Changes in the expression pattern of OsWUS negatively regulate plant stature and panicle development in rice

Abstract WUSCHEL (WUS) and WUSCHEL-RELATED HOMEOBOX (WOX) encode transcription factors and play important roles in regulating the formation and maintenance of shoot and floral meristems. OsWUS have distinct functions in meristem development with slightly tuned expression. However, the mechanisms regulating the specific expression of OsWUS need to be further explored. In this study, an abnormal expression mutant of OsWUS, called Dwarf and aberrant panicle 1 (Dap1) was used. In order to identify the causal gene in Dap1, high-efficiency thermal asymmetric interlaced (hiTAIL)-PCR and co-segregation analysis were performed. We surveyed the growth and yield traits in Dap1 and wild type. Changes in gene expression between Dap1 and wild type were determined by RNA-seq. The Dap1 mutant is due to the T-DNA inserted at 3,628-bp upstream of the translation start codon of OsWUS. Plant height, tiller numbers, panicle length, the number of grains per main panicle, and the number of secondary branches was significantly reduced in the Dap1 mutant. The expression of OsWUS was markedly increased in Dap1 mutant plants compared to the wild type, which might be due to a disruption in the genomic sequence integrity. Simultaneously, the expression levels of gibberellic acid-related genes and genes involved in panicle development were significantly changed in the Dap1 mutant. Our results suggest that OsWUS is a precise regulatory element, its specific spatio-temporal expression pattern is critical for its function, and both loss-of-function and gain-of-function mutations lead to abnormal plant growth.

[1]  Liu Yang,et al.  Rice SEPALLATA Genes OsMADS5 and OsMADS34 Cooperate to Limit Inflorescence Branching by Repressing the TERMINAL FLOWER1-like Gene RCN4. , 2021, The New phytologist.

[2]  M. Galli,et al.  Structural variation at the maize WUSCHEL1 locus alters stem cell organization in inflorescences , 2021, Nature Communications.

[3]  Changyin Wu,et al.  Phosphorylation of OsFD1 by OsCIPK3 Promotes the Formation of RFT1-containing Florigen Activation Complex for Long-day Flowering in Rice. , 2021, Molecular plant.

[4]  Xu-dong Zhu,et al.  OsWUS promotes tiller bud growth by establishing weak apical dominance in rice. , 2020, The Plant journal : for cell and molecular biology.

[5]  H. Hirano,et al.  Antagonistic action of TILLERS ABSENT1 and FLORAL ORGAN NUMBER2 regulates stem cell maintenance during axillary meristem development in rice. , 2019, The New phytologist.

[6]  Zefu Lu,et al.  Tiller Bud Formation Regulators MOC1 and MOC3 Cooperatively Promote Tiller Bud Outgrowth by Activating FON1 Expression in Rice. , 2019, Molecular plant.

[7]  Guifu Liu,et al.  Strigolactone promotes cytokinin degradation through transcriptional activation of CYTOKININ OXIDASE/DEHYDROGENASE 9 in rice , 2019, Proceedings of the National Academy of Sciences.

[8]  Jinmi Yoon,et al.  Overexpression of RICE FLOWERING LOCUS T 1 (RFT1) Induces Extremely Early Flowering in Rice , 2019, Molecules and cells.

[9]  Qinlong Zhu,et al.  The Intronic cis Element SE1 Recruits trans-Acting Repressor Complexes to Repress the Expression of ELONGATED UPPERMOST INTERNODE1 in Rice. , 2018, Molecular plant.

[10]  Caihuan Tian,et al.  Cytokinin Signaling Activates WUSCHEL Expression during Axillary Meristem Initiation[OPEN] , 2017, Plant Cell.

[11]  Yan Zheng,et al.  Homeobox Is Pivotal for OsWUS Controlling Tiller Development and Female Fertility in Rice , 2016, G3: Genes, Genomes, Genetics.

[12]  S. Kawano,et al.  Axillary Meristem Formation in Rice Requires the WUSCHEL Ortholog TILLERS ABSENT1[OPEN] , 2015, Plant Cell.

[13]  H. Matsumura,et al.  A cytochrome P450, OsDSS1, is involved in growth and drought stress responses in rice (Oryza sativa L.) , 2015, Plant Molecular Biology.

[14]  H. Matsumura,et al.  A cytochrome P450, OsDSS1, is involved in growth and drought stress responses in rice (Oryza sativa L.) , 2015, Plant Molecular Biology.

[15]  Zefu Lu,et al.  MONOCULM 3, an ortholog of WUSCHEL in rice, is required for tiller bud formation. , 2015, Journal of genetics and genomics = Yi chuan xue bao.

[16]  Chuanyou Li,et al.  The Rice Semi-Dwarf Mutant sd37, Caused by a Mutation in CYP96B4, Plays an Important Role in the Fine-Tuning of Plant Growth , 2014, PloS one.

[17]  Chengcai Chu,et al.  The rice GERMINATION DEFECTIVE 1, encoding a B3 domain transcriptional repressor, regulates seed germination and seedling development by integrating GA and carbohydrate metabolism , 2013, The Plant journal : for cell and molecular biology.

[18]  H. Yoshida,et al.  Inflorescence Meristem Identity in Rice Is Specified by Overlapping Functions of Three AP1/FUL-Like MADS Box Genes and PAP2, a SEPALLATA MADS Box Gene[C][W] , 2012, Plant Cell.

[19]  S. Ramachandran,et al.  Oryza sativa Cytochrome P450 Family Member OsCYP96B4 Reduces Plant Height in a Transcript Dosage Dependent Manner , 2011, PloS one.

[20]  Henrik Jönsson,et al.  WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. , 2011, Genes & development.

[21]  Qian Qian,et al.  Short panicle1 encodes a putative PTR family transporter and determines rice panicle size. , 2009, The Plant journal : for cell and molecular biology.

[22]  C. Beveridge,et al.  Roles for Auxin, Cytokinin, and Strigolactone in Regulating Shoot Branching1[C][W][OA] , 2009, Plant Physiology.

[23]  Su-May Yu,et al.  A Novel Class of Gibberellin 2-Oxidases Control Semidwarfism, Tillering, and Root Development in Rice[W] , 2008, The Plant Cell Online.

[24]  Lei Wang,et al.  Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice , 2008, Nature Genetics.

[25]  G. An,et al.  Rice SVP-group MADS-box proteins, OsMADS22 and OsMADS55, are negative regulators of brassinosteroid responses. , 2008, The Plant journal : for cell and molecular biology.

[26]  Yaoguang Liu,et al.  High-efficiency thermal asymmetric interlaced PCR for amplification of unknown flanking sequences. , 2007, BioTechniques.

[27]  Q. Qian,et al.  Genetic and Molecular Analysis of Utility of sd1 Alleles in Rice Breeding , 2007 .

[28]  W. Werr,et al.  The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. , 2006, Molecular biology and evolution.

[29]  Nori Kurata,et al.  Identification and characterization of cytokinin-signalling gene families in rice. , 2006, Gene.

[30]  Qian Qian,et al.  EUI1, encoding a putative cytochrome P450 monooxygenase, regulates internode elongation by modulating gibberellin responses in rice. , 2006, Plant & cell physiology.

[31]  T. Sun,et al.  A DELLAcate balance: the role of gibberellin in plant morphogenesis. , 2005, Current opinion in plant biology.

[32]  H. Yoshida,et al.  A role of OsGA20ox1, encoding an isoform of gibberellin 20-oxidase, for regulation of plant stature in rice , 2004, Plant Molecular Biology.

[33]  G. An,et al.  Functional Analyses of the ¯owering Time Gene Osmads50, the Putative Suppressor of Overexpression of Co 1/ Agamous-like 20 (soc1/agl20) Ortholog in Rice , 1976 .

[34]  M. Ellis,et al.  Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  G. S. Khush,et al.  Green revolution: A mutant gibberellin-synthesis gene in rice , 2002, Nature.

[36]  K. Shimamoto,et al.  Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. , 2002, The Plant journal : for cell and molecular biology.

[37]  D. Weigel,et al.  A Molecular Link between Stem Cell Regulation and Floral Patterning in Arabidopsis , 2001, Cell.

[38]  M. Lenhard,et al.  Termination of Stem Cell Maintenance in Arabidopsis Floral Meristems by Interactions between WUSCHEL and AGAMOUS , 2001, Cell.

[39]  M. Hobe,et al.  Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. , 2000, Science.

[40]  S. Yamaguchi,et al.  Gibberellin biosynthesis: its regulation by endogenous and environmental signals. , 2000, Plant & cell physiology.

[41]  C. Somerville,et al.  PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Heiko Schoof,et al.  Role of WUSCHEL in Regulating Stem Cell Fate in the Arabidopsis Shoot Meristem , 1998, Cell.

[43]  D W Nebert,et al.  P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature. , 1996, Pharmacogenetics.

[44]  K. Fellows,et al.  The significance of right aortic arch in D-transposition of the great arteries. , 1974, American heart journal.

[45]  Zhukuan Cheng,et al.  Activation of gibberellin 2-oxidase 6 decreases active gibberellin levels and creates a dominant semi-dwarf phenotype in rice (Oryza sativa L.). , 2010, Journal of genetics and genomics = Yi chuan xue bao.

[46]  Yoshihiro Ugawa,et al.  Plant cis-acting regulatory DNA elements (PLACE) database: 1999 , 1999, Nucleic Acids Res..

[47]  G. Jürgens,et al.  The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. , 1996, Development.