to night breaks in photomorphogenic mutants of Arabidopsis. Physiol Plant 1991, 83:209-215.
39. Sugiyama N, Izawa T, Oikawa T, Shimamoto K: Light regulation of circadian clock-controlled gene expression in rice. Plant J 2001, 26:607-615.
40. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G: Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 2000, 288:1613-1616.
41. Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G: CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 2001, 410:1116-1120.
42. Yanovsky MJ, Kay SA: Molecular basis of seasonal time measurement in Arabidopsis. Nature 2002, 419:308-312. This paper describes how Arabidopsis, a long-day plant, recognizes daylength at the molecular level. The Arabidopsis toc1 mutant was used for this work as genetic modification in toc1 is likely to be specific to the circadian-clock system. The authors successfully separated the effect of the circadian clock from direct light signaling. It is interesting to compare this work with that by Izawa et al. [15••], who described how rice, a short-day plant, recognizes daylength.
43. Roden LC, Song H-R, Jackson S, Morris K, Carre IA: Floral responses to photoperiod are correlated with the timing of rhythmic expression relative to dawn and dusk in Arabidopsis. Proc Natl Acad Sci USA 2002, 99:13313-13318. The authors performed extensive physiological experiments. Non-24-h light/dark cycles were used to examine the photoperiodic control of flowering in Arabidopsis. The results support the external coincidence model.
44. Bünning E: Circadian rhythms and the time measurement in photoperiodism. Cold Spring Harb Symp Quant Biol 1960, 25:249-256.
45. Pittendrigh CS, Minis DH: The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Am Nat 1964, 108:261-295.
46. Guo H, Yang H, Mockler TC, Lin C: Regulation of flowering time by Arabidopsis photoreceptors. Science 1998, 279:1360-1363.
47. Mockler TC, Guo H, Yang H, Duong H, Lin C: Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development 1999, 126:2073-2082.
48. Blazquez MA, Weigel D: Independent regulation of flowering by phytochrome B and gibberellins in Arabidopsis. Plant Physiol 1999, 120:1025-1032.
49. Takahashi Y, Shomura A, Sasaki T, Yano M: Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc Natl Acad Sci USA 1998, 98:7922-7927.
50. Sugano S, Andronis C, Ong MS, Green RM, Tobin EM: The protein kinase CK2 is involved in regulation of circadian rhythms in Arabidopsis. Proc Natl Acad Sci USA 1999, 96:12362-12366.
51. Sugano S, Andronis C, Green RM, Wang ZY, Tobin EM: Protein kinase CK2 interacts with and phosphorylates the Arabidopsis circadian clock-associated 1 protein. Proc Natl Acad Sci USA 1998, 95:11020-11025.
52. Lee Y, Lloyd AM, Roux SJ: Antisense expression of the CK2 α-subunit gene in Arabidopsis. Effects on light-regulated gene expression and plant growth. Plant Physiol 1999, 119:989-1000.
53. Yano M, Kojima S, Takahashi Y, Lin HX, Sasaki T: Genetic control of flowering time in rice, a short-day plant. Plant Physiol 2001, 127:1425-1429.
54. Jander G, Norris SR, Rounsley SD, Bish DF, Levin IM, Last RL: Arabidopsis map-based cloning in the post-genome era. Plant Physiol 2002, 129:440-450.
55. El-Assal SE, Alonso-Blanco C, Peeters AJM, Raz V, Koornneef M: A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet 2001, 29:435-440. This paper describes the map-based cloning of a QTL, EARLY DAY-LENGTH INSENSITIVE (EDI), that was detected due to allelic variation between two Arabidopsis accessions, Landsberg erecta from northern Europe and Cvi from the tropical Cape Verde Islands. EDI encodes the blue-light photoreceptor. A single amino-acid substitution in EDI gives a unique function rather than loss of function.
56. Vaughan DA: The genus Oryza L.: current status of taxonomy. IRRI Res Pap Ser 1989, 138:1-21.
57. Yano M: Genetic and molecular dissection of naturally occurring variation. Curr Opin Plant Biol 2001, 4:130-135.
58. Risch NJ: Searching for genetic determinants in the new millennium. Nature 2000, 405:847-856.
59. Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES IV: Structure of linkage disequilibrium and phenotypic association in the maize genome. Proc Natl Acad Sci USA 2001, 98:11479-11484. The authors describe local LD by analyzing six genes and genome-wide LD by analyzing 47 single-sequence-repeat loci in 102 maize inbred lines. Local LD decayed by less than 0.1 bp within 2000 bp; the decay varied among genes. A genome-wide survey showed a LD that was generally higher than that of candidate genes. The results suggest that association studies can contribute to the fine mapping of QTLs in maize.
60. Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, Hagenblad J, Kreitman M, Maloof JN, Noyes T, Oefner PJ et al.: The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 2002, 30:190-193. This paper describes a genome-wide survey of LD and develops a genome-wide LD map for Arabidopsis. Although Arabidopsis thaliana is thought to harbor extensive LD, because of the high degree of self-pollination in this species, the LD decays within approximately 1 centiMorgan (or 250 kb). This study clearly demonstrates that association study is an effective strategy for the functional analysis of Arabidopsis genes.
61. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES IV: Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 2001, 28:286-289. The authors report the first example of the use of association study for the functional identification of a plant gene. They surveyed the sequence polymorphisms of Dwarf8 in 92 maize inbred lines. Their results indicate that a particular region, which includes a key domain in the coding region, is associated with differences in flowering time.
62. Hagenblad J, Nordborg M: Sequence variation and haplotype structure surrounding the flowering time locus FRI in Arabidopsis thaliana. Genetics 2002, 161:289-298.
63. Corre VL, Roux F, Reboud X: DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Mol Biol Evol 2002, 19:1261-1271.
64. Osterberg MK, Lascoux M, Lagercrantz U: Naturally occurring indel variation in the Brassica nigra COL1 gene is associated with variation in flowering time. Genetics 2002, 161:299-306. The authors report the fine mapping of quantitative trait nucleotides (QTNs) in a candidate gene for the control of flowering time in Brassica nigra by means of association study. One indel in the COL1 coding region showed a significant association with flowering time, suggesting that the QTNs for flowering time were localized in the region of COL1. An open reading frame upstream of COL1 may play a role in controlling flowering time.
65. Lagercrantz U, Osterberg MK, Lascoux M: Sequence variation and haplotype structure at the putative flowering-time locus COL1 of Brassica nigra. Mol Biol Evol 2002, 19:1474-1482.
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