Homologous NF-YC2 Subunit from Arabidopsis and Tobacco Is Activated by Photooxidative Stress and Induces Flowering

The transcription factor NF-Y consists of the three subunits A, B and C, which are encoded in Arabidopsis in large gene families. The multiplicity of the genes implies that NF-Y may act in diverse combinations of each subunit for the transcriptional control. We aimed to assign a function in stress response and plant development to NF-YC subunits by analyzing the expression of NF-Y genes and exploitation of nf-y mutants. Among the subunit family, NF-YC2 showed the strongest inducibility towards oxidative stress, e.g. photodynamic, light, oxidative, heat and drought stress. A tobacco NF-YC homologous gene was found to be inducible by photooxidative stress generated by an accumulation of the tetrapyrrole metabolite, coproporphyrin. Despite the stress induction, an Arabidopsis nf-yc2 mutant and NF-YC2 overexpressors did not show phenotypical differences compared to wild-type seedlings in response to photooxidative stress. This can be explained by the compensatory potential of other members of the NF-YC family. However, NF-YC2 overexpression leads to an early flowering phenotype that is correlated with increased FLOWERING LOCUS T-transcript levels. It is proposed that NF-YC2 functions in floral induction and is a candidate gene among the NF-Y family for the transcriptional activation upon oxidative stress.

[1]  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.

[2]  H. Mock,et al.  Kinetics of antioxidative defence responses to photosensitisation in porphyrin-accumulating tobacco plants , 2002 .

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

[4]  G. Coupland,et al.  Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. , 2009, The Plant journal : for cell and molecular biology.

[5]  Robert B Goldberg,et al.  LEAFY COTYLEDON1-LIKE Defines a Class of Regulators Essential for Embryo Development Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006973. , 2003, The Plant Cell Online.

[6]  K. Roháček.  Chlorophyll Fluorescence Parameters: The Definitions, Photosynthetic Meaning, and Mutual Relationships , 2002, Photosynthetica.

[7]  Hailing Jin,et al.  Multifunctionality and diversity within the plant MYB-gene family , 1999, Plant Molecular Biology.

[8]  Jianhua Zhu,et al.  The Arabidopsis NFYA5 Transcription Factor Is Regulated Transcriptionally and Posttranscriptionally to Promote Drought Resistance[W] , 2008, The Plant Cell Online.

[9]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

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

[11]  O. Ratcliffe,et al.  The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. , 2010, The New phytologist.

[12]  K. Matuoka,et al.  Nuclear factor Y (NF-Y) and cellular senescence. , 1999, Experimental cell research.

[13]  O. Nilsson,et al.  The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. , 2007, The Plant journal : for cell and molecular biology.

[14]  Robert B Goldberg,et al.  Arabidopsis LEAFY COTYLEDON1 Is Sufficient to Induce Embryo Development in Vegetative Cells , 1998, Cell.

[15]  C. Turnbull,et al.  Long-distance regulation of flowering time. , 2011, Journal of experimental botany.

[16]  M. Rieping,et al.  Synergistic effect of upstream sequences, CCAAT box elements, and HSE sequences for enhanced expression of chimaeric heat shock genes in transgenic tobacco , 2004, Molecular and General Genetics MGG.

[17]  G. Coupland,et al.  The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. , 2006, The Plant journal : for cell and molecular biology.

[18]  B. Crombrugghe,et al.  Role of the CCAAT-binding protein CBF/NF-Y in transcription. , 1998, Trends in biochemical sciences.

[19]  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.

[20]  S. Maity,et al.  Recombinant rat CBF-C, the third subunit of CBF/NFY, allows formation of a protein-DNA complex with CBF-A and CBF-B and with yeast HAP2 and HAP3. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Nobuhiro Suzuki,et al.  Ascorbate Peroxidase 1 Plays a Key Role in the Response of Arabidopsis thaliana to Stress Combination* , 2008, Journal of Biological Chemistry.

[22]  E. Kruse,et al.  Reduction of coproporphyrinogen oxidase level by antisense RNA synthesis leads to deregulated gene expression of plastid proteins and affects the oxidative defense system. , 1995, The EMBO journal.

[23]  B. P. Halling,et al.  Inhibition of plant protoporphyrinogen oxidase by the herbicide acifluorfen-methyl. , 1989, Plant physiology.

[24]  R. Canales,et al.  Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres , 2007, Proceedings of the National Academy of Sciences.

[25]  O. Ratcliffe,et al.  The Nuclear Factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis , 2008, Planta.

[26]  R. Mantovani,et al.  The molecular biology of the CCAAT-binding factor NF-Y. , 1999, Gene.

[27]  S. Howell,et al.  bZIP28 and NF-Y Transcription Factors Are Activated by ER Stress and Assemble into a Transcriptional Complex to Regulate Stress Response Genes in Arabidopsis[W][OA] , 2010, Plant Cell.

[28]  C. Tonelli,et al.  Regulation of novel members of the Arabidopsis thaliana CCAAT-binding nuclear factor Y subunits. , 2002, Gene.

[29]  C. Benoist,et al.  Evolutionary variation of the CCAAT-binding transcription factor NF-Y. , 1992, Nucleic acids research.

[30]  F. Turck,et al.  Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. , 2008, Annual review of plant biology.

[31]  T. Hisamatsu,et al.  The nature of floral signals in Arabidopsis. II. Roles for FLOWERING LOCUS T (FT) and gibberellin , 2008, Journal of experimental botany.

[32]  Yan Zhang,et al.  NF-YC3, NF-YC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. , 2010, The Plant journal : for cell and molecular biology.

[33]  M. Tamoi,et al.  Regulation and function of ascorbate peroxidase isoenzymes. , 2002, Journal of experimental botany.

[34]  R. Mantovani,et al.  A survey of 178 NF-Y binding CCAAT boxes. , 1998, Nucleic acids research.

[35]  R. Mantovani,et al.  NF-Y binding to twin CCAAT boxes: role of Q-rich domains and histone fold helices. , 1999, Journal of molecular biology.

[36]  A. Moorman,et al.  Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data , 2003, Neuroscience Letters.

[37]  Kristen K. Dang,et al.  Tissue-Specific Expression Patterns of Arabidopsis NF-Y Transcription Factors Suggest Potential for Extensive Combinatorial Complexity1[W][OA] , 2008, Plant Physiology.

[38]  Jean-Michel Claverie,et al.  Phylogeny.fr: robust phylogenetic analysis for the non-specialist , 2008, Nucleic Acids Res..

[39]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[40]  L. Tian,et al.  Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in Photosystem II antenna size and stability. , 2002, Biochimica et biophysica acta.

[41]  C. Tonelli,et al.  Regulation of the CCAAT-Binding NF-Y subunits in Arabidopsis thaliana. , 2001, Gene.

[42]  B. Grimm,et al.  Studies on differential nuclear translocation mechanism and assembly of the three subunits of the Arabidopsis thaliana transcription factor NF-Y. , 2012, Molecular plant.

[43]  S. Masiero,et al.  Ternary Complex Formation between MADS-box Transcription Factors and the Histone Fold Protein NF-YB* , 2002, The Journal of Biological Chemistry.

[44]  K. Folta,et al.  Regions of the pea Lhcb1*4 promoter necessary for blue-light regulation in transgenic Arabidopsis. , 1999, Plant physiology.