Interaction of Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase with a homolog of mammalian TGF-beta receptor interacting protein.

Brassinosteroids (BRs) regulate multiple aspects of plant growth and development and require an active BRASSINOSTEROID-INSENSITIVE 1 (BRI1) receptor serine/threonine kinase for hormone perception and signal transduction. In mammals, the transforming growth factor-beta (TGF-beta) family of polypeptides modulate numerous aspects of development and are perceived at the cell surface by a complex of type I and type II TGF-beta receptor serine/threonine kinases. TGF-beta receptor interacting protein (TRIP-1) is a cytoplasmic substrate of the TGF-beta type II receptor kinase and plays a role in TGF-beta signaling. TRIP-1 is a WD domain protein that also functions as an essential subunit of the eIF3 eukaryotic translation initiation factor in animals, yeast and plants. We previously cloned putative TRIP-1 homologs from bean and Arabidopsis and found that transgenic Arabidopsis plants expressing antisense TRIP-1 RNA exhibited a broad range of developmental defects including some morphological characteristics that resemble the phenotype of BR-deficient and -insensitive mutants. We now show that the BRI1 kinase domain phosphorylates Arabidopsis TRIP-1 on three specific sites in vitro (Thr-14, Thr-89 and either Thr-197 or Ser-198). Co-immunoprecipitation experiments using antibodies against TRIP-1, BRI1 and various fusion proteins strongly suggest that TRIP-1 and BRI1 also interact directly in vivo. These findings support a role for TRIP-1 in the molecular mechanisms of BR-regulated plant growth and development, possibly as a cytoplasmic substrate of the BRI1 receptor kinase.

[1]  S. Clouse,et al.  A Brassinosteroid-Insensitive Mutant in Arabidopsis thaliana Exhibits Multiple Defects in Growth and Development , 1996, Plant physiology.

[2]  S. Clouse Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression. , 2002, Molecular cell.

[3]  C. Koncz,et al.  Brassinosteroids and Plant Steroid Hormone Signaling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001461. , 2002, The Plant Cell Online.

[4]  K. Miyazono,et al.  [TGF-beta signal transduction and Smad]. , 1997, Seikagaku. The Journal of Japanese Biochemical Society.

[5]  Zhi-Yong Wang,et al.  The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. Massagué,et al.  Mechanisms of TGF-beta signaling from cell membrane to the nucleus. , 2003, Cell.

[7]  E. Schwarz,et al.  A Phage Display Technique Identifies a Novel Regulator of Cell Differentiation* , 2003, The Journal of Biological Chemistry.

[8]  R. Gardner,et al.  A putative role for the tomato genes DUMPY and CURL-3 in brassinosteroid biosynthesis and response. , 2000, Plant physiology.

[9]  K. Browning,et al.  Plant Initiation Factor 3 Subunit Composition Resembles Mammalian Initiation Factor 3 and Has a Novel Subunit* , 2001, The Journal of Biological Chemistry.

[10]  K. Tomer,et al.  Detection and sequencing of phosphopeptides , 2000, Journal of the American Society for Mass Spectrometry.

[11]  J. Chory,et al.  A New Class of Transcription Factors Mediates Brassinosteroid-Regulated Gene Expression in Arabidopsis , 2005, Cell.

[12]  Hua Jin,et al.  Regulation of brassinosteroid signaling. , 2007, Trends in plant science.

[13]  Zhenbiao Yang,et al.  The CLAVATA1 Receptor-like Kinase Requires CLAVATA3 for Its Assembly into a Signaling Complex That Includes KAPP and a Rho-Related Protein , 1999, Plant Cell.

[14]  J. Chory,et al.  A Putative Leucine-Rich Repeat Receptor Kinase Involved in Brassinosteroid Signal Transduction , 1997, Cell.

[15]  J. Asara,et al.  Recombinant brassinosteroid insensitive 1 receptor-like kinase autophosphorylates on serine and threonine residues and phosphorylates a conserved peptide motif in vitro. , 2000, Plant physiology.

[16]  T. Kinzy,et al.  Conservation and Diversity of Eukaryotic Translation Initiation Factor eIF3* , 1997, The Journal of Biological Chemistry.

[17]  Jianming Li,et al.  BRI1/BAK1, a Receptor Kinase Pair Mediating Brassinosteroid Signaling , 2002, Cell.

[18]  Jia Li,et al.  BAK1, an Arabidopsis LRR Receptor-like Protein Kinase, Interacts with BRI1 and Modulates Brassinosteroid Signaling , 2002, Cell.

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

[20]  Ana I. Caño-Delgado,et al.  Heterodimerization and Endocytosis of Arabidopsis Brassinosteroid Receptors BRI1 and AtSERK3 (BAK1) , 2004, The Plant Cell Online.

[21]  J. Chory,et al.  BRI1 is a critical component of a plasma-membrane receptor for plant steroids , 2001, Nature.

[22]  T. Hunter,et al.  Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. , 2000, Plant physiology.

[23]  K. Browning,et al.  Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. , 2002, The Plant journal : for cell and molecular biology.

[24]  D. Goring,et al.  Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  T. Nomura,et al.  Cloning the Tomato Curl3 Gene Highlights the Putative Dual Role of the Leucine-Rich Repeat Receptor Kinase tBRI1/SR160 in Plant Steroid Hormone and Peptide Hormone Signaling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006379. , 2002, The Plant Cell Online.

[26]  Jianming Li,et al.  Regulation of Brassinosteroid Signaling by a GSK3/SHAGGY-Like Kinase , 2002, Science.

[27]  Zhi-Yong Wang,et al.  BZR1 Is a Transcriptional Repressor with Dual Roles in Brassinosteroid Homeostasis and Growth Responses , 2005, Science.

[28]  Jianming Li,et al.  Brassinosteroid Signal Transduction: A Mix of Conservation and Novelty , 2003, Journal of Plant Growth Regulation.

[29]  S. Clouse,et al.  BRASSINOSTEROIDS: Essential Regulators of Plant Growth and Development. , 1998, Annual review of plant physiology and plant molecular biology.

[30]  J. Chory,et al.  Steroid signaling in plants: from the cell surface to the nucleus , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[31]  Robert J. Schmitz,et al.  Arabidopsis Brassinosteroid-Insensitive dwarf12Mutants Are Semidominant and Defective in a Glycogen Synthase Kinase 3β-Like Kinase1 , 2002, Plant Physiology.

[32]  M. Collinge,et al.  Interaction of a protein phosphatase with an Arabidopsis serine-threonine receptor kinase. , 1994, Science.

[33]  M. Matsuoka,et al.  Loss of Function of a Rice brassinosteroid insensitive1 Homolog Prevents Internode Elongation and Bending of the Lamina Joint , 2000, Plant Cell.

[34]  R. Derynck,et al.  The Type II Transforming Growth Factor (TGF)-β Receptor-interacting Protein TRIP-1 Acts as a Modulator of the TGF-β Response* , 1998, The Journal of Biological Chemistry.

[35]  S. Rothstein,et al.  Two members of the thioredoxin-h family interact with the kinase domain of a Brassica S locus receptor kinase. , 1996, The Plant cell.

[36]  Temple F. Smith,et al.  The ancient regulatory-protein family of WD-repeat proteins , 1994, Nature.

[37]  J. Massagué,et al.  Mechanisms of TGF-β Signaling from Cell Membrane to the Nucleus , 2003, Cell.

[38]  J. Chory,et al.  Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. , 2002, Developmental cell.

[39]  R. Derynck,et al.  A WD-domain protein that is associated with and phosphorylated by the type II TGF-β receptor , 1995, Nature.

[40]  S. Clouse,et al.  Soybean BRU1 Encodes a Functional Xyloglucan Endotransglycosylase That is Highly Expressed in Inner Epicotyl Tissues during Brassinosteroid-Promoted Elongation , 1998 .

[41]  Joseph Schlessinger,et al.  Ligand-Induced, Receptor-Mediated Dimerization and Activation of EGF Receptor , 2002, Cell.

[42]  K. Feldmann,et al.  Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. , 1999, Plant physiology.

[43]  D. Chamovitz,et al.  The COP9 signalosome: from light signaling to general developmental regulation and back. , 2000, Current opinion in plant biology.

[44]  C. Heldin,et al.  Dimerization of cell surface receptors in signal transduction , 1995, Cell.

[45]  E. Winter,et al.  Arabidopsis eIF3e (INT-6) Associates with Both eIF3c and the COP9 Signalosome Subunit CSN7* , 2001, The Journal of Biological Chemistry.

[46]  Jianming Li,et al.  The Arabidopsis Transthyretin-Like Protein Is a Potential Substrate of BRASSINOSTEROID-INSENSITIVE 1 , 2004, The Plant Cell Online.

[47]  S. Clouse,et al.  Expression of a plant gene with sequence similarity to animal TGF-beta receptor interacting protein is regulated by brassinosteroids and required for normal plant development. , 2001, The Plant journal : for cell and molecular biology.

[48]  Ana I. Caño-Delgado,et al.  Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1 , 2005, Nature.

[49]  J. Chory,et al.  BES1 Accumulates in the Nucleus in Response to Brassinosteroids to Regulate Gene Expression and Promote Stem Elongation , 2002, Cell.

[50]  J. Shabanowitz,et al.  Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae , 2002, Nature Biotechnology.

[51]  T. Altmann Molecular physiology of brassinosteroids revealed by the analysis of mutants , 1999, Planta.