The OsFOR1 gene encodes a polygalacturonase-inhibiting protein (PGIP) that regulates floral organ number in rice

We have isolated a cDNA clone, OsFOR1, from the immature panicles of rice. The OsFOR1 (Oryza sativa floral organ regulator 1) gene encodes a protein that contains a leucine-rich repeat (LRR) domain. This domain comprises 10 tandem repeats of a canonical 24-amino acid LRR sequence. The structure and the number of LRRs for OsFOR1 are similar to those of polygalacturonase-inhibiting proteins (PGIPs) from various other plant species. Moreover, the OsFOR1 recombinant protein, when fused to maltose-binding protein (MBP), shows PGIP activity against the Aspergillus niger polygalacturonase. OsFOR1 is highly expressed in the calli and immature and mature panicles, while detectable at only low levels in seedling roots and mature stems. In situ hybridization experiments showed the transcripts of OsFOR1 are present in young spikelet primordia and in almost all of the young floral organs. Transgenic approaches were used to study in vivo functioning. Antisense expression of OsFOR1 resulted in an increase in the numbers of floral organs, including the stamen, carpel, palea/lemma, stigma, and lodicule. OsFOR1 transcript was not detected in the frizzy panicle mutant, which is defective in its spikelet formation but normal in inflorescence-meristem initiation and maintenance. Therefore, we suggest that OsFOR1 plays a role in the formation and/or maintenance of floral organ primordia.

[1]  V. Ramanathan,et al.  A Protein from Immature Raspberry Fruits which Inhibits Endopolygalacturonases from Botrytis cinerea and other Micro-organisms , 1993 .

[2]  E. Ruoslahti,et al.  Negative regulation of transforming growth factor-beta by the proteoglycan decorin. , 1990, Nature.

[3]  G. De Lorenzo,et al.  The promoter of a gene encoding a polygalacturonase-inhibiting protein of Phaseolus vulgaris L. is activated by wounding but not by elicitors or pathogen infection , 1998, Planta.

[4]  P. Lillford,et al.  A carrot leucine-rich-repeat protein that inhibits ice recrystallization. , 1998, Science.

[5]  C. Weurman.  PECTINASE INHIBITORS IN PEARS , 1953 .

[6]  G. An,et al.  Molecular cloning and characterization of OsLRK1 encoding a putative receptor-like protein kinase from Oryza sativa , 2000 .

[7]  Y. Moon,et al.  Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. , 1999, Plant physiology.

[8]  A. Kajava.  Structural diversity of leucine-rich repeat proteins. , 1998, Journal of molecular biology.

[9]  G. Tucker,et al.  Polygalacturonase expression during leaf abscission of normal and transgenic tomato plants , 1991, Planta.

[10]  J. Fletcher,et al.  Shoot and floral meristem maintenance in arabidopsis. , 2002, Annual review of plant biology.

[11]  M. Matsuoka,et al.  Regional Expression of the Rice KN1-Type Homeobox Gene Family during Embryo, Shoot, and Flower Development , 1999, Plant Cell.

[12]  F. Cervone,et al.  Polygalacturonase­ Inhibiting Proteins (PGIPs): Their Role in Specificity and Defense against Pathogenic Fungi , 1997 .

[13]  A. Powell,et al.  Structure and expression of an inhibitor of fungal polygalacturonases from tomato , 1994, Plant Molecular Biology.

[14]  G. An,et al.  Identification of class B and class C floral organ identity genes from rice plants , 1998, Plant Molecular Biology.

[15]  Colin Brownlee,et al.  Role of the extracellular matrix in cell-cell signalling: paracrine paradigms. , 2002, Current opinion in plant biology.

[16]  R. D'Ovidio,et al.  Purification and molecular characterization of a soybean polygalacturonase-inhibiting protein , 2004, Planta.

[17]  A. Hemmings,et al.  The specificity of polygalacturonase‐inhibiting protein (PGIP): a single amino acid substitution in the solvent‐exposed β‐strand/β‐turn region of the leucine‐rich repeats (LRRs) confers a new recognition capability , 1999, The EMBO journal.

[18]  L. Vázquez-Moreno,et al.  Floral transcription factor AGAMOUS interacts in vitro with a leucine-rich repeat and an acid phosphatase protein complex. , 2001, Biochemical and biophysical research communications.

[19]  R. D'Ovidio,et al.  The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi. , 2001, Annual review of phytopathology.

[20]  G. An,et al.  Identification of a rice APETALA3 homologue by yeast two-hybrid screening , 1999, Plant Molecular Biology.

[21]  E. Ruoslahti,et al.  Negative regulation of transforming growth factor-β by the proteoglycan decorin , 1990, Nature.

[22]  P. Becraft.  First published online as a Review in Advance on June 26, 2002 RECEPTOR KINASE SIGNALING IN PLANT DEVELOPMENT , 2022 .

[23]  A. Powell,et al.  Molecular Characterization of a Polygalacturonase Inhibitor from Pyrus communis L. cv Bartlett , 1993, Plant physiology.

[24]  P. Ulvskov,et al.  Analysis of a dehiscence zone endo-polygalacturonase in oilseed rape (Brassica napus) and Arabidopsis thaliana: evidence for roles in cell separation in dehiscence and abscission zones, and in stylar tissues during pollen tube growth , 2001, Plant Molecular Biology.

[25]  N. Rascio,et al.  Cellulase and polygalacturonase involvement in the abscission of leaf and fruit explants of peach , 1992, Plant Molecular Biology.

[26]  L. Federici,et al.  Secondary structure and post-translational modifications of the leucine-rich repeat protein PGIP (polygalacturonase-inhibiting protein) from Phaseolus vulgaris. , 2001, Biochemistry.

[27]  A. Falciatore,et al.  Semi-quantitative RT-PCR analysis of photoregulated gene expression in marine diatoms , 1999, Plant Molecular Biology.

[28]  H. Sommer,et al.  FIL2, an extracellular Leucine-Rich Repeat protein, is specifically expressed in Antirrhinum flowers. , 1994, The Plant journal : for cell and molecular biology.

[29]  G. Khush,et al.  Chromosomal location of some mutant genes through the use of primary trisomics of rice , 1986 .

[30]  S. Brunak,et al.  Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. , 2000, Journal of molecular biology.

[31]  P. Quail,et al.  Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation , 1992, Plant Molecular Biology.

[32]  G. An,et al.  Two rice MADS domain proteins interact with OsMADS1 , 2000, Plant Molecular Biology.

[33]  J. Roberts,et al.  Anatomical and biochemical changes associated with the induction of oilseed rape (Brassica napus) pod dehiscence by Dasineura brassicae (Winn.) , 1991 .

[34]  R. D'Ovidio,et al.  Polygalacturonase inhibiting proteins fromAllium porrumL. and their role in plant tissue against fungal endo-polygalacturonases☆ , 1997 .

[35]  J Kyozuka,et al.  The LAX1 and FRIZZY PANICLE 2 genes determine the inflorescence architecture of rice by controlling rachis-branch and spikelet development. , 2001, Developmental biology.

[36]  D. Hegedus,et al.  Two Brassica napus polygalacturonase inhibitory protein genes are expressed at different levels in response to biotic and abiotic stresses , 2003, Planta.

[37]  G. An,et al.  T-DNA Insertional Mutagenesis for Activation Tagging in Rice1 , 2002, Plant Physiology.

[38]  P. Albersheim,et al.  Host-Pathogen Interactions : XXXIII. A Plant Protein Converts a Fungal Pathogenesis Factor into an Elicitor of Plant Defense Responses. , 1989, Plant physiology.

[39]  Masahiro Miyoshi,et al.  Mutations associated with floral organ number in rice , 1996, Planta.

[40]  C. Yao.  Purification and characterization of a polygalacturonase-inhibiting protein from apple fruit , 1995 .

[41]  R. Forrest,et al.  Polygalacturonase, PGIP and oligogalacturonides in cell-cell communication. , 1994, Biochemical Society transactions.

[42]  R. Pressey,et al.  Polygalacturonase in pollen from corn and other grasses , 1989 .

[43]  P. Hirsch,et al.  A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid , 1983, Nature.

[44]  A. E. Watada,et al.  Degradation and solubilization of pectin by β‐galactosidases purified from avocado mesocarp , 1993 .

[45]  R. Pressey,et al.  Occurrence and properties of polygalacturonase in Avena and other plants. , 1977, Plant physiology.

[46]  P. Albersheim,et al.  Cloning and characterization of the gene encoding the endopolygalacturonase-inhibiting protein (PGIP) of Phaseolus vulgaris L. , 1992, The Plant journal : for cell and molecular biology.

[47]  D. Choi,et al.  Nucleotide sequence of a cDNA encoding ribosomal protein L31 (GenBank U23784) from Nicotiana glutinosa , 1995 .

[48]  P. Albersheim,et al.  Isolation and characterization of plant cell walls and cell wall components , 1986 .

[49]  J Deisenhofer,et al.  Proteins with leucine-rich repeats. , 1995, Current opinion in structural biology.

[50]  G. An,et al.  leafy hull sterile1 Is a Homeotic Mutation in a Rice MADS Box Gene Affecting Rice Flower Development , 2000, Plant Cell.

[51]  C. Sams,et al.  Gene encoding polygalacturonase inhibitor in apple fruit is developmentally regulated and activated by wounding and fungal infection , 1999, Plant Molecular Biology.

[52]  Sudhir Kumar,et al.  MEGA2: molecular evolutionary genetics analysis software , 2001, Bioinform..

[53]  S. Jang,et al.  Ectopic expression of tobacco MADS genes modulates flowering time and plant architecture. , 1999, Molecules and cells.