The 14-3-3 Proteins μ and υ Influence Transition to Flowering and Early Phytochrome Response1[C][OA]

14-3-3 proteins regulate a diverse set of biological responses but developmental phenotypes associated with 14-3-3 mutations have not been described in plants. Here, physiological and biochemical tests demonstrate interactions between 14-3-3s and the well-established mechanisms that govern light sensing and photoperiodic flowering control. Plants featuring homozygous disruption of 14-3-3 isoforms υ and μ display defects in light sensing and/or response. Mutant plants flower late and exhibit long hypocotyls under red light, with little effect under blue or far-red light. The long hypocotyl phenotype is consistent with a role for 14-3-3 υ and μ in phytochrome B signaling. Yeast two-hybrid and coimmunoprecipitation assays indicate that 14-3-3 υ and μ proteins physically interact with CONSTANS, a central regulator of the photoperiod pathway. Together, these data indicate a potential role for specific 14-3-3 isoforms in affecting photoperiodic flowering via interaction with CONSTANS, possibly as integrators of light signals sensed through the phytochrome system.

[1]  G. Rédei Supervital Mutants of Arabidopsis. , 1962, Genetics.

[2]  J. Heslop-Harrison,et al.  The Transition to Flowering , 1964, Nature.

[3]  Jeffrey H. Miller Experiments in molecular genetics , 1972 .

[4]  M. Koornneef,et al.  Flowering responses to light-breaks in photomorphogenic mutants of Arabidopsis thaliana, a long-day plant , 1991 .

[5]  R. Ferl,et al.  Brain proteins in plants: an Arabidopsis homolog to neurotransmitter pathway activators is part of a DNA binding complex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[6]  E. Liscum,et al.  Genetic Evidence That the Red-Absorbing Form of Phytochrome B Modulates Gravitropism in Arabidopsis thaliana , 1993, Plant physiology.

[7]  Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. , 1993, The Plant cell.

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

[9]  P. Robson,et al.  Genetic and Transgenic Evidence That Phytochromes A and B Act to Modulate the Gravitropic Orientation of Arabidopsis thaliana Hypocotyls , 1996, Plant physiology.

[10]  R. Ferl,et al.  14‐3‐3 proteins associate with the regulatory phosphorylation site of spinach leaf nitrate reductase in an isoform‐specific manner and reduce dephosphorylation of Ser‐543 by endogenous protein phosphatases , 1996, FEBS letters.

[11]  Robert J. Ferl,et al.  14-3-3 PROTEINS AND SIGNAL TRANSDUCTION. , 1996, Annual review of plant physiology and plant molecular biology.

[12]  R. Ferl,et al.  The heterologous interactions among plant 14-3-3 proteins and identification of regions that are important for dimerization. , 1997, Archives of biochemistry and biophysics.

[13]  C. Larsson,et al.  A phosphothreonine residue at the C-terminal end of the plasma membrane H+-ATPase is protected by fusicoccin-induced 14-3-3 binding. , 1998, Plant physiology.

[14]  D. Toroser,et al.  Site‐specific regulatory interaction between spinach leaf sucrose‐phosphate synthase and 14‐3‐3 proteins , 1998, FEBS letters.

[15]  X. Deng,et al.  Arabidopsis bZIP Protein HY5 Directly Interacts with Light-Responsive Promoters in Mediating Light Control of Gene Expression , 1998, Plant Cell.

[16]  J. Chory,et al.  Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. , 1998, Plant physiology.

[17]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[18]  A. Aitken,et al.  Human cruciform binding protein belongs to the 14-3-3 family. , 1998, Biochemistry.

[19]  S. Masters,et al.  Interaction of 14-3-3 with a nonphosphorylated protein ligand, exoenzyme S of Pseudomonas aeruginosa. , 1999, Biochemistry.

[20]  M. Piotrowski,et al.  Phosphorylation of Thr-948 at the C Terminus of the Plasma Membrane H+-ATPase Creates a Binding Site for the Regulatory 14-3-3 Protein , 1999, Plant Cell.

[21]  A. Stensballe,et al.  Binding of 14-3-3 Protein to the Plasma Membrane H+-ATPase AHA2 Involves the Three C-terminal Residues Tyr946-Thr-Val and Requires Phosphorylation of Thr947 * , 1999, The Journal of Biological Chemistry.

[22]  R. Ferl,et al.  Specific Interactions with TBP and TFIIB in Vitro Suggest That 14-3-3 Proteins May Participate in the Regulation of Transcription When Part of a DNA Binding Complex , 1999, Plant Cell.

[23]  C. Gatz,et al.  Sequences within both the N- and C-terminal domains of phytochrome A are required for PFR ubiquitination and degradation. , 1999, The Plant journal : for cell and molecular biology.

[24]  S. Kay,et al.  Light-dependent Translocation of a Phytochrome B-GFP Fusion Protein to the Nucleus in Transgenic Arabidopsis , 1999, The Journal of cell biology.

[25]  Toshinori Kinoshita,et al.  Blue light activates the plasma membrane H+‐ATPase by phosphorylation of the C‐terminus in stomatal guard cells , 1999, The EMBO journal.

[26]  D. E. Somers,et al.  Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. , 2000, Science.

[27]  E. Huq,et al.  Direct targeting of light signals to a promoter element-bound transcription factor. , 2000, Science.

[28]  E. Huq,et al.  GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  S. Huber Faculty Opinions recommendation of 14-3-3 proteins regulate intracellular localization of the bZIP transcriptional activator RSG. , 2001 .

[30]  D K Chapman,et al.  Transgene expression patterns indicate that spaceflight affects stress signal perception and transduction in arabidopsis. , 2001, Plant physiology.

[31]  G. Coupland,et al.  Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. , 2002, The Plant journal : for cell and molecular biology.

[32]  S. Ishida,et al.  14-3-3 Proteins Regulate Intracellular Localization of the bZIP Transcriptional Activator RSG Article, publication date, and citation information can be found at www.aspb.org/cgi/doi/10.1105/tpc.010188. , 2001, The Plant Cell Online.

[33]  K. Folta,et al.  Photocontrol of stem growth. , 2001, Current opinion in plant biology.

[34]  J. Christie,et al.  Blue Light Sensing in Higher Plants* , 2001, The Journal of Biological Chemistry.

[35]  Robert J Ferl,et al.  Consummating signal transduction: the role of 14-3-3 proteins in the completion of signal-induced transitions in protein activity. , 2002, The Plant cell.

[36]  Chentao Lin Phototropin Blue Light Receptors and Light-Induced Movement Responses in Plants , 2002, Science's STKE.

[37]  Dirk Inzé,et al.  GATEWAY vectors for Agrobacterium-mediated plant transformation. , 2002, Trends in plant science.

[38]  J. Chory,et al.  Regulation of flowering time by light quality , 2003, Nature.

[39]  K. Halliday,et al.  Phytochromes B, D, and E Act Redundantly to Control Multiple Physiological Responses in Arabidopsis , 2003, Plant Physiology.

[40]  E. Huq,et al.  Nuclear translocation of the photoreceptor phytochrome B is necessary for its biological function in seedling photomorphogenesis. , 2003, The Plant journal : for cell and molecular biology.

[41]  T. Kinoshita,et al.  Blue-Light- and Phosphorylation-Dependent Binding of a 14-3-3 Protein to Phototropins in Stomatal Guard Cells of Broad Bean1 , 2003, Plant Physiology.

[42]  Angel F. Lopez,et al.  The Dimeric Versus Monomeric Status of 14-3-3ζ Is Controlled by Phosphorylation of Ser58 at the Dimer Interface* , 2003, Journal of Biological Chemistry.

[43]  J. Ecker,et al.  Isolation and Characterization of phyC Mutants in Arabidopsis Reveals Complex Crosstalk between Phytochrome Signaling Pathways Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012971. , 2003, The Plant Cell Online.

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

[45]  J. Borst,et al.  The Arabidopsis SERK1 protein interacts with the AAA-ATPase AtCDC48, the 14-3-3 protein GF14λ and the PP2C phosphatase KAPP , 2005, Planta.

[46]  E. Schäfer,et al.  The light-induced reduction of the gravitropic growth-orientation of seedlings of Arabidopsis thaliana (L.) Heynh. is a photomorphogenic response mediated synergistically by the far-red-absorbing forms of phytochromes A and B , 2004, Planta.

[47]  D. Ravenscroft,et al.  Photoreceptor Regulation of CONSTANS Protein in Photoperiodic Flowering , 2004, Science.

[48]  R. Macknight,et al.  It's time to flower: the genetic control of flowering time , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[49]  R. Amasino,et al.  Vernalization and flowering time. , 2005, Current opinion in biotechnology.

[50]  Raymond Wheeler,et al.  Design and fabrication of adjustable red-green-blue LED light arrays for plant research , 2005, BMC Plant Biology.

[51]  Jeong-Il Kim,et al.  Phytochrome phosphorylation in plant light signaling , 2005, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[52]  Shin-Ichiro Inoue,et al.  Biochemical characterization of plasma membrane H+-ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light. , 2005, Plant & cell physiology.

[53]  J. L. Carrasco,et al.  14-3-3 Mediates Transcriptional Regulation by Modulating Nucleocytoplasmic Shuttling of Tobacco DNA-binding Protein Phosphatase-1* , 2006, Journal of Biological Chemistry.

[54]  R. Ferl,et al.  Exposed Loop Domains of Complexed 14-3-3 Proteins Contribute to Structural Diversity and Functional Specificity1 , 2006, Plant Physiology.

[55]  Richard M. Clark,et al.  The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana , 2006, Nature Genetics.

[56]  Broome,et al.  Literature cited , 1924, A Guide to the Carnivores of Central America.