Multiple interactions amongst floral homeotic MADS box proteins.

Most known floral homeotic genes belong to the MADS box family and their products act in combination to specify floral organ identity by an unknown mechanism. We have used a yeast two‐hybrid system to investigate the network of interactions between the Antirrhinum organ identity gene products. Selective heterodimerization is observed between MADS box factors. Exclusive interactions are detected between two factors, DEFICIENS (DEF) and GLOBOSA (GLO), previously known to heterodimerize and control development of petals and stamens. In contrast, a third factor, PLENA (PLE), which is required for reproductive organ development, can interact with the products of MADS box genes expressed at early, intermediate and late stages. We also demonstrate that heterodimerization of DEF and GLO requires the K box, a domain not found in non‐plant MADS box factors, indicating that the plant MADS box factors may have different criteria for interaction. The association of PLENA and the temporally intermediate MADS box factors suggests that part of their function in mediating between the meristem and organ identity genes is accomplished through direct interaction. These data reveal an unexpectedly complex network of interactions between the factors controlling flower development and have implications for the determination of organ identity.

[1]  Song Tan,et al.  Structure of serum response factor core bound to DNA , 1995, Nature.

[2]  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.

[3]  E. Meyerowitz,et al.  Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. , 1994, Genes & development.

[4]  H. Sommer,et al.  Characterization of the Antirrhinum floral homeotic MADS‐box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. , 1992, The EMBO journal.

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

[6]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[7]  A. Sharrocks,et al.  The MADS-box family of transcription factors. , 1995, European journal of biochemistry.

[8]  H. Ma,et al.  Isolation and characterization of the binding sequences for the product of the Arabidopsis floral homeotic gene AGAMOUS. , 1993, Nucleic acids research.

[9]  M. Purugganan,et al.  Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. , 1995, Genetics.

[10]  H. Ma,et al.  DNA binding properties of two Arabidopsis MADS domain proteins: binding consensus and dimer formation. , 1996, The Plant cell.

[11]  Cindy Gustafson-Brown,et al.  Regulation of the arabidopsis floral homeotic gene APETALA1 , 1994, Cell.

[12]  S. Fields,et al.  The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[13]  H. Sommer,et al.  Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. , 1990, The EMBO journal.

[14]  A. Nordheim,et al.  A protein domain conserved between yeast MCM1 and human SRF directs ternary complex formation. , 1991, The EMBO journal.

[15]  L. Breeden,et al.  Regulation of the yeast HO gene. , 1985, Cold Spring Harbor symposia on quantitative biology.

[16]  S. Fields,et al.  The two-hybrid system: an assay for protein-protein interactions. , 1994, Trends in genetics : TIG.

[17]  M. Yanofsky.  Floral Meristems to Floral Organs: Genes Controlling Early Events in Arabidopsis Flower Development , 1995 .

[18]  S. McKnight,et al.  Diversity and specificity in transcriptional regulation: the benefits of heterotypic dimerization. , 1991, Trends in biochemical sciences.

[19]  R. Schiestl,et al.  Improved method for high efficiency transformation of intact yeast cells. , 1992, Nucleic acids research.

[20]  Z. Schwarz‐Sommer,et al.  Control of floral organ identity by homeotic MADS-box transcription factors. , 1994, Results and problems in cell differentiation.

[21]  E. Meyerowitz,et al.  Arabidopsis homeotic gene APETALA3 ectopic expression: Transcriptional and posttranscriptional regulation determine floral organ identity , 1994, Cell.

[22]  C. Somerville,et al.  Genetic control of morphogenesis in Arabidopsis , 1988 .

[23]  J. Thomas,et al.  Thinking about genetic redundancy. , 1993, Trends in genetics : TIG.

[24]  Hong Ma,et al.  The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors , 1990, Nature.

[25]  A. Sharrocks,et al.  Identification of amino acids essential for DNA binding and dimerization in p67SRF: implications for a novel DNA-binding motif , 1993, Molecular and cellular biology.

[26]  L. Pnueli,et al.  The TM5 MADS Box Gene Mediates Organ Differentiation in the Three Inner Whorls of Tomato Flowers. , 1994, The Plant cell.

[27]  E. Coen,et al.  Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of antirrhinum , 1993, Cell.

[28]  E. Meyerowitz,et al.  AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. , 1991, Genes & development.

[29]  H. Sommer,et al.  GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. , 1992, The EMBO journal.

[30]  Richard Treisman,et al.  Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element , 1988, Cell.

[31]  H. Feilotter,et al.  Construction of an improved host strain for two hybrid screening. , 1994, Nucleic acids research.

[32]  W. Nacken,et al.  Genetic Control of Flower Development by Homeotic Genes in Antirrhinum majus , 1990, Science.

[33]  S. Fields,et al.  Elimination of false positives that arise in using the two-hybrid system. , 1993, BioTechniques.

[34]  G. Angenent,et al.  Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. , 1994, The Plant journal : for cell and molecular biology.

[35]  R. Treisman,et al.  Human SRF-related proteins: DNA-binding properties and potential regulatory targets. , 1991, Genes & development.

[36]  S. Elledge,et al.  The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. , 1993, Genes & development.

[37]  W. Nacken,et al.  The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes from Antirrhinum and Arabidopsis. , 1991, The Plant journal : for cell and molecular biology.

[38]  H. Sommer,et al.  Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS‐box gene squamosa in Antirrhinum majus. , 1992, The EMBO journal.

[39]  Y. Shimura,et al.  Nucleotide sequences recognized by the AGAMOUS MADS domain of Arabidopsis thaliana in vitro. , 1993, The Plant journal : for cell and molecular biology.

[40]  G. Angenent,et al.  Differential expression of two MADS box genes in wild-type and mutant petunia flowers. , 1992, The Plant cell.

[41]  R. Sternglanz,et al.  Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system , 1995, Molecular and cellular biology.

[42]  G. Ammerer.  Identification, purification, and cloning of a polypeptide (PRTF/GRM) that binds to mating-specific promoter elements in yeast. , 1990, Genes & development.

[43]  Elliot M. Meyerowitz,et al.  The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens , 1992, Cell.

[44]  F. Winston,et al.  A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. , 1987, Gene.

[45]  S. Rounsley,et al.  Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. , 1995, The Plant cell.

[46]  Cindy Gustafson-Brown,et al.  Molecular characterization of the Arabidopsis floral homeotic gene APETALA1 , 1992, Nature.