Aberrant spikelet and panicle1, encoding a TOPLESS-related transcriptional co-repressor, is involved in the regulation of meristem fate in rice.

Post-embryonic development depends on the activity of meristems in plants, and thus control of cell fate in the meristem is crucial to plant development and its architecture. In grasses such as rice and maize, the fate of reproductive meristems changes from indeterminate meristems, such as inflorescence and branch meristems, to determinate meristems, such as the spikelet meristem. Here we analyzed a recessive mutant of rice, aberrant spikelet and panicle1 (asp1), that showed pleiotropic phenotypes such as a disorganized branching pattern, aberrant spikelet morphology, and disarrangement of phyllotaxy. Close examination revealed that regulation of meristem fate was compromised in asp1: degeneration of the inflorescence meristem was delayed, transition from the branch meristem to the spikelet meristem was accelerated, and stem cell maintenance in both the branch meristem and the spikelet meristem was compromised. The genetic program was also disturbed in terms of spikelet development. Gene isolation revealed that ASP1 encodes a transcriptional co-repressor that is related to TOPLESS (TPL) in Arabidopsis and RAMOSA ENHANCER LOCUS2 (REL2) in maize. It is likely that the pleiotropic defects are associated with de-repression of multiple genes related to meristem function in the asp1 mutant. The asp1 mutant also showed de-repression of axillary bud growth and disturbed phyllotaxy in the vegetative phase, suggesting that the function of this gene is closely associated with auxin action. Consistent with these observations and the molecular function of Arabidopsis TPL, auxin signaling was also compromised in the rice asp1 mutant. Taken together, these results indicate that ASP1 regulates various aspects of developmental processes and physiological responses as a transcriptional co-repressor in rice.

[1]  A. Yoshida,et al.  Functional Diversification of CLAVATA3-Related CLE Proteins in Meristem Maintenance in Rice[W][OA] , 2008, The Plant Cell Online.

[2]  G. An,et al.  The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem. , 2006, The Plant journal : for cell and molecular biology.

[3]  S. Hake,et al.  The Control of Spikelet Meristem Identity by the branched silkless1 Gene in Maize , 2002, Science.

[4]  S. Hake,et al.  Floral meristem initiation and meristem cell fate are regulated by the maize AP2 genes ids1 and sid1 , 2008, Development.

[5]  Tadashi Hirasawa,et al.  New approach for rice improvement using a pleiotropic QTL gene for lodging resistance and yield , 2010, Nature communications.

[6]  S. Hake,et al.  The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1. , 1998, Genes & development.

[7]  J. Kyozuka,et al.  Characterization of OsPID, the rice ortholog of PINOID, and its possible involvement in the control of polar auxin transport. , 2007, Plant & cell physiology.

[8]  Xianting Wu,et al.  Genetic and physical interaction suggest that BARREN STALK 1 is a target of BARREN INFLORESCENCE2 in maize inflorescence development. , 2008, The Plant journal : for cell and molecular biology.

[9]  H. Kitano,et al.  panicle phytomer 1 mutations affect the panicle architecture of rice , 1998, Theoretical and Applied Genetics.

[10]  S. Hake,et al.  barren inflorescence2 Encodes a Co-Ortholog of the PINOID Serine/Threonine Kinase and Is Required for Organogenesis during Inflorescence and Vegetative Development in Maize1[C][W][OA] , 2007, Plant Physiology.

[11]  A. Yoshida,et al.  The homeotic gene long sterile lemma (G1) specifies sterile lemma identity in the rice spikelet , 2009, Proceedings of the National Academy of Sciences.

[12]  Takuji Sasaki,et al.  Rice Biology in the Genomics Era , 2008 .

[13]  J. Doebley,et al.  The role of barren stalk1 in the architecture of maize , 2004, Nature.

[14]  H. Hirano.  Genetic Regulation of Meristem Maintenance and Organ Specification in Rice Flower Development , 2008 .

[15]  H. Tsukaya,et al.  Distinct Regulation of Adaxial-Abaxial Polarity in Anther Patterning in Rice[C][W][OA] , 2010, Plant Cell.

[16]  Q. Qian,et al.  Cytokinin Oxidase Regulates Rice Grain Production , 2005, Science.

[17]  H. Kouchi,et al.  Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development , 1993, Molecular and General Genetics MGG.

[18]  Jerry D. Cohen,et al.  BARREN INFLORESCENCE2 interaction with ZmPIN1a suggests a role in auxin transport during maize inflorescence development. , 2009, Plant & cell physiology.

[19]  H. Kitano,et al.  Conservation and diversification of meristem maintenance mechanism in Oryza sativa: Function of the FLORAL ORGAN NUMBER2 gene. , 2006, Plant & cell physiology.

[20]  P. Springer,et al.  Architecture of floral branch systems in maize and related grasses , 2005, Nature.

[21]  J. Long,et al.  TOPLESS Mediates Auxin-Dependent Transcriptional Repression During Arabidopsis Embryogenesis , 2008, Science.

[22]  A. Gallavotti,et al.  sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize , 2008, Proceedings of the National Academy of Sciences.

[23]  G. An,et al.  Functional Diversification of the Two C-Class MADS Box Genes OSMADS3 and OSMADS58 in Oryza sativa[W][OA] , 2005, The Plant Cell Online.

[24]  Hirohiko Hirochika,et al.  PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADS-box protein, positively controls spikelet meristem identity in rice , 2009, Plant & cell physiology.

[25]  J. Long,et al.  Development and Stem Cells Research Article , 2022 .

[26]  Qian Qian,et al.  Control of tillering in rice , 2003, Nature.

[27]  S. Hake,et al.  barren inflorescence2 regulates axillary meristem development in the maize inflorescence. , 2001, Development.

[28]  S. Iida,et al.  Expression Level of ABERRANT PANICLE ORGANIZATION1 Determines Rice Inflorescence Form through Control of Cell Proliferation in the Meristem1[W] , 2009, Plant Physiology.

[29]  E. Meyerowitz,et al.  Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. , 2002, Development.

[30]  H. Kitano,et al.  Rice plant development: from zygote to spikelet. , 2005, Plant & cell physiology.

[31]  J. Long,et al.  Why so repressed? Turning off transcription during plant growth and development. , 2009, Current opinion in plant biology.

[32]  Z. Liu,et al.  LEUNIG, a putative transcriptional corepressor that regulates AGAMOUS expression during flower development. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[33]  S. Hake,et al.  The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1 , 2007, Nature Genetics.

[34]  The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1 , 2004, Development.

[35]  Zhongchi Liu,et al.  Groucho/Tup1 family co-repressors in plant development. , 2008, Trends in plant science.

[36]  Jukon Kim,et al.  The histone deacetylase OsHDAC1 epigenetically regulates the OsNAC6 gene that controls seedling root growth in rice. , 2009, The Plant journal : for cell and molecular biology.

[37]  E. Meyerowitz,et al.  TOPLESS Regulates Apical Embryonic Fate in Arabidopsis , 2006, Science.

[38]  R. S. Conlan,et al.  The Transcription Corepressor LEUNIG Interacts with the Histone Deacetylase HDA19 and Mediator Components MED14 (SWP) and CDK8 (HEN3) To Repress Transcription , 2007, Molecular and Cellular Biology.

[39]  K. Jung,et al.  T-DNA insertional mutagenesis for functional genomics in rice. , 2000, The Plant journal : for cell and molecular biology.

[40]  Andrea Gallavotti,et al.  The Relationship between Auxin Transport and Maize Branching1[C][W][OA] , 2008, Plant Physiology.

[41]  J. Kyozuka,et al.  Rice ABERRANT PANICLE ORGANIZATION 1, encoding an F-box protein, regulates meristem fate. , 2007, The Plant journal : for cell and molecular biology.

[42]  Thomas L. Slewinski,et al.  vanishing tassel2 Encodes a Grass-Specific Tryptophan Aminotransferase Required for Vegetative and Reproductive Development in Maize[C][W][OA] , 2011, Plant Cell.

[43]  K. Shimamoto,et al.  FRIZZY PANICLE is required to prevent the formation of axillary meristems and to establish floral meristem identity in rice spikelets , 2003, Development.

[44]  S. Hake,et al.  Flowering and determinacy in maize. , 2007, Journal of experimental botany.

[45]  Hitoshi Sakakibara,et al.  DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. , 2007, The Plant journal : for cell and molecular biology.

[46]  N. Nagasawa,et al.  A trehalose metabolic enzyme controls inflorescence architecture in maize , 2006, Nature.

[47]  Masahiko Maekawa,et al.  LAX and SPA: Major regulators of shoot branching in rice , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[48]  S. Hake,et al.  thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase , 2005, Development.

[49]  Qian Qian,et al.  Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice , 2010, Nature Genetics.

[50]  T. Laux,et al.  Analysis of the Transcription Factor WUSCHEL and Its Functional Homologue in Antirrhinum Reveals a Potential Mechanism for Their Roles in Meristem Maintenance[W] , 2006, The Plant Cell Online.

[51]  Makoto Matsuoka,et al.  OsSPL14 promotes panicle branching and higher grain productivity in rice , 2010, Nature Genetics.

[52]  R. Martienssen,et al.  ramosa2 Encodes a LATERAL ORGAN BOUNDARY Domain Protein That Determines the Fate of Stem Cells in Branch Meristems of Maize[W] , 2006, The Plant Cell Online.

[53]  Kazumasa Murata,et al.  A large-scale collection of phenotypic data describing an insertional mutant population to facilitate functional analysis of rice genes , 2006, Plant Molecular Biology.

[54]  P. McSteen.  Hormonal Regulation of Branching in Grasses12[C] , 2009, Plant Physiology.

[55]  Hong-Gyu Kang,et al.  Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. , 2006, The Plant journal : for cell and molecular biology.