OsBBX14 delays heading date by repressing florigen gene expression under long and short-day conditions in rice

Plant Science

Volumn 247, Issue , 2016, Pages 25-34

  Bai, Bo ^a   Zhao, Jie ^a   Li, Yaping ^a,b   Zhang, Fang ^c   Zhou, Jinjun ^a   Chen, Fan ^c   Xie, Xianzhi ^a  

^a SHANDONG PEANUT RESEARCH INSTITUTE   (China)

^b SHANDONG NORMAL UNIVERSITY   (China)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

B box zinc finger protein; Circadian clock; Heading date; Photoperiod pathway; Rice

Indexed keywords

FLORIGEN; PHYTOHORMONE; PLANT PROTEIN; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

CIRCADIAN RHYTHM; DOWN REGULATION; FLOWER; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; ORYZA; PHOTOPERIODICITY; PHYSIOLOGY; PLANT LEAF; RADIATION RESPONSE; REPORTER GENE; UPREGULATION;

CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; DOWN-REGULATION; FLORIGEN; FLOWERS; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; LIGHT; ORYZA; PHOTOPERIOD; PLANT GROWTH REGULATORS; PLANT LEAVES; PLANT PROTEINS; TRANSCRIPTION FACTORS; UP-REGULATION; ZINC FINGERS;

EID: 84960193640     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2016.02.017     Document Type: Article

References (45)

1. 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, 12:2473-2483.
2. 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 conditions. Plant Cell Physiol. 2002, 43:1096-1105.
3. Hayama R., Yokoi S., Tamaki S., Yano M., Shimamoto K. Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 2003, 422:719-722.
4. Lin H., Yamamoto T., Sasaki T., Yano M. Characterization and detection of epistatic interactions of 3 QTLs, Hd1, Hd2, and Hd3 controlling heading date in rice using nearly isogenic lines. Theor. Appl. Genet. 2000, 101:1021-1028.
5. Tamaki S., Matsuo S., Wong H.L., Yokoi S., Shimamoto K. Hd3a protein is a mobile flowering signal in rice. Science 2007, 316:1033-1036.
6. Komiya R., Yokoi S., Shimamoto K. A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 2009, 136:3443-3450.
7. Komiya R., Ikegami A., Tamaki S., Yokoi S., Shimamoto K. Hd3a and RFT1 are essential for flowering in rice. Development 2008, 135:767-774.
8. Doi K., Izawa T., Fuse T., Yamanouchi U., Kubo T., Shimatani Z., Yano M., Yoshimura A. 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. 2004, 18:926-936.
9. Xue W., Xing Y., Weng X., Zhao Y., Tang W., Wang L., Zhou H., Yu S., Xu C., Li X., Zhang Q. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 2008, 40:761-767.
10. Matsubara K., Yamanouchi U., Nonoue Y., Sugimoto K., Wang Z.X., Minobe Y., Yano M. Ehd3 encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering. Plant J. 2011, 66:603-612.
11. Wei X., Xu J., Guo H., Jiang L., Chen S., Yu C., Zhou Z., Hu P., Zhai H., Wan J. DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol. 2010, 153:1747-1758.
12. Yan W., Wang P., Chen H., Zhou H., Li Q., Wang C., Ding Z., Zhang Y., Yu S., Xing Y., Zhang Q. A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol. Plant 2011, 4:319-330.
13. Park S.J., Kim S.L., Lee S., Je B.I., Piao H.L., Park S.H., Kim C.M., Ryu C.H., Park S.H., Xuan Y.H., Colasanti J., An G., Han C.D. Rice indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. Plant J. 2008, 56:1018-1029.
14. Matsubara K., Yamanouchi U., Wang Z.-X., Minobe Y., Izawa T., Yano M. Ehd2 a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiol. 2008, 148:1425-1435.
15. Wu C., You C., Li C., Long T., Chen G., Byrne M.E., Zhang Q. RID1 encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc. Natl. Acad. Sci. 2008, 105:12915-12920.
16. Kim S.L., Lee S., Kim H.J., Nam H.G., An G. OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiol. 2007, 145:1484-1494.
17. Gao H., Zheng X.-M., Fei G., Chen J., Jin M., Ren Y., Wu W., Zhou K., Sheng P., Zhou F., Jiang L., Wang J., Zhang X., Guo X., Wang J.L., Cheng Z., Wu C., Wang H., Wan J.M. Ehd4 encodes a novel and Oryza-genus-specific regulator of photoperiodic flowering in rice. PLoS Genet 2013, 9:e1003281.
18. Klug A., Schwabe J. Protein motifs 5. Zinc fingers. FASEB J. 1995, 9:597-604.
19. Khanna R., Kronmiller B., Maszle D.R., Coupland G., Holm M., Mizuno T., Wu S.-H. The Arabidopsis B-box zinc finger family. Plant Cell 2009, 21:3416-3420.
20. Datta S., Hettiarachchi C., Johansson H., Holm M. SALT TOLERANCE HOMOLOG2, a B-box protein in Arabidopsis that activates transcription and positively regulates light-mediated development. Plant Cell 2007, 19:3242-3255.
21. Datta S., Johansson H., Hettiarachchi C., Irigoyen M.L., Desai M., Rubio V., Holm M. LZF1/SALT TOLERANCE HOMOLOG3 an Arabidopsis B-box protein involved in light-dependent development and gene expression, undergoes COP1-mediated ubiquitination. Plant Cell 2008, 20:2324-2338.
22. Chang C.s.J., Li Y.H., Chen L.T., Chen W.C., Hsieh W.P., Shin J., Jane W.N., Chou S.J., Choi G., Hu J.M., Somerville S., Wu S.H. LZF1, a HY5-regulated transcriptional factor, functions in Arabidopsis de-etiolation. Plant J. 2008, 54:205-219.
23. Crocco C.D., Holm M., Yanovsky M.J., Botto J.F. AtBBX21 and COP1 genetically interact in the regulation of shade avoidance. Plant J. 2010, 64:551-562.
24. Holtan H.E., Bandong S., Marion C.M., Adam L., Tiwari S., Shen Y., Maloof J.N., Maszle D.R., Ohto M.-a., Preuss S., Meister R., Petracek M., Repetti P.P., Reuber T.L., Ratcliffe O.J., Khanna R. BBX32, an Arabidopsis B-box protein, functions in light signaling by suppressing HY5-regulated gene expression and interacting with STH2. Plant Physiol. 2011, pp. 111.177139.
25. Huang J., Zhao X., Weng X., Wang L., Xie W. The rice B-box zinc finger gene family: genomic identification, characterization, expression profiling and diurnal analysis. PLoS One 2012, 7:e48242.
26. Kim S.-K., Yun C.-H., Lee J.H., Jang Y.H., Park H.-Y., Kim J.-K. OsCO3 a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like genes under SD conditions in rice. Planta 2008, 228:355-365.
27. Griffiths S., Dunford R.P., Coupland G., Laurie D.A. The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol. 2003, 131:1855-1867.
28. Lee Y.S., Jeong D.H., Lee D.Y., Yi J., Ryu C.H., Kim S.L., Jeong H.J., Choi S.C., Jin P., Yang J., Cho L.H., Choi H., An G. OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J. 2010, 63:18-30.
29. Chen L., Hamada S., Fujiwara M., Zhu T., Thao N.P., Wong H.L., Krishna P., Ueda T., Kaku H., Shibuya N., Kawasaki T., Shimamoto K. The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host Microbe 2010, 7:185-196.
30. Jain M., Nijhawan A., Tyagi A.K., Khurana J.P. Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem. Biophys. Res. Commun. 2006, 345:646-651.
31. Li M., Li H., Hu X., Pan X., Wu G. Genetic transformation and overexpression of a rice Hd3a induces early flowering in Saussurea involucrata Kar. et Kir. ex Maxim. Plant Cell Tissue Organ Cult. (PCTOC) 2011, 106:363-371.
32. Hiei Y., Ohta S., Komari T., Kumashiro T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 1994, 6:271-282.
33. 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.
34. Robson F., Costa M.M.R., Hepworth S.R., Vizir I., Reeves P.H., Putterill J., Coupland G. Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J. 2001, 28:619-631.
35. Gangappa S.N., Botto J.F. The BBX family of plant transcription factors. Trends Plant Sci. 2014, 19:460-470.
36. Indorf M., Cordero J., Neuhaus G., Rodríguez-Franco M. Salt tolerance (STO) a stress-related protein, has a major role in light signalling. Plant J. 2007, 51:563-574.
37. Gangappa S.N., Crocco C.D., Johansson H., Datta S., Hettiarachchi C., Holm M., Botto J.F. The Arabidopsis B-BOX protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell 2013, 25:1243-1257.
38. Crocco C.D., Botto J.F. BBX proteins in green plants: insights into their evolution, structure, feature and functional diversification. Gene 2013, 531:44-52.
39. Schaffer R., Ramsay N., Samach A., Corden S., Putterill J., Carré I.A., Coupland G. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 1998, 93:1219-1229.
40. Strayer C., Oyama T., Schultz T.F., Raman R., Somers D.E., Más P., Panda S., Kreps J.A., Kay S.A. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 2000, 289:768-771.
41. Alabadí D., Oyama T., Yanovsky M.J., Harmon F.G., Más P., Kay S.A. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 2001, 293:880-883.
42. Yang Y., Peng Q., Chen G.-X., Li X.-H., Wu C.-Y. OsELF3 is involved in circadian clock regulation for promoting flowering under long-day conditions in rice. Mol. Plant 2013, 6:202-215.
43. Gao H., Jin M., Zheng X.-M., Chen J., Yuan D., Xin Y., Wang M., Huang D., Zhang Z., Zhou K., Sheng P., Ma J., Ma W., Deng H., Jiang L., Liu S., Wang H., Wu C., Yuan L., Wan J.M. Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc. Natl. Acad. Sci. 2014, 111:16337-16342.
44. Chang C.-S.J., Maloof J.N., Wu S.-H. COP1-mediated degradation of BBX22/LZF1 optimizes seedling development in Arabidopsis. Plant Physiol. 2011, 156:228-239.
45. Tiwari S.B., Shen Y., Chang H.C., Hou Y., Harris A., Ma S.F., McPartland M., Hymus G.J., Adam L., Marion C., Belachew A., Repetti P.P., Reuber T.L., Ratcliffe O.J. The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol. 2010, 187:57-66.