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      KCI등재 SCOPUS SCIE

      Casein kinases I and 2α phosphorylate oryza sativa pseudo-response regulator 37 (OsPRR37) in photoperiodic flowering in rice

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      https://www.riss.kr/link?id=A103928127

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      다국어 초록 (Multilingual Abstract)

      Flowering time (or heading date) is controlled by intrinsic genetic programs in response to environmental cues, such as photoperiod and temperature. Rice, a facultative short-day (SD) plant, flowers early in SD and late in long-day (LD) conditions. Casein kinases (CKs) generally act as positive regulators in many signaling pathways in plants. In rice, Heading date 6 (Hd6) and Hd16 encode CK2α and CKI, respectively, and mainly function to delay flowering time. Additionally, the major LD-dependent floral repressors Hd2/Oryza sativa Pseudo-Response Regulator 37 (OsPRR37; hereafter PRR37) and Ghd7 also confer strong photoperiod sensitivity. In floral induction, Hd16 acts upstream of Ghd7 and CKI interacts with and phosphorylates Ghd7. In addition, Hd6 and Hd16 also act upstream of Hd2. However, whether CKI and CK2α directly regulate the function of PRR37 remains unclear. Here, we use in vitro pull-down and in vivo bimolecular fluorescence complementation assays to show that CKI and CK2α interact with PRR37. We further use in vitro kinase assays to show that CKI and CK2α phosphorylate different regions of PRR37. Our results indicate that direct posttranslational modification of PRR37 mediates the genetic interactions between these two protein kinases and PRR37. The significance of CK-mediated phosphorylation for PRR37 and Ghd7 function is discussed.
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      Flowering time (or heading date) is controlled by intrinsic genetic programs in response to environmental cues, such as photoperiod and temperature. Rice, a facultative short-day (SD) plant, flowers early in SD and late in long-day (LD) conditions. Ca...

      Flowering time (or heading date) is controlled by intrinsic genetic programs in response to environmental cues, such as photoperiod and temperature. Rice, a facultative short-day (SD) plant, flowers early in SD and late in long-day (LD) conditions. Casein kinases (CKs) generally act as positive regulators in many signaling pathways in plants. In rice, Heading date 6 (Hd6) and Hd16 encode CK2α and CKI, respectively, and mainly function to delay flowering time. Additionally, the major LD-dependent floral repressors Hd2/Oryza sativa Pseudo-Response Regulator 37 (OsPRR37; hereafter PRR37) and Ghd7 also confer strong photoperiod sensitivity. In floral induction, Hd16 acts upstream of Ghd7 and CKI interacts with and phosphorylates Ghd7. In addition, Hd6 and Hd16 also act upstream of Hd2. However, whether CKI and CK2α directly regulate the function of PRR37 remains unclear. Here, we use in vitro pull-down and in vivo bimolecular fluorescence complementation assays to show that CKI and CK2α interact with PRR37. We further use in vitro kinase assays to show that CKI and CK2α phosphorylate different regions of PRR37. Our results indicate that direct posttranslational modification of PRR37 mediates the genetic interactions between these two protein kinases and PRR37. The significance of CK-mediated phosphorylation for PRR37 and Ghd7 function is discussed.

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      참고문헌 (Reference)

      1 Ogiso, E., "The role of Casein Kinase II in Flowering Time Regulation Has Diversified during Evolution" 152 : 808-820, 2010

      2 Turner, A., "The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley" 310 : 1031-1034, 2005

      3 Portoles, S., "The functional interplay between protein kinase CK2 and CCA1 transcriptional activity is essential for clock temperature compensation in Arabidopsis" 6 : 1001201-, 2010

      4 Knippschild, U., "The casein kinase 1 family : participation in multiple cellular processes in eukaryotes" 17 : 675-689, 2005

      5 Nusinow, D. A., "The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature, 475" 475 : 398-U161-, 2011

      6 Citovsky, V., "Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta" 362 : 1120-1131, 2006

      7 윤지현, "Structural and Functional Characterization of Arabidopsis GSK3-like Kinase AtSK12" 한국분자세포생물학회 36 (36): 564-570, 2013

      8 Fujino, K., "Roles of the Hd5gene controlling heading date for adaptation to the northern limits of rice cultivation" 126 : 611-618, 2013

      9 Park, S. J., "Rice indeterminate 1(OsId1)is necessary for the expression of Ehd1(Early heading date 1)regardless of photoperiod" 56 : 1018-1029, 2008

      10 Dai, C., "Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling" 29 : 1916-1927, 2010

      1 Ogiso, E., "The role of Casein Kinase II in Flowering Time Regulation Has Diversified during Evolution" 152 : 808-820, 2010

      2 Turner, A., "The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley" 310 : 1031-1034, 2005

      3 Portoles, S., "The functional interplay between protein kinase CK2 and CCA1 transcriptional activity is essential for clock temperature compensation in Arabidopsis" 6 : 1001201-, 2010

      4 Knippschild, U., "The casein kinase 1 family : participation in multiple cellular processes in eukaryotes" 17 : 675-689, 2005

      5 Nusinow, D. A., "The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature, 475" 475 : 398-U161-, 2011

      6 Citovsky, V., "Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta" 362 : 1120-1131, 2006

      7 윤지현, "Structural and Functional Characterization of Arabidopsis GSK3-like Kinase AtSK12" 한국분자세포생물학회 36 (36): 564-570, 2013

      8 Fujino, K., "Roles of the Hd5gene controlling heading date for adaptation to the northern limits of rice cultivation" 126 : 611-618, 2013

      9 Park, S. J., "Rice indeterminate 1(OsId1)is necessary for the expression of Ehd1(Early heading date 1)regardless of photoperiod" 56 : 1018-1029, 2008

      10 Dai, C., "Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling" 29 : 1916-1927, 2010

      11 강창호, "Rice Small C2-Domain Proteins Are Phosphorylated by Calcium-Dependent Protein Kinase" 한국분자세포생물학회 35 (35): 381-387, 2013

      12 Alabadi, D., "Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock" 293 : 880-883, 2001

      13 Wu, C. Y., "RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice" 105 : 12915-12920, 2008

      14 Sugano, S., "Protein kinase CK2 interacts with and phosphorylates the Arabidopsis circadian clock-associated 1 protein" 95 : 11020-11025, 1998

      15 Fujiwara, S., "Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins" 283 : 23073-23083, 2008

      16 Nakamichi, N., "PSEUDO-RESPONSE REGULATORS, PRR9, PRR7and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana" 46 : 686-698, 2005

      17 Salome, P. A., "PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock" 17 : 791-803, 2005

      18 Farre, E. M., "PRR7 protein levels are regulated by light and the circadian clock in Arabidopsis" 52 : 548-560, 2007

      19 Wang, L., "PRR5 regulates phosphorylation, nuclear import and subnuclear localization of TOC1 in the Arabidopsis circadian clock" 29 : 1903-1915, 2010

      20 Zhao, J. M., "OsELF3-1, an ortholog of Arabidopsis EARLY FLOWERING 3, regulates rice circadian rhythm and photoperiodic flowering" 7 : 43705-, 2012

      21 Yang, Y., "OsELF3 is involved in circadian clock regulation for promoting flowering under long-day conditions in rice" 6 : 202-215, 2013

      22 Matsubara, K., "Novel QTLs for photoperiodic flowering revealed by using reciprocal backcross inbred lines from crosses between japonica rice cultivars" 117 : 935-945, 2008

      23 Kwon, C. T., "Natural variation in early flowering1 contributes to early flowering in japonica rice under long days" 37 : 101-112, 2014

      24 Koo, B. H., "Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes" 6 : 1877-1888, 2013

      25 Matsubara, K., "Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering" 53 : 709-716, 2012

      26 Yan, W. H., "Natural variation in Ghd7. 1 plays an important role in grain yield and adaptation in rice" 23 : 969-971, 2013

      27 Xue, W. Y., "Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice" 40 : 761-767, 2008

      28 Fujino, K., "Mapping of QTLs conferring extremely early heading in rice(Oryza sativa L. )" 111 : 393-398, 2005

      29 Yamamoto, T., "Identification of heading date quantitative trait locus Hd6 and characterization of its epistatic interactions with Hd2 in rice using advanced backcross progeny" 154 : 885-891, 2000

      30 Takahashi, Y., "Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2" 98 : 7922-7927, 2001

      31 Komiya, R., "Hd3a and RFT1 are essential for flowering in rice" 135 : 767-774, 2008

      32 Hori, K., "Hd16, a gene for casein kinase I, is involved in the control of rice flowering time by modulating the day-length response" 76 : 36-46, 2013

      33 Yano, M., "Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the arabidopsis flowering time gene CONSTANS" 12 : 2473-2483, 2000

      34 Shibaya, T., "Genetic interactions involved in the inhibition of heading by heading date QTL, Hd2 in rice under long-day conditions" 123 : 1133-1143, 2011

      35 Wei, X. J., "Genetic analyses of heading date of Japonica rice cultivars from Northeast China" 107 : 147-154, 2008

      36 Huq, E., "GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis" 97 : 9789-9794, 2000

      37 Tsuji, H., "Florigen and the photoperiodic control of flowering in rice" 1 : 25-35, 2008

      38 Corbesier, L., "FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis" 316 : 1030-1033, 2007

      39 Sawa, M., "FKF1and GIGANTEA complex formation is required for day-length measurement in Arabidopsis" 318 : 261-265, 2007

      40 Song, Y. H., "FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering" 336 : 1045-1049, 2012

      41 Abe, M., "FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex" 309 : 1052-1056, 2005

      42 Mulekar, J. J., "Expanding roles of protein kinase CK2 in regulating plant growth and development" 65 : 2883-2893, 2014

      43 Gao, H., "Ehd4Encodes a Novel and Oryza-Genus-Specific Regulator of Photoperiodic Flowering in Rice" 9 : 1003281-, 2013

      44 Matsubara, K., "Ehd3, encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering" 66 : 603-612, 2011

      45 Matsubara, K., "Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1" 148 : 1425-1435, 2008

      46 Doi, K., "Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-Iike gene expression independently of Hd1" 18 : 926-936, 2004

      47 Saito, H., "Ef7 encodes an ELF3-like protein and promotes rice flowering by negatively regulating the floral repressor gene Ghd7 under both short-and long-day conditions" 53 : 717-728, 2012

      48 Herrero, E., "EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock" 24 : 428-443, 2012

      49 Nonoue, Y., "Detection of quantitative trait loci controlling extremely early heading in rice" 116 : 715-722, 2008

      50 Wei, X. J., "DTH8suppresses flowering in rice, influencing plant height and yield potential simultaneously" 153 : 1747-1758, 2010

      51 Park, D. H., "Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene" 285 : 1579-1582, 1999

      52 Yamamoto, Y., "Comparative genetic studies on the APRR5 and APRR7genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering time, and early photomorphogenesis" 44 : 1119-1130, 2003

      53 Murphy, R. L., "Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum" 108 : 16469-16474, 2011

      54 Murakami, M., "Circadian-associated rice pseudo response regulators(OsPRRs) : Insight into the control of flowering time" 69 : 410-414, 2005

      55 Matsushika, A., "Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana : Insight into the plant circadian clock" 41 : 1002-1012, 2000

      56 Murakami, M., "Characterization of the rice circadian clock-associated pseudoresponse regulators in Arabidopsis thaliana" 71 : 1107-1110, 2007

      57 Lin, H. X., "Characterization and detection of epistatic interactions of 3QTLs, Hd1, Hd2, and Hd3, controlling heading date in rice using nearly isogenic lines" 101 : 1021-1028, 2000

      58 Yu, J. W., "COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability" 32 : 617-630, 2008

      59 Daniel, X., "CK2 phosphorylation of CCA1 is necessary for its circadian oscillator function in Arabidopsis" 101 : 3292-3297, 2004

      60 Wu, W. X., "Association of functional nucleotide polymorphisms at DTH2with the northward expansion of rice cultivation in Asia" 110 : 2775-2780, 2013

      61 Nakamichi, N., "Arabidopsis clockassociated pseudo-response regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway" 48 : 822-832, 2007

      62 Tan, S. T., "Arabidopsis casein kinase1 proteins CK1. 3 and CK1. 4 phosphorylate cryptochrome2 to regulate blue light signaling" 25 : 2618-2632, 2013

      63 Kaczorowski, K. A., "Arabidopsis PSEUDORESPONSE REGULATOR7 is a signaling intermediate in phytochrome-regulated seedling deetiolation and phasing of the circadian clock" 15 : 2654-2665, 2003

      64 Kim, S. L., "Analysis of the early-flowering mechanisms and generation of T-DNA tagging lines in Kitaake, a model rice cultivar" 64 : 4169-4182, 2013

      65 Hayama, R., "Adaptation of photoperiodic control pathways produces short-day flowering in rice" 422 : 719-722, 2003

      66 Izawa, T., "Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice" 58 : 3091-3097, 2007

      67 Kardailsky, I., "Activation tagging of the floral inducer FT" 286 : 1962-1965, 1999

      68 Lu, S. X., "A role for protein kinase casein kinase2 alphasubunits in the Arabidopsis circadian clock" 157 : 1537-1545, 2011

      69 Beales, J., "A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat(Triticum aestivum L. )" 115 : 721-733, 2007

      70 Kobayashi, Y., "A pair of related genes with antagonistic roles in mediating flowering signals" 286 : 1960-1962, 1999

      71 Yan, W. H., "A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice" 4 : 319-330, 2011

      72 Ito, S., "A genetic study of the Arabidopsis circadian clock with reference to the TIMING OF CAB EXPRESSION 1(TOC1)Gene" 50 : 290-303, 2009

      73 Komiya, R., "A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice" 136 : 3443-3450, 2009

      74 Taoka, K., "14-3-3 proteins act as intracellular receptors for rice Hd3a florigen" 476 : 332-397, 2011

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