DETORQUEO, QUIRKY, and ZERZAUST Represent Novel Components Involved in Organ Development Mediated by the Receptor-Like Kinase STRUBBELIG in Arabidopsis thaliana

Intercellular signaling plays an important role in controlling cellular behavior in apical meristems and developing organs in plants. One prominent example in Arabidopsis is the regulation of floral organ shape, ovule integument morphogenesis, the cell division plane, and root hair patterning by the leucine-rich repeat receptor-like kinase STRUBBELIG (SUB). Interestingly, kinase activity of SUB is not essential for its in vivo function, indicating that SUB may be an atypical or inactive receptor-like kinase. Since little is known about signaling by atypical receptor-like kinases, we used forward genetics to identify genes that potentially function in SUB-dependent processes and found recessive mutations in three genes that result in a sub-like phenotype. Plants with a defect in DETORQEO (DOQ), QUIRKY (QKY), and ZERZAUST (ZET) show corresponding defects in outer integument development, floral organ shape, and stem twisting. The mutants also show sub-like cellular defects in the floral meristem and in root hair patterning. Thus, SUB, DOQ, QKY, and ZET define the STRUBBELIG-LIKE MUTANT (SLM) class of genes. Molecular cloning of QKY identified a putative transmembrane protein carrying four C2 domains, suggesting that QKY may function in membrane trafficking in a Ca2+-dependent fashion. Morphological analysis of single and all pair-wise double-mutant combinations indicated that SLM genes have overlapping, but also distinct, functions in plant organogenesis. This notion was supported by a systematic comparison of whole-genome transcript profiles during floral development, which molecularly defined common and distinct sets of affected processes in slm mutants. Further analysis indicated that many SLM-responsive genes have functions in cell wall biology, hormone signaling, and various stress responses. Taken together, our data suggest that DOQ, QKY, and ZET contribute to SUB-dependent organogenesis and shed light on the mechanisms, which are dependent on signaling through the atypical receptor-like kinase SUB.

[1]  Jean-Pierre Métraux,et al.  EDS5, an Essential Component of Salicylic Acid–Dependent Signaling for Disease Resistance in Arabidopsis, Is a Member of the MATE Transporter Family Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010376. , 2002, The Plant Cell Online.

[2]  K. Mayer,et al.  Endothelial Lipase: A New Risk Factor for Atherosclerosis? , 2005, PLoS Medicine.

[3]  D. McCarty,et al.  CRINKLY4: A TNFR-Like Receptor Kinase Involved in Maize Epidermal Differentiation , 1996, Science.

[4]  Bryan C Thines,et al.  JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling , 2007, Nature.

[5]  K. Yamaguchi-Shinozaki,et al.  A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. , 1996, The Plant cell.

[6]  C. Koncz,et al.  The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector , 1986, Molecular and General Genetics MGG.

[7]  T. Mengiste,et al.  Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. , 2006, The Plant journal : for cell and molecular biology.

[8]  Xiufeng Yan,et al.  Regulation of plant glucosinolate metabolism , 2007, Planta.

[9]  M. Hülskamp,et al.  Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana. , 1997, Development.

[10]  Xinnian Dong,et al.  NPR1, all things considered. , 2004, Current opinion in plant biology.

[11]  E. Meyerowitz,et al.  CLAVATA1, a regulator of meristem and flower development in Arabidopsis. , 1993, Development.

[12]  S. Abel,et al.  Glucosinolate metabolism and its control. , 2006, Trends in plant science.

[13]  P. Benfey,et al.  Not just another hole in the wall: understanding intercellular protein trafficking. , 2005, Genes & development.

[14]  N. Raikhel,et al.  Trehalose-6-Phosphate Synthase/Phosphatase Regulates Cell Shape and Plant Architecture in Arabidopsis1[W][OA] , 2007, Plant Physiology.

[15]  G. Ingram.  Between the sheets: inter-cell-layer communication in plant development. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  S. Ward,et al.  A nematode gene required for sperm vesicle fusion. , 1997, Journal of cell science.

[17]  F. Ausubel,et al.  Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[18]  B. G. Hansen,et al.  Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Jonathan D. G. Jones,et al.  EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R. Amasino,et al.  A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment , 1998, Plant Molecular Biology.

[21]  E. Chapman,et al.  The C2 domains of synaptotagmin--partners in exocytosis. , 2004, Trends in biochemical sciences.

[22]  J. Beckmann,et al.  A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B , 1998, Nature Genetics.

[23]  A. Krogh,et al.  Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. , 2001, Journal of molecular biology.

[24]  P. Mcneil,et al.  Plasma membrane disruption: repair, prevention, adaptation. , 2003, Annual review of cell and developmental biology.

[25]  S. Davis.  Faculty Opinions recommendation of Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. , 2006 .

[26]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

[27]  V. Irish,et al.  Regulation of cell proliferation patterns by homeotic genes during Arabidopsis floral development. , 2000, Development.

[28]  K. Ljung,et al.  The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Synan F. AbuQamar,et al.  Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. , 2006, The Plant journal : for cell and molecular biology.

[30]  T. Südhof,et al.  Evolutionarily Conserved Multiple C2 Domain Proteins with Two Transmembrane Regions (MCTPs) and Unusual Ca2+ Binding Properties* , 2005, Journal of Biological Chemistry.

[31]  Z. He,et al.  Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. , 1998, The Plant journal : for cell and molecular biology.

[32]  T. Südhof,et al.  Synaptotagmin I functions as a calcium regulator of release probability , 2001, Nature.

[33]  T. Eulgem,et al.  Networks of WRKY transcription factors in defense signaling. , 2007, Current opinion in plant biology.

[34]  Chien-Chang Chen,et al.  Defective membrane repair in dysferlin-deficient muscular dystrophy , 2003, Nature.

[35]  J. Meldolesi,et al.  Regulated exocytosis: new organelles for non-secretory purposes , 2005, Nature Reviews Molecular Cell Biology.

[36]  J. Meldolesi,et al.  Enlargeosome Traffic: Exocytosis Triggered by Various Signals Is Followed by Endocytosis, Membrane Shedding or Both , 2007, Traffic.

[37]  B. Halkier,et al.  Cytochrome P450 CYP79B2 from Arabidopsis Catalyzes the Conversion of Tryptophan to Indole-3-acetaldoxime, a Precursor of Indole Glucosinolates and Indole-3-acetic Acid* , 2000, The Journal of Biological Chemistry.

[38]  A. K. Grennan.  The Role of Trehalose Biosynthesis in Plants , 2007, Plant Physiology.

[39]  H. Goodman,et al.  Cloning and chromosomal mapping of nuclear genes encoding chloroplast and cytosolic glyceraldehyde-3-phosphate-dehydrogenase from Arabidopsis thaliana. , 1991, Gene.

[40]  C. Gatz,et al.  Interaction of NIMIN1 with NPR1 Modulates PR Gene Expression in Arabidopsis , 2005, The Plant Cell Online.

[41]  R. Yadav,et al.  STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  B. Bartel,et al.  Characterization of a Family of IAA-Amino Acid Conjugate Hydrolases from Arabidopsis* , 2002, The Journal of Biological Chemistry.

[43]  K. Akiyama,et al.  Functional Annotation of a Full-Length Arabidopsis cDNA Collection , 2002, Science.

[44]  Frederick M. Ausubel,et al.  Isochorismate synthase is required to synthesize salicylic acid for plant defence , 2001, Nature.

[45]  E. Caler,et al.  Plasma Membrane Repair Is Mediated by Ca2+-Regulated Exocytosis of Lysosomes , 2001, Cell.

[46]  A. Blakeslee,et al.  Demonstration of the three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras , 1940 .

[47]  M. Frohman,et al.  Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[48]  A. Gleave.  A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome , 1992, Plant Molecular Biology.

[49]  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.

[50]  R. Last,et al.  Arabidopsis Map-Based Cloning in the Post-Genome Era , 2002, Plant Physiology.

[51]  D. Galbraith,et al.  CYP83B1, a Cytochrome P450 at the Metabolic Branch Point in Auxin and Indole Glucosinolate Biosynthesis in Arabidopsis , 2001, Plant Cell.

[52]  Yuji Kohara,et al.  Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi , 2001, Current Biology.

[53]  J. Meldolesi,et al.  Regulated exocytosis: a novel, widely expressed system , 2002, Nature Cell Biology.

[54]  Joanne Chory,et al.  The epidermis both drives and restricts plant shoot growth , 2007, Nature.

[55]  R. Shen,et al.  Positional Signaling Mediated by a Receptor-like Kinase in Arabidopsis , 2005, Science.

[56]  Z. Peng,et al.  Reciprocal regulation of Δ1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants , 1996, Molecular and General Genetics MGG.

[57]  J. Thevelein,et al.  An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. , 2001, Trends in plant science.

[58]  T. Eulgem,et al.  Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. , 2007, Molecular plant-microbe interactions : MPMI.

[59]  Martin Frenz,et al.  Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem , 2003, Development.

[60]  A. Tunnacliffe,et al.  LEA proteins prevent protein aggregation due to water stress. , 2005, The Biochemical journal.

[61]  Teva Vernoux,et al.  An Evolutionarily Conserved Mechanism Delimiting SHR Movement Defines a Single Layer of Endodermis in Plants , 2007, Science.

[62]  Jing Li,et al.  The WRKY70 Transcription Factor: A Node of Convergence for Jasmonate-Mediated and Salicylate-Mediated Signals in Plant Defense On-line version contains Web-only data. , 2004, The Plant Cell Online.

[63]  J. Casacuberta,et al.  Signalling through kinase-defective domains: the prevalence of atypical receptor-like kinases in plants. , 2007, Journal of experimental botany.

[64]  Christopher Johnson,et al.  Salicylic Acid and NPR1 Induce the Recruitment of trans-Activating TGA Factors to a Defense Gene Promoter in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012211. , 2003, The Plant Cell Online.

[65]  J. Micol,et al.  The JAZ family of repressors is the missing link in jasmonate signalling , 2007, Nature.

[66]  J. Parker,et al.  Plant immunity: the EDS1 regulatory node. , 2005, Current opinion in plant biology.

[67]  S. Shiu,et al.  Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[68]  W. J. Lucas,et al.  Selective Trafficking of KNOTTED1 Homeodomain Protein and Its mRNA Through Plasmodesmata , 1995, Science.

[69]  J. Celenza,et al.  Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[70]  W. Aufsatz,et al.  The ECS1 gene of Arabidopsis encodes a plant cell wall-associated protein and is potentially linked to a locus influencing resistance to Xanthomonas campestris , 1998, Plant Molecular Biology.

[71]  J. Glazebrook,et al.  Arabidopsis Cytochrome P450 Monooxygenase 71A13 Catalyzes the Conversion of Indole-3-Acetaldoxime in Camalexin Synthesis[W] , 2007, The Plant Cell Online.

[72]  T. Südhof,et al.  Synaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse , 1994, Cell.

[73]  T. Steeves,et al.  Patterns in plant development: Subject index , 1972 .

[74]  F. Nagy,et al.  Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter , 1985, Nature.

[75]  R W Innes,et al.  The GH3 Acyl Adenylase Family Member PBS3 Regulates Salicylic Acid-Dependent Defense Responses in Arabidopsis1[W][OA] , 2007, Plant Physiology.

[76]  Lucio Conti,et al.  TERMINAL FLOWER1 Is a Mobile Signal Controlling Arabidopsis Architecture[W] , 2007, The Plant Cell Online.

[77]  Toshihiro Tanaka,et al.  Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis , 2007, Development.

[78]  S. Driscoll,et al.  Yeast complementation reveals a role for an Arabidopsis thaliana late embryogenesis abundant (LEA)-like protein in oxidative stress tolerance. , 2006, The Plant journal : for cell and molecular biology.

[79]  The maize CRINKLY4 receptor kinase controls a cell-autonomous differentiation response. , 2001, Plant physiology.

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

[81]  C. Carter,et al.  Arabidopsis thaliana contains a large family of germin-like proteins: characterization of cDNA and genomic sequences encoding 12 unique family members , 1998, Plant Molecular Biology.

[82]  K. Campbell,et al.  Dysferlin and the plasma membrane repair in muscular dystrophy. , 2004, Trends in cell biology.

[83]  M. Gifford,et al.  The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development , 2003, Development.

[84]  J. Schiefelbein,et al.  The role of the SCRAMBLED receptor-like kinase in patterning the Arabidopsis root epidermis. , 2007, Developmental biology.

[85]  H. Saedler,et al.  Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. , 1996, Development.

[86]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[87]  Ramesh Raina,et al.  Arabidopsis GH3-LIKE DEFENSE GENE 1 is required for accumulation of salicylic acid, activation of defense responses and resistance to Pseudomonas syringae. , 2007, The Plant journal : for cell and molecular biology.

[88]  M. Van Montagu,et al.  Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[89]  Sandra Pelletier,et al.  A Receptor-like Kinase Mediates the Response of Arabidopsis Cells to the Inhibition of Cellulose Synthesis , 2007, Current Biology.

[90]  T. Südhof.  Synaptotagmins: Why So Many?* , 2002, The Journal of Biological Chemistry.

[91]  G. Ingram,et al.  Keeping it together: co-ordinating plant growth. , 2006, Current opinion in plant biology.

[92]  S. Ward,et al.  FER-1 regulates Ca2+-mediated membrane fusion during C. elegans spermatogenesis , 2006, Journal of Cell Science.

[93]  E. M. Meyerowitz,et al.  Arabidopsis thaliana , 2022, CABI Compendium.

[94]  T. Südhof,et al.  E-Syts, a family of membranous Ca2+-sensor proteins with multiple C2 domains , 2007, Proceedings of the National Academy of Sciences.

[95]  B. Hyman,et al.  Dysferlin Interacts with Annexins A1 and A2 and Mediates Sarcolemmal Wound-healing* , 2003, Journal of Biological Chemistry.

[96]  S M Burgess,et al.  beta-Glucuronidase from Escherichia coli as a gene-fusion marker. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[97]  Y. Machida,et al.  The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[98]  D. Jackson.  Double Labeling of KNOTTED1 mRNA and Protein Reveals Multiple Potential Sites of Protein Trafficking in the Shoot Apex1 , 2002, Plant Physiology.

[99]  K. Shinozaki,et al.  A gene encoding proline dehydrogenase is not only induced by proline and hypoosmolarity, but is also developmentally regulated in the reproductive organs of Arabidopsis. , 1998, Plant physiology.

[100]  L. Sieburth,et al.  Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. , 1997, The Plant cell.

[101]  L. Williams,et al.  Stem cell regulation in the Arabidopsis shoot apical meristem. , 2005, Current opinion in plant biology.

[102]  R. Yadav,et al.  The Arabidopsis receptor-like kinase STRUBBELIG mediates inter-cell-layer signaling during floral development. , 2008, Developmental biology.

[103]  Pieter J. de Jong,et al.  Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy , 1998, Nature Genetics.

[104]  J. Glazebrook,et al.  Arabidopsis PAD3, a Gene Required for Camalexin Biosynthesis, Encodes a Putative Cytochrome P450 Monooxygenase , 1999, Plant Cell.

[105]  N. Amornsiripanitch,et al.  A Genomic Approach to Identify Regulatory Nodes in the Transcriptional Network of Systemic Acquired Resistance in Plants , 2006, PLoS pathogens.

[106]  B. Halkier,et al.  CYP71B15 (PAD3) Catalyzes the Final Step in Camalexin Biosynthesis1 , 2006, Plant Physiology.

[107]  G. Fink,et al.  ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. , 1995, Science.

[108]  R. Steele,et al.  Deceiving appearances: signaling by “dead” and “fractured” receptor protein‐tyrosine kinases , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[109]  K. Keegstra,et al.  Biosynthesis of plant cell wall polysaccharides - a complex process. , 2006, Current opinion in plant biology.

[110]  Rafael A. Irizarry,et al.  A Model-Based Background Adjustment for Oligonucleotide Expression Arrays , 2004 .

[111]  S. Potter,et al.  Acquired resistance in Arabidopsis. , 1992, The Plant cell.

[112]  Detlef Weigel,et al.  Dissection of floral induction pathways using global expression analysis , 2003, Development.

[113]  J. Glazebrook.  Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. , 2005, Annual review of phytopathology.

[114]  I. Sussex,et al.  WHAT CHIMERAS CAN TELL US ABOUT PLANT DEVELOPMENT. , 1996, Annual review of plant physiology and plant molecular biology.

[115]  J. Schiefelbein,et al.  The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. , 1996, Development.

[116]  P. Benfey,et al.  Intercellular movement of the putative transcription factor SHR in root patterning , 2001, Nature.

[117]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[118]  B. Usadel,et al.  The inositol oxygenase gene family of Arabidopsis is involved in the biosynthesis of nucleotide sugar precursors for cell-wall matrix polysaccharides , 2005, Planta.

[119]  Kentaro Inoue,et al.  Arabidopsis Isochorismate Synthase Functional in Pathogen-induced Salicylate Biosynthesis Exhibits Properties Consistent with a Role in Diverse Stress Responses* , 2007, Journal of Biological Chemistry.

[120]  T. Südhof,et al.  C2-domains, Structure and Function of a Universal Ca2+-binding Domain* , 1998, The Journal of Biological Chemistry.

[121]  A. Blakeslee,et al.  PERICLINAL CHIMERAS IN DATURA STRAMONIUM IN RELATION TO DEVELOPMENT OF LEAF AND FLOWER , 1941 .

[122]  Jean YH Yang,et al.  Bioconductor: open software development for computational biology and bioinformatics , 2004, Genome Biology.

[123]  C. A. Thomas,et al.  Molecular cloning. , 1977, Advances in pathobiology.

[124]  E. T. Palva,et al.  WRKY70 modulates the selection of signaling pathways in plant defense. , 2006, The Plant journal : for cell and molecular biology.

[125]  S. Satina.  PERICLINAL CHIMERAS IN DATURA IN RELATION TO THE DEVELOPMENT AND STRUCTURE OF THE OVULE , 1945 .

[126]  H. Sondermann,et al.  C2 Can Do It, Too , 2005, Cell.

[127]  Mark Zander,et al.  SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. , 2007, The Plant journal : for cell and molecular biology.

[128]  F. Rolland,et al.  Plant development: introducing trehalose metabolism. , 2007, Trends in plant science.