Encodes a Novel and -Genus-Specific Regulator of Photoperiodic Flowering in Rice

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Land plants have evolved increasingly complex regulatory modes of their flowering time (or heading date in crops). Rice (Oryza sativa L.) is a short-day plant that flowers more rapidly in short-day but delays under long-day conditions. Previous studies have shown that the CO-FT module initially identified in long-day plants (Arabidopsis) is evolutionary conserved in short-day plants (Hd1-Hd3a in rice). However, in rice, there is a unique Ehd1-dependent flowering pathway that is Hd1-independent. Here, we report isolation and characterization of a positive regulator of Ehd1, Early heading date 4 (Ehd4). ehd4 mutants showed a never flowering phenotype under natural long-day conditions. Map-based cloning revealed that Ehd4 encodes a novel CCCH-type zinc finger protein, which is localized to the nucleus and is able to bind to nucleic acids in vitro and transactivate transcription in yeast, suggesting that it likely functions as a transcriptional regulator. Ehd4 expression is most active in young leaves with a diurnal expression pattern similar to that of Ehd1 under both short-day and long-day conditions. We show that Ehd4 up-regulates the expression of the “florigen” genes Hd3a and RFT1 through Ehd1, but it acts independently of other known Ehd1 regulators. Strikingly, Ehd4 is highly conserved in the Oryza genus including wild and cultivated rice, but has no homologs in other species, suggesting that Ehd4 is originated along with the diversification of the Oryza genus from the grass family during evolution. We conclude that Ehd4 is a novel Oryza-genus-specific regulator of Ehd1, and it plays an essential role in photoperiodic control of flowering time in rice.

Vyšlo v časopise: Encodes a Novel and -Genus-Specific Regulator of Photoperiodic Flowering in Rice. PLoS Genet 9(2): e32767. doi:10.1371/journal.pgen.1003281
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003281

Souhrn

Zdroje

1. SimpsonGG, DeanC (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296: 285–289.

2. IzawaT (2007) Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J Exp Bot 58: 3091–3097.

3. SrikanthA, SchmidM (2011) Regulation of flowering time: all roads lead to Rome. Cellular and Molecular Life Sciences 68: 2013–2037.

4. KobayashiY, WeigelD (2007) Move on up, it's time for change–mobile signals controlling photoperiod-dependent flowering. Genes Dev 21: 2371–2384.

5. ImaizumiT, KaySA (2006) Photoperiodic control of flowering: not only by coincidence. Trends in plant science 11: 550–558.

6. TurckF, FornaraF, CouplandG (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59: 573–594.

7. YanovskyMJ, KaySA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419: 308–312.

8. ValverdeF, MouradovA, SoppeW, RavenscroftD, SamachA, et al. (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science Signalling 303: 1003.

9. SawaM, NusinowDA, KaySA, ImaizumiT (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science Signalling 318: 261.

10. FornaraF, PanigrahiK, GissotL, SauerbrunnN, RühlM, et al. (2009) Arabidopsis DOF Transcription Factors Act Redundantly to Reduce CONSTANS Expression and Are Essential for a Photoperiodic Flowering Response. Developmental cell 17: 75–86.

11. PutterillJ, RobsonF, LeeK, SimonR, CouplandG (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80: 847–857.

12. TiwariSB, ShenY, ChangHC, HouY, HarrisA, et al. (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis‐element. New Phytologist 187: 57–66.

13. AbeM, KobayashiY, YamamotoS, DaimonY, YamaguchiA, et al. (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science Signalling 309: 1052.

14. WiggePA, KimMC, JaegerKE, BuschW, SchmidM, et al. (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science Signalling 309: 1056.

15. CorbesierL, VincentC, JangS, FornaraF, FanQ, et al. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science Signalling 316: 1030.

16. TAKIMOTOA, IKEDAK (1961) Effect of twilight on photoperiodic induction in some short day plants. Plant and Cell Physiology 2: 213–229.

17. ItohH, NonoueY, YanoM, IzawaT (2010) A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nature genetics 42: 635–638.

18. HayamaR, YokoiS, TamakiS, YanoM, ShimamotoK (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422: 719–722.

19. YanoM, KatayoseY, AshikariM, YamanouchiU, MonnaL, et al. (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. The Plant Cell Online 12: 2473–2483.

20. KojimaS, TakahashiY, KobayashiY, MonnaL, SasakiT, et al. (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant and Cell Physiology 43: 1096–1105.

21. TamakiS, MatsuoS, WongHL, YokoiS, ShimamotoK (2007) Hd3a protein is a mobile flowering signal in rice. Science Signalling 316: 1033.

22. KomiyaR, IkegamiA, TamakiS, YokoiS, ShimamotoK (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135: 767–774.

23. TakahashiY, TeshimaKM, YokoiS, InnanH, ShimamotoK (2009) Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proceedings of the National Academy of Sciences 106: 4555–4560.

24. DoiK, IzawaT, FuseT, YamanouchiU, KuboT, et al. (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18: 926–936.

25. KomiyaR, YokoiS, ShimamotoK (2009) A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136: 3443–3450.

26. LeeYS, JeongDH, LeeDY, YiJ, RyuCH, et al. (2010) OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. The Plant Journal 63: 18–30.

27. IzawaT, OikawaT, SugiyamaN, TanisakaT, YanoM, et al. (2002) Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev 16: 2006–2020.

28. XueW, XingY, WengX, ZhaoY, TangW, et al. (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature genetics 40: 761–767.

29. WeiX, XuJ, GuoH, JiangL, ChenS, et al. (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiology 153: 1747–1758.

30. KimSL, LeeS, KimHJ, NamHG, AnG (2007) OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiology 145: 1484–1494.

31. LeeS, KimJ, HanJJ, HanMJ, AnG (2004) Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS‐LIKE 20 (SOC1/AGL20) ortholog in rice. The Plant Journal 38: 754–764.

32. WuC, YouC, LiC, LongT, ChenG, et al. (2008) RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proceedings of the National Academy of Sciences 105: 12915–12920.

33. ParkSJ, KimSL, LeeS, JeBI, PiaoHL, et al. (2008) Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. The Plant Journal 56: 1018–1029.

34. MatsubaraK, YamanouchiU, WangZX, MinobeY, IzawaT, et al. (2008) Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiology 148: 1425–1435.

35. ColasantiJ, YuanZ, SundaresanV (1998) The indeterminate Gene Encodes a Zinc Finger Protein and Regulates a Leaf-Generated Signal Required for the Transition to Flowering in Maize. Cell 93: 593–603.

36. MatsubaraK, YamanouchiU, NonoueY, SugimotoK, WangZX, et al. (2011) Ehd3, encoding a plant homeodomain finger‐containing protein, is a critical promoter of rice flowering. The Plant Journal 66: 603–612.

37. TakahashiY, ShomuraA, SasakiT, YanoM (2001) Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the α subunit of protein kinase CK2. Proceedings of the National Academy of Sciences 98: 7922–7927.

38. OgisoE, TakahashiY, SasakiT, YanoM, IzawaT (2010) The role of casein kinase II in flowering time regulation has diversified during evolution. Plant Physiology 152: 808–820.

39. YuJ, HuS, WangJ, WongGKS, LiS, et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 79–92.

40. LiJ, JiaD, ChenX (2001) HUA1, a regulator of stamen and carpel identities in Arabidopsis, codes for a nuclear RNA binding protein. The Plant Cell Online 13: 2269–2281.

41. KimDH, YamaguchiS, LimS, OhE, ParkJ, et al. (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. The Plant Cell Online 20: 1260–1277.

42. HurtJA, ObarRA, ZhaiB, FarnyNG, GygiSP, et al. (2009) A conserved CCCH-type zinc finger protein regulates mRNA nuclear adenylation and export. The Journal of Cell Biology 185: 265–277.

43. LinR, DingL, CasolaC, RipollDR, FeschotteC, et al. (2007) Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science Signalling 318: 1302.

44. LiuH, YuX, LiK, KlejnotJ, YangH, et al. (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science Signalling 322: 1535.

45. PengLT, ShiZY, LiL, ShenGZ, ZhangJL (2007) Ectopic expression of OsLFL1 in rice represses Ehd1 by binding on its promoter. Biochemical and biophysical research communications 360: 251–256.

46. SeayD, HookB, EvansK, WickensM (2006) A three-hybrid screen identifies mRNAs controlled by a regulatory protein. Rna 12: 1594–1600.

47. ChinL, HahnWC, GetzG, MeyersonM (2011) Making sense of cancer genomic data. Genes Dev 25: 534–555.

48. GarrisAJ, TaiTH, CoburnJ, KresovichS, McCOUCHS (2005) Genetic structure and diversity in Oryza sativa L. Genetics. 169: 1631–1638.

49. ZhuQ, ZhengX, LuoJ, GautBS, GeS (2007) Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Molecular Biology and Evolution 24: 875–888.

50. RyuCH, LeeS, ChoLH, KimSL, LeeYS, et al. (2009) OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant Cell and Environment 32: 1412–1427.

51. BergJM, ShiY (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271: 1081–1085.

52. WangD, GuoY, WuC, YangG, LiY, et al. (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genomics 9: 44.

53. Vaughan D. Collection, conservation, and potential use of the wild relatives of rice in Asia and Australia; 1989. IRRI.

54. LondoJP, ChiangYC, HungKH, ChiangTY, SchaalBA (2006) Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc Natl Acad Sci U S A 103: 9578–9583.

55. BartR, ChernM, ParkCJ, BartleyL, RonaldPC (2006) A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods 2: 13.

56. HuangXY, ChaoDY, GaoJP, ZhuMZ, ShiM, et al. (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23: 1805–1817.