SEPALLATA3: the 'glue' for MADS box transcription factor complex formation

BackgroundPlant MADS box proteins play important roles in a plethora of developmental processes. In order to regulate specific sets of target genes, MADS box proteins dimerize and are thought to assemble into multimeric complexes. In this study a large-scale yeast three-hybrid screen is utilized to provide insight into the higher-order complex formation capacity of the Arabidopsis MADS box family. SEPALLATA3 (SEP3) has been shown to mediate complex formation and, therefore, special attention is paid to this factor in this study.ResultsIn total, 106 multimeric complexes were identified; in more than half of these at least one SEP protein was present. Besides the known complexes involved in determining floral organ identity, various complexes consisting of combinations of proteins known to play a role in floral organ identity specification, and flowering time determination were discovered. The capacity to form this latter type of complex suggests that homeotic factors play essential roles in down-regulation of the MADS box genes involved in floral timing in the flower via negative auto-regulatory loops. Furthermore, various novel complexes were identified that may be important for the direct regulation of the floral transition process. A subsequent detailed analysis of the APETALA3, PISTILLATA, and SEP3 proteins in living plant cells suggests the formation of a multimeric complex in vivo.ConclusionsOverall, these results provide strong indications that higher-order complex formation is a general and essential molecular mechanism for plant MADS box protein functioning and attribute a pivotal role to the SEP3 'glue' protein in mediating multimerization.

[1]  G. Angenent,et al.  Identification and Characterization of Four Chrysanthemum MADS-Box Genes, Belonging to the APETALA1/FRUITFULL and SEPALLATA3 Subfamilies1 , 2004, Plant Physiology.

[2]  Cindy Gustafson-Brown,et al.  AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. , 2003, The Plant journal : for cell and molecular biology.

[3]  E. Álvarez-Buylla,et al.  Conversion of leaves into petals in Arabidopsis , 2001, Current Biology.

[4]  B. Berger,et al.  MultiCoil: A program for predicting two‐and three‐stranded coiled coils , 1997, Protein science : a publication of the Protein Society.

[5]  Koji Goto,et al.  Complexes of MADS-box proteins are sufficient to convert leaves into floral organs , 2001, Nature.

[6]  M. Kater,et al.  AGL24, SHORT VEGETATIVE PHASE, and APETALA1 Redundantly Control AGAMOUS during Early Stages of Flower Development in Arabidopsis[W] , 2006, The Plant Cell Online.

[7]  D. Horner,et al.  Molecular and Phylogenetic Analyses of the Complete MADS-Box Transcription Factor Family in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011544. , 2003, The Plant Cell Online.

[8]  P. Robles,et al.  The SEP4 Gene of Arabidopsis thaliana Functions in Floral Organ and Meristem Identity , 2004, Current Biology.

[9]  Catherine A. Risebro,et al.  Nucleolar release of Hand1 acts as a molecular switch to determine cell fate , 2007, Nature Cell Biology.

[10]  Gerco C Angenent,et al.  Transcription factors do it together: the hows and whys of studying protein-protein interactions. , 2002, Trends in plant science.

[11]  J. Bowman,et al.  Turning floral organs into leaves, leaves into floral organs. , 2001, Current opinion in genetics & development.

[12]  G. Angenent,et al.  Control of Floral Meristem Determinacy in Petunia by MADS-Box Transcription Factors1[W] , 2006, Plant Physiology.

[13]  Joshua G. Steffen,et al.  The AGL62 MADS Domain Protein Regulates Cellularization during Endosperm Development in Arabidopsis[W] , 2008, The Plant Cell Online.

[14]  Yingzhen Yang,et al.  Defining subdomains of the K domain important for protein–protein interactions of plant MADS proteins , 2004, Plant Molecular Biology.

[15]  Detlef Weigel,et al.  Modes of intercellular transcription factor movement in the Arabidopsis apex , 2003, Development.

[16]  G. Angenent,et al.  Analysis of the petunia MADS-box transcription factor family , 2003, Molecular Genetics and Genomics.

[17]  Hong Ma,et al.  Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity , 1992, Cell.

[18]  B. Berger,et al.  Predicting coiled coils by use of pairwise residue correlations. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Gunnar Rätsch,et al.  At-TAX: a whole genome tiling array resource for developmental expression analysis and transcript identification in Arabidopsis thaliana , 2008, Genome Biology.

[20]  S. Yalovsky,et al.  Specification of Arabidopsis floral meristem identity by repression of flowering time genes , 2007, Development.

[21]  W. Crosby,et al.  APETALA1 and SEPALLATA3 interact to promote flower development. , 2001, The Plant journal : for cell and molecular biology.

[22]  H. Saedler,et al.  Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant. , 1995, Development.

[23]  L. Mao,et al.  Interaction study of MADS-domain proteins in tomato. , 2008, Journal of experimental botany.

[24]  E. Meyerowitz,et al.  Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[25]  D. Soltis,et al.  The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. , 2005, Genetics.

[26]  J L Bowman,et al.  Genes directing flower development in Arabidopsis. , 1989, The Plant cell.

[27]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

[28]  Detlef Weigel,et al.  Dissection of floral induction pathways using global expression analysis , 2003, Development.

[29]  L. Hennig,et al.  Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. , 2006, Genes & development.

[30]  G. Angenent,et al.  In vivo imaging of MADS-box transcription factor interactions. , 2006, Journal of experimental botany.

[31]  L. Hennig,et al.  The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. , 2003, Genes & development.

[32]  H. Saedler,et al.  Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. , 1996, Development.

[33]  Gerco C Angenent,et al.  Analysis of MADS box protein–protein interactions in living plant cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[34]  P. Burkhard,et al.  Coiled coils: a highly versatile protein folding motif. , 2001, Trends in cell biology.

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

[36]  Stefan de Folter,et al.  trans meets cis in MADS science. , 2006, Trends in plant science.

[37]  Melissa D. Lehti-Shiu,et al.  The MADS domain factors AGL15 and AGL18 act redundantly as repressors of the floral transition in Arabidopsis. , 2007, The Plant journal : for cell and molecular biology.

[38]  E. Coen,et al.  The war of the whorls: genetic interactions controlling flower development , 1991, Nature.

[39]  Hans Sommer,et al.  Ternary complex formation between the MADS‐box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus , 1999, The EMBO journal.

[40]  J. Borst,et al.  The Arabidopsis thaliana AAA protein CDC48A interacts in vivo with the somatic embryogenesis receptor-like kinase 1 receptor at the plasma membrane. , 2006, Journal of structural biology.

[41]  H. M. Duttweiler A highly sensitive and non-lethal beta-galactosidase plate assay for yeast. , 1996, Trends in genetics : TIG.

[42]  Johann Wolfgang von Goethe,et al.  Versuch die Metamorphose der Pflanzen zu erklären , 1973 .

[43]  H. Saedler,et al.  Mutant analysis, protein–protein interactions and subcellular localization of the Arabidopsis Bsister (ABS) protein , 2005, Molecular Genetics and Genomics.

[44]  U. Grossniklaus,et al.  The MADS Domain Protein DIANA Acts Together with AGAMOUS-LIKE80 to Specify the Central Cell in Arabidopsis Ovules[W] , 2008, The Plant Cell Online.

[45]  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.

[46]  H. Saedler,et al.  MADS-complexes regulate transcriptome dynamics during pollen maturation , 2007, Genome Biology.

[47]  R. D. Gietz,et al.  Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. , 2002, Methods in enzymology.

[48]  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.

[49]  Lucia Colombo,et al.  MADS-Box Protein Complexes Control Carpel and Ovule Development in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.015123. , 2003, The Plant Cell Online.

[50]  G. An,et al.  Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain , 1999, Plant Molecular Biology.

[51]  M. Robertson,et al.  The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. , 2006, The Plant journal : for cell and molecular biology.

[52]  E. Meyerowitz,et al.  The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS , 2004, Nature.

[53]  E. Meyerowitz,et al.  The Homeotic Protein AGAMOUS Controls Late Stamen Development by Regulating a Jasmonate Biosynthetic Gene in Arabidopsis[W] , 2007, The Plant Cell Online.

[54]  Kerstin Kaufmann,et al.  Tagging of MADS domain proteins for chromatin immunoprecipitation , 2007, BMC Plant Biology.

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

[56]  E. Craig,et al.  Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. , 1996, Genetics.

[57]  Yingzhen Yang,et al.  The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. , 2003, The Plant journal : for cell and molecular biology.

[58]  E. Álvarez-Buylla,et al.  An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[59]  H. M. Duttweiler A highly sensitive and non-lethal β-galactosidase plate assay for yeast , 1996 .

[60]  G. Angenent,et al.  Transcript profiling of transcription factor genes during silique development in Arabidopsis , 2004, Plant Molecular Biology.

[61]  Kerstin Kaufmann,et al.  In planta localisation patterns of MADS domain proteins during floral development in Arabidopsis thaliana , 2009, BMC Plant Biology.

[62]  Kerstin Kaufmann,et al.  Protein interactions of MADS box transcription factors involved in flowering in Lolium perenne. , 2006, Journal of experimental botany.

[63]  Hao Yu,et al.  AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[64]  S. Masiero,et al.  AGL23, a type I MADS-box gene that controls female gametophyte and embryo development in Arabidopsis. , 2008, The Plant journal : for cell and molecular biology.

[65]  V. Irish,et al.  Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. , 1996, Genes & development.

[66]  Richard G. H. Immink,et al.  The MADS Box Gene FBP2 Is Required for SEPALLATA Function in Petunia Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010280. , 2003, The Plant Cell Online.

[67]  M. Kater,et al.  AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. , 2008, The Plant journal : for cell and molecular biology.

[68]  Akira Kanno,et al.  Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization. , 2002, Molecular biology and evolution.

[69]  Joshua G. Steffen,et al.  AGL61 Interacts with AGL80 and Is Required for Central Cell Development in Arabidopsis1[W][OA] , 2008, Plant Physiology.

[70]  G. Ditta,et al.  B and C floral organ identity functions require SEPALLATA MADS-box genes , 2000, Nature.

[71]  U. Grossniklaus,et al.  A Bsister MADS-box gene involved in ovule and seed development in petunia and Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[72]  Detlef Weigel,et al.  Comprehensive Interaction Map of the Arabidopsis MADS Box Transcription Factorsw⃞ , 2005, The Plant Cell Online.

[73]  G. Ditta,et al.  Diverse roles for MADS box genes in Arabidopsis development. , 1995, The Plant cell.

[74]  G. Theißen,et al.  The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in ‘floral quartet’-like complexes in vitro , 2008, Nucleic acids research.

[75]  Heinz Saedler,et al.  Plant biology: Floral quartets , 2001, Nature.

[76]  Tal Nawy,et al.  Transcriptional Profile of the Arabidopsis Root Quiescent Centerw⃞ , 2005, The Plant Cell Online.

[77]  Joshua G. Steffen,et al.  AGL80 Is Required for Central Cell and Endosperm Development in Arabidopsis[W] , 2006, The Plant Cell Online.

[78]  M. Yanofsky,et al.  Function and evolution of the plant MADS-box gene family , 2001, Nature Reviews Genetics.

[79]  Robert B. Russell,et al.  DILIMOT: discovery of linear motifs in proteins , 2006, Nucleic Acids Res..

[80]  E. Meyerowitz,et al.  The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. , 1996, Development.

[81]  Elena R Alvarez-Buylla,et al.  AGAMOUS-LIKE 17, a novel flowering promoter, acts in a FT-independent photoperiod pathway. , 2008, The Plant journal : for cell and molecular biology.

[82]  Ana I. Caño-Delgado,et al.  Heterodimerization and Endocytosis of Arabidopsis Brassinosteroid Receptors BRI1 and AtSERK3 (BAK1) , 2004, The Plant Cell Online.

[83]  S. Masiero,et al.  Genetic and Molecular Interactions between BELL1 and MADS Box Factors Support Ovule Development in Arabidopsis[W] , 2007, The Plant Cell Online.