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.

The AGAMOUS (AG) gene is necessary for stamen and carpel development and is part of a monophyletic clade of MADS-box genes that also includes SHATTERPROOF1 (SHP1), SHP2, and SEEDSTICK (STK). Here, we show that ectopic expression of either the STK or SHP gene is sufficient to induce the transformation of sepals into carpeloid organs bearing ovules. Moreover, the fact that these organ transformations occur when the STK gene is expressed ectopically in ag mutants shows that STK can promote carpel development in the absence of AG activity. We also show that STK, AG, SHP1, and SHP2 can form multimeric complexes and that these interactions require the SEPALLATA (SEP) MADS-box proteins. We provide genetic evidence for this role of the SEP proteins by showing that a reduction in SEP activity leads to the loss of normal ovule development, similar to what occurs in stk shp1 shp2 triple mutants. Together, these results indicate that the SEP proteins, which are known to form multimeric complexes in the control of flower organ identity, also form complexes to control normal ovule development.

[1]  C. Koncz,et al.  A simple method to transfer, integrate and study expression of foreign genes, such as chicken ovalbumin and alpha‐actin in plant tumors. , 1984, The EMBO journal.

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

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

[4]  P. Benfey,et al.  Combinatorial and synergistic properties of CaMV 35S enhancer subdomains. , 1990, The EMBO journal.

[5]  P. Benfey,et al.  Tissue‐specific expression from CaMV 35S enhancer subdomains in early stages of plant development. , 1990, The EMBO journal.

[6]  J. Bowman,et al.  Genetic interactions among floral homeotic genes of Arabidopsis. , 1991, Development.

[7]  D. Jacobson,et al.  Rapid, nonradioactive screening for activating ras oncogene mutations using PCR-primer introduced restriction analysis (PCR-PIRA) , 1991, PCR methods and applications.

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

[9]  D. Jacobson,et al.  Rapid, nonradioactive screening for activating ras oncogene mutations using PCR-primer introduced restriction analysis (PCR-PIRA). , 1992, PCR methods and applications.

[10]  Ectopic expression of pMADS3 in transgenic petunia phenocopies the petunia blind mutant. , 1993, The Plant cell.

[11]  S. Hake,et al.  Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. , 1993, The Plant cell.

[12]  A. V. Van Dijken,et al.  A novel class of MADS box genes is involved in ovule development in petunia. , 1995, The Plant cell.

[13]  M. Hülskamp,et al.  Wild‐type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole‐mount tissue , 1995 .

[14]  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.

[15]  H. Saedler,et al.  Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs of AGAMOUS-like MADS-box genes from maize. , 1995, Gene.

[16]  E. Koetje,et al.  The petunia MADS box gene FBP11 determines ovule identity. , 1995, The Plant cell.

[17]  H. Sommer,et al.  Multiple interactions amongst floral homeotic MADS box proteins. , 1996, The EMBO journal.

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

[19]  U. Grossniklaus,et al.  The molecular and genetic basis of ovule and megagametophyte development. , 1998, Seminars in cell & developmental biology.

[20]  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.

[21]  Multiple AGAMOUS Homologs from Cucumber and Petunia Differ in Their Ability to Induce Reproductive Organ Fate , 1998, Plant Cell.

[22]  M. Mandel,et al.  The ArabidopsisAGL9 MADS box gene is expressed in young flower primordia , 1998, Sexual Plant Reproduction.

[23]  G. Haughn,et al.  BELL1 and AGAMOUS genes promote ovule identity in Arabidopsis thaliana. , 1999, The Plant journal : for cell and molecular biology.

[24]  P. Wittich,et al.  OsMADS13, a novel rice MADS-box gene expressed during ovule development. , 1999, Developmental genetics.

[25]  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.

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

[27]  Yuval Eshed,et al.  SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis , 2000, Nature.

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

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

[30]  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.

[31]  G. Angenent,et al.  Ovule-specific MADS-box proteins have conserved protein-protein interactions in monocot and dicot plants , 2002, Molecular Genetics and Genomics.

[32]  G. Ditta,et al.  Assessing the redundancy of MADS-box genes during carpel and ovule development , 2003, Nature.

[33]  Hong Ma,et al.  Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant arabidopsis flowers , 1994, Plant Molecular Biology.