Crosstalk between Cold Response and Flowering in Arabidopsis Is Mediated through the Flowering-Time Gene SOC1 and Its Upstream Negative Regulator FLC

The appropriate timing of flowering is pivotal for reproductive success in plants; thus, it is not surprising that flowering is regulated by complex genetic networks that are fine-tuned by endogenous signals and environmental cues. The Arabidopsis thaliana flowering-time gene SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1) encodes a MADS box transcription factor and is one of the key floral activators integrating multiple floral inductive pathways, namely, long-day, vernalization, autonomous, and gibberellin-dependent pathways. To elucidate the downstream targets of SOC1, microarray analyses were performed. The analysis revealed that the soc1-2 knockout mutant has increased, and an SOC1 overexpression line has decreased, expression of cold response genes such as CBFs (for CRT/DRE binding factors) and COR (for cold regulated) genes, suggesting that SOC1 negatively regulates the expression of the cold response genes. By contrast, overexpression of cold-inducible CBFs caused late flowering through increased expression of FLOWERING LOCUS C (FLC), an upstream negative regulator of SOC1. Our results demonstrate the presence of a feedback loop between cold response and flowering-time regulation; this loop delays flowering through the increase of FLC when a cold spell is transient as in fall or early spring but suppresses the cold response when floral induction occurs through the repression of cold-inducible genes by SOC1.

[1]  J. A. Jarillo,et al.  Regulation of flowering time by FVE, a retinoblastoma-associated protein , 2004, Nature Genetics.

[2]  Y. Liou,et al.  Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis , 2008, Development.

[3]  S. Park,et al.  Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. , 2007, Genes & development.

[4]  R. Mittler,et al.  The Zinc Finger Protein Zat12 Is Required for Cytosolic Ascorbate Peroxidase 1 Expression during Oxidative Stress in Arabidopsis*[boxs] , 2004, Journal of Biological Chemistry.

[5]  D. Weigel,et al.  Potent Induction of Arabidopsis thaliana Flowering by Elevated Growth Temperature , 2006, PLoS genetics.

[6]  S. J. Gilmour,et al.  Cold signalling associated with vernalization in Arabidopsis thaliana does not involve CBF1 or abscisic acid. , 2002, Physiologia plantarum.

[7]  K. Halliday,et al.  Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. , 2003, The Plant journal : for cell and molecular biology.

[8]  Ilha Lee,et al.  A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana , 2004, Nature Genetics.

[9]  M. Ishitani,et al.  The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo--cytoplasmic partitioning. , 2001, Genes & development.

[10]  D. Weigel,et al.  Floral determination and expression of floral regulatory genes in Arabidopsis. , 1997, Development.

[11]  S. J. Gilmour,et al.  Arabidopsis Transcriptional Activators CBF1, CBF2, and CBF3 have Matching Functional Activities , 2004, Plant Molecular Biology.

[12]  R. Simon,et al.  The CONSTANS gene of arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors , 1995, Cell.

[13]  R. Amasino,et al.  Regulation of Flowering Time by Histone Acetylation in Arabidopsis , 2003, Science.

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

[15]  Ilha Lee,et al.  SUPPRESSOR OF FRIGIDA4, Encoding a C2H2-Type Zinc Finger Protein, Represses Flowering by Transcriptional Activation of Arabidopsis FLOWERING LOCUS C[W] , 2006, The Plant Cell Online.

[16]  M. Thomashow,et al.  Arabidopsis Transcriptome Profiling Indicates That Multiple Regulatory Pathways Are Activated during Cold Acclimation in Addition to the CBF Cold Response Pathway Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1 , 2002, The Plant Cell Online.

[17]  Minsoo Kim,et al.  Analysis of flowering pathway integrators in Arabidopsis. , 2005, Plant & cell physiology.

[18]  Ilha Lee,et al.  SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. , 2008, The Plant journal : for cell and molecular biology.

[19]  D. Weigel,et al.  A thermosensory pathway controlling flowering time in Arabidopsis thaliana , 2003, Nature Genetics.

[20]  S. Kay,et al.  Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. , 2000, Science.

[21]  Jianhua Zhu,et al.  Cold stress regulation of gene expression in plants. , 2007, Trends in plant science.

[22]  R. Amasino,et al.  Vernalization and epigenetics: how plants remember winter. , 2004, Current opinion in plant biology.

[23]  G. Whitelam,et al.  Light-quality regulation of freezing tolerance in Arabidopsis thaliana , 2007, Nature Genetics.

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

[25]  Stephen J. Powers,et al.  Real-Time Quantitative RT-PCR: Design, Calculations, and Statistics , 2009, The Plant Cell Online.

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

[27]  P. Huijser,et al.  Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. , 2000, The Plant journal : for cell and molecular biology.

[28]  G. Coupland,et al.  GIGANTEA: a circadian clock‐controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane‐spanning domains , 1999, The EMBO journal.

[29]  E. Wisman,et al.  A MADS domain gene involved in the transition to flowering in Arabidopsis. , 2000, The Plant journal : for cell and molecular biology.

[30]  C. Lister,et al.  Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN 3 , 2022 .

[31]  10,et al.  Direct interaction of AGL 24 and SOC 1 integrates flowering signals in Arabidopsis , 2022 .

[32]  Lisha Shen,et al.  Regulation of floral patterning by flowering time genes. , 2009, Developmental cell.

[33]  Kira M. Veley,et al.  Functional Redundancy and New Roles for Genes of the Autonomous Floral-Promotion Pathway1[C][W][OA] , 2008, Plant Physiology.

[34]  R. Martienssen,et al.  Vernalization requires epigenetic silencing of FLC by histone methylation , 2004, Nature.

[35]  Ilha Lee,et al.  The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[36]  R. Amasino,et al.  FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering , 1999, Plant Cell.

[37]  J. Chory,et al.  Activation tagging of the floral inducer FT. , 1999, Science.

[38]  M Koornneef,et al.  Genetic interactions among late-flowering mutants of Arabidopsis. , 1998, Genetics.

[39]  S. Jacobsen,et al.  LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[40]  C. Dean,et al.  Multiple Pathways in the Decision to Flower: Enabling, Promoting, and Resetting , 2004, The Plant Cell Online.

[41]  D. Inzé,et al.  Oxidative stress tolerance and longevity in Arabidopsis: the late-flowering mutant gigantea is tolerant to paraquat. , 1998, The Plant journal : for cell and molecular biology.

[42]  Mijin Oh,et al.  Historical perspective on breakthroughs in flowering field , 2007, Journal of Plant Biology.

[43]  M. Thomashow,et al.  Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[44]  K. Shinozaki,et al.  A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. , 1994, The Plant cell.

[45]  D. Weigel,et al.  Integration of floral inductive signals in Arabidopsis , 2000, Nature.

[46]  Ilha Lee,et al.  SUPPRESSOR OF FRIGIDA3 Encodes a Nuclear ACTIN-RELATED PROTEIN6 Required for Floral Repression in Arabidopsisw⃞ , 2005, The Plant Cell Online.

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

[48]  M. Koornneef,et al.  A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana , 1991, Molecular and General Genetics MGG.

[49]  R. Macknight,et al.  Genetic interactions of the Arabidopsis flowering time gene FCA, with genes regulating floral initiation. , 1999, The Plant journal : for cell and molecular biology.

[50]  Jian-Kang Zhu,et al.  ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. , 2003, Genes & development.

[51]  R. Amasino,et al.  Isolation of LUMINIDEPENDENS: a gene involved in the control of flowering time in Arabidopsis. , 1994, The Plant cell.

[52]  E. Stockinger,et al.  Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[53]  F. Parcy Flowering: a time for integration. , 2005, The International journal of developmental biology.

[54]  Hongyu Zhao,et al.  Analysis of Transcription Factor HY5 Genomic Binding Sites Revealed Its Hierarchical Role in Light Regulation of Development[W] , 2007, The Plant Cell Online.

[55]  Y. Kobayashi,et al.  A pair of related genes with antagonistic roles in mediating flowering signals. , 1999, Science.

[56]  Michael F. Thomashow,et al.  PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. , 1999, Annual review of plant physiology and plant molecular biology.

[57]  R. Amasino,et al.  Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1 , 2006, Nature Genetics.

[58]  R. Amasino,et al.  Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3 , 2004, Nature.

[59]  Michael F. Thomashow,et al.  Low Temperature Induction of Arabidopsis CBF1, 2, and 3 Is Gated by the Circadian Clock1 , 2005, Plant Physiology.

[60]  Yang Wu,et al.  A repressor complex governs the integration of flowering signals in Arabidopsis. , 2008, Developmental cell.