A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice

Although some genes that encode sensory or regulatory elements for photoperiodic flowering are conserved between the long-day (LD) plant Arabidopsis thaliana and the short-day (SD) plant rice, the gene networks that control rice flowering, and particularly flowering under LD conditions, are not well understood. We show here that RICE FLOWERING LOCUS T 1 (RFT1), the closest homolog to Heading date 3a (Hd3a), is a major floral activator under LD conditions. An RFT1:GFP fusion protein localized in the shoot apical meristem (SAM) under LD conditions, suggesting that RFT1 is a florigen gene in rice. Furthermore, mutants in OsMADS50, a rice ortholog of Arabidopsis SUPPRESOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) did not flower up to 300 days after sowing under LD conditions, indicating that OsMADS50, which acts upstream of RFT1, promotes flowering under LD conditions. We propose that both positive (OsMADS50 and Ehd1) and negative (Hd1, phyB and Ghd7) regulators of RFT1 form a gene network that regulates LD flowering in rice. Among these regulators, Ehd1, a rice-specific floral inducer, integrates multiple pathways to regulate RFT1, leading to flowering under appropriate photoperiod conditions. A rice ortholog of Arabidopsis APETALA1, OsMADS14, was expressed in the floral meristem in wild-type but not in RFT1 RNAi plants, suggesting that OsMADS14 is activated by RFT1 protein in the SAM after the transition to flowering. We have thus exposed a network of genes that regulate LD flowering in rice.

[1]  Y. Sano,et al.  Diversification in flowering time due to tandem FT‐like gene duplication, generating novel Mendelian factors in wild and cultivated rice , 2009, Molecular ecology.

[2]  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.

[3]  Y. Xuan,et al.  Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. , 2008, The Plant journal : for cell and molecular biology.

[4]  M. Yano,et al.  Ehd2, a Rice Ortholog of the Maize INDETERMINATE1 Gene, Promotes Flowering by Up-Regulating Ehd11[C][W] , 2008, Plant Physiology.

[5]  Qifa Zhang,et al.  RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice , 2008, Proceedings of the National Academy of Sciences.

[6]  Shojiro Tamaki,et al.  Florigen and the Photoperiodic Control of Flowering in Rice , 2008, Rice.

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

[8]  Shojiro Tamaki,et al.  Hd3a and RFT1 are essential for flowering in rice , 2008, Development.

[9]  Gynheung An,et al.  OsMADS51 Is a Short-Day Flowering Promoter That Functions Upstream of Ehd1, OsMADS14, and Hd3a1[W][OA] , 2007, Plant Physiology.

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

[11]  J. Mathieu,et al.  Export of FT Protein from Phloem Companion Cells Is Sufficient for Floral Induction in Arabidopsis , 2007, Current Biology.

[12]  Katja E. Jaeger,et al.  FT Protein Acts as a Long-Range Signal in Arabidopsis , 2007, Current Biology.

[13]  Fabio Fornara,et al.  FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis , 2007, Science.

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

[15]  W. J. Lucas,et al.  FLOWERING LOCUS T Protein May Act as the Long-Distance Florigenic Signal in the Cucurbits[W] , 2007, The Plant Cell Online.

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

[17]  C. Dean,et al.  The Timing of Developmental Transitions in Plants , 2006, Cell.

[18]  J. Kyozuka,et al.  Genome-wide analysis of spatial and temporal gene expression in rice panicle development. , 2006, The Plant journal : for cell and molecular biology.

[19]  C. Vincent,et al.  The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. , 2006, Genes & development.

[20]  T. Ishizuka,et al.  Distinct and Cooperative Functions of Phytochromes A, B, and C in the Control of Deetiolation and Flowering in Rice[W][OA] , 2005, The Plant Cell Online.

[21]  R. Ishikawa,et al.  Suppression of the Floral Activator Hd3a Is the Principal Cause of the Night Break Effect in Rice[W] , 2005, The Plant Cell Online.

[22]  Joonki Kim,et al.  CONSTANS Activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to Promote Flowering in Arabidopsis1[w] , 2005, Plant Physiology.

[23]  F. Chardon,et al.  Phylogenomic Analysis of the PEBP Gene Family in Cereals , 2005, Journal of Molecular Evolution.

[24]  K. Goto,et al.  FD, a bZIP Protein Mediating Signals from the Floral Pathway Integrator FT at the Shoot Apex , 2005, Science.

[25]  Wolfgang Busch,et al.  Integration of Spatial and Temporal Information During Floral Induction in Arabidopsis , 2005, Science.

[26]  K. Goto,et al.  TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. , 2005, Plant & cell physiology.

[27]  H. Maki,et al.  RNAi-mediated silencing of OsGEN-L (OsGEN-like), a new member of the RAD2/XPG nuclease family, causes male sterility by defect of microspore development in rice. , 2005, Plant & cell physiology.

[28]  R. Amasino,et al.  Integration of Flowering Signals in Winter-Annual Arabidopsis1 , 2005, Plant Physiology.

[29]  안진흥.  Functional analyses of the flowering time gene OsMADS50, the putagive SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in rice , 2004 .

[30]  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.

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

[32]  Takashi Araki,et al.  Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. , 2002, Plant & cell physiology.

[33]  M. Yano,et al.  Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. , 2002, Genes & development.

[34]  K. Shimamoto,et al.  Isolation of rice genes possibly involved in the photoperiodic control of flowering by a fluorescent differential display method. , 2002, Plant & cell physiology.

[35]  Y. Okumoto,et al.  A Novel Gene ef1‐h Conferring an Extremely Long Basic Vegetative Growth Period in Rice , 2002 .

[36]  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.

[37]  J. S. Lee,et al.  The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. , 2000, Genes & development.

[38]  Z. Schwarz‐Sommer,et al.  Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. , 2000, Science.

[39]  Claire Périlleux,et al.  Mutagenesis of Plants Overexpressing CONSTANS Demonstrates Novel Interactions among Arabidopsis Flowering-Time Genes , 2000, Plant Cell.

[40]  D. E. Somers,et al.  Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. , 1999, Science.

[41]  K. Shimamoto,et al.  Down-regulation of RFL, the FLO/LFY homolog of rice, accompanied with panicle branch initiation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  T. Komari,et al.  Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. , 1994, The Plant journal : for cell and molecular biology.

[43]  Daphne Vince-Prue,et al.  Photoperiodism in Plants , 1975 .

[44]  S. Hendricks,et al.  Photoperiodism in Plants. , 1960, Science.