Hd16, a gene for casein kinase I, is involved in the control of rice flowering time by modulating the day-length response

The alteration of photoperiod sensitivity has let breeders diversify flowering time in Oryza sativa (rice) and develop cultivars adjusted to a range of growing season periods. Map-based cloning revealed that the rice flowering-time quantitative trait locus (QTL) Heading date 16 (Hd16) encodes a casein kinase-I protein. One non-synonymous substitution in Hd16 resulted in decreased photoperiod sensitivity in rice, and this substitution occurred naturally in an old rice cultivar. By using near-isogenic lines with functional or deficient alleles of several rice flowering-time genes, we observed significant digenetic interactions between Hd16 and four other flowering-time genes (Ghd7, Hd1, DTH8 and Hd2). In a near-isogenic line with the weak-photoperiod-sensitivity allele of Hd16, transcription levels of Ehd1, Hd3a, and RFT1 increased under long-day conditions, and transcription levels of Hd3a and RFT1 decreased under short-day conditions. Expression analysis under continuous light and dark conditions showed that Hd16 was not likely to be associated with circadian clock regulation. Biochemical characterization indicated that the functional Hd16 recombinant protein specifically phosphorylated Ghd7. These results demonstrate that Hd16 acts as an inhibitor in the rice flowering pathway by enhancing the photoperiod response as a result of the phosphorylation of Ghd7.

[1]  D. Laurie,et al.  The Pseudo-Response Regulator Ppd-H1 Provides Adaptation to Photoperiod in Barley , 2005, Science.

[2]  C. Dean,et al.  Arabidopsis, the Rosetta stone of flowering time? , 2002, Science.

[3]  M. Yano,et al.  Adaptation of photoperiodic control pathways produces short-day flowering in rice , 2003, Nature.

[4]  M. Matsuoka,et al.  Gain of deleterious function causes an autoimmune response and Bateson–Dobzhansky–Muller incompatibility in rice , 2010, Molecular Genetics and Genomics.

[5]  C. Welcker,et al.  Analysis of photoperiod sensitivity within a collection of tropical maize populations , 2002, Genetic Resources and Crop Evolution.

[6]  M. Yano,et al.  Detection of quantitative trait loci controlling pre-harvest sprouting resistance by using backcrossed populations of japonica rice cultivars , 2010, Theoretical and Applied Genetics.

[7]  A. Graner,et al.  Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley , 2012, Proceedings of the National Academy of Sciences.

[8]  K. Asano,et al.  Isolation and characterization of dominant dwarf mutants, Slr1-d, in rice , 2009, Molecular Genetics and Genomics.

[9]  H. Xue,et al.  Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling , 2010, The EMBO journal.

[10]  A. Crilly The regulation of flowering , 1992 .

[11]  Weibo Xie,et al.  Natural variation in Ghd7.1 plays an important role in grain yield and adaptation in rice , 2013, Cell Research.

[12]  Shoichi Matsuo,et al.  Hd3a Protein Is a Mobile Flowering Signal in Rice , 2007, Science.

[13]  R. Ishikawa,et al.  Phytochrome B regulates Heading date 1 (Hd1)-mediated expression of rice florigen Hd3a and critical day length in rice , 2011, Molecular Genetics and Genomics.

[14]  Michael W Young,et al.  The Drosophila Clock Gene double-time Encodes a Protein Closely Related to Human Casein Kinase Iε , 1998, Cell.

[15]  S. D. Gross,et al.  Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family. , 1998, Cellular signalling.

[16]  Jorng-Tzong Horng,et al.  KinasePhos: a web tool for identifying protein kinase-specific phosphorylation sites , 2005, Nucleic Acids Res..

[17]  M. Yano,et al.  Variation in heading date conceals quantitative trait loci for other traits of importance in breeding selection of rice , 2012, Breeding science.

[18]  S. Kay,et al.  Photoperiodic control of flowering: not only by coincidence. , 2006, Trends in plant science.

[19]  M. Yano,et al.  Genetic interactions involved in the inhibition of heading by heading date QTL, Hd2 in rice under long-day conditions , 2011, Theoretical and Applied Genetics.

[20]  Christian Jung,et al.  Flowering time control and applications in plant breeding. , 2009, Trends in plant science.

[21]  F. Turck,et al.  CONSTANS and the CCAAT Box Binding Complex Share a Functionally Important Domain and Interact to Regulate Flowering of Arabidopsis[W][OA] , 2006, The Plant Cell Online.

[22]  M. Yano,et al.  The Role of Casein Kinase II in Flowering Time Regulation Has Diversified during Evolution1[W][OA] , 2009, Plant Physiology.

[23]  H. Sekiguchi,et al.  Mapping of QTLs conferring extremely early heading in rice (Oryza sativa L.) , 2005, Theoretical and Applied Genetics.

[24]  J. A. Traugh,et al.  Casein kinase I and II--multipotential serine protein kinases: structure, function, and regulation. , 1991, Advances in second messenger and phosphoprotein research.

[25]  K. Shimamoto,et al.  Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. , 2011, Current opinion in plant biology.

[26]  E. Tobin,et al.  The protein kinase CK2 is involved in regulation of circadian rhythms in Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[27]  T. Izawa,et al.  Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. , 2007, Journal of experimental botany.

[28]  K. Mechtler,et al.  Casein kinase 1 is required for efficient removal of Rec8 during meiosis I , 2010, Cell cycle.

[29]  Yoshinobu Takeuchi,et al.  Construction and evaluation of chromosome segment substitution lines carrying overlapping chromosome segments of indica rice cultivar 'Kasalath' in a genetic background of japonica elite cultivar 'Koshihikari' , 2005 .

[30]  E. Tobin,et al.  CK2 phosphorylation of CCA1 is necessary for its circadian oscillator function in Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Ying Xu,et al.  Functional consequences of a CKIδ mutation causing familial advanced sleep phase syndrome , 2005, Nature.

[32]  Lei Wang,et al.  Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice , 2008, Nature Genetics.

[33]  Kaworu Ebana,et al.  Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. , 2012, Plant & cell physiology.

[34]  S. Yokoi,et al.  A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice , 2009, Development.

[35]  G. Coupland,et al.  Induction of flowering by seasonal changes in photoperiod , 2004, The EMBO journal.

[36]  M. Yano,et al.  Uncovering of major genetic factors generating naturally occurring variation in heading date among Asian rice cultivars , 2011, Theoretical and Applied Genetics.

[37]  Jianmin Wan,et al.  DTH8 Suppresses Flowering in Rice, Influencing Plant Height and Yield Potential Simultaneously1[W][OA] , 2010, Plant Physiology.

[38]  Diana V. Dugas,et al.  Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum , 2011, Proceedings of the National Academy of Sciences.

[39]  M. Yano,et al.  Hd1, a Major Photoperiod Sensitivity Quantitative Trait Locus in Rice, Is Closely Related to the Arabidopsis Flowering Time Gene CONSTANS , 2000, Plant Cell.

[40]  M. Yano,et al.  A pair of floral regulators sets critical day length for Hd3a florigen expression in rice , 2010, Nature Genetics.

[41]  T. Nishio,et al.  Novel QTLs for photoperiodic flowering revealed by using reciprocal backcross inbred lines from crosses between japonica rice cultivars , 2008, Theoretical and Applied Genetics.

[42]  G. Coupland,et al.  The Molecular Basis of Diversity in the Photoperiodic Flowering Responses of Arabidopsis and Rice , 2004, Plant Physiology.

[43]  Kosuke M. Teshima,et al.  Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice , 2009, Proceedings of the National Academy of Sciences.

[44]  M. Menaker,et al.  A mutation of the circadian system in golden hamsters. , 1988, Science.

[45]  W. Liu,et al.  Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. , 2003, The Plant journal : for cell and molecular biology.

[46]  Kazuyuki Doi,et al.  Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. , 2004, Genes & development.