The U-Box E3 Ubiquitin Ligase TUD1 Functions with a Heterotrimeric G α Subunit to Regulate Brassinosteroid-Mediated Growth in Rice

Heterotrimeric G proteins are an important group of signaling molecules found in eukaryotes. They function with G-protein-coupled-receptors (GPCRs) to transduce various signals such as steroid hormones in animals. Nevertheless, their functions in plants are not well-defined. Previous studies suggested that the heterotrimeric G protein α subunit known as D1/RGA1 in rice is involved in a phytohormone gibberellin-mediated signaling pathway. Evidence also implicates D1 in the action of a second phytohormone Brassinosteroid (BR) and its pathway. However, it is unclear how D1 functions in this pathway, because so far no partner has been identified to act with D1. In this study, we report a D1 genetic interactor Taihu Dwarf1 (TUD1) that encodes a functional U-box E3 ubiquitin ligase. Genetic, phenotypic, and physiological analyses have shown that tud1 is epistatic to d1 and is less sensitive to BR treatment. Histological observations showed that the dwarf phenotype of tud1 is mainly due to decreased cell proliferation and disorganized cell files in aerial organs. Furthermore, we found that D1 directly interacts with TUD1. Taken together, these results demonstrate that D1 and TUD1 act together to mediate a BR-signaling pathway. This supports the idea that a D1-mediated BR signaling pathway occurs in rice to affect plant growth and development.

[1]  J. Botella Can heterotrimeric G proteins help to feed the world? , 2012, Trends in plant science.

[2]  Shin-Han Shiu,et al.  Characterization of Genes Involved in Cytokinin Signaling and Metabolism from Rice1[W][OA] , 2012, Plant Physiology.

[3]  Y. Iwasaki,et al.  Suppression of the rice heterotrimeric G protein β-subunit gene, RGB1, causes dwarfism and browning of internodes and lamina joint regions. , 2011, The Plant journal : for cell and molecular biology.

[4]  J. Chai,et al.  Structural insight into brassinosteroid perception by BRI1 , 2011, Nature.

[5]  Lei Li,et al.  Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways. , 2011, Journal of integrative plant biology.

[6]  H. Hamm,et al.  Interaction of a G protein with an activated receptor opens the interdomain interface in the alpha subunit , 2011, Proceedings of the National Academy of Sciences.

[7]  S. Clouse Brassinosteroid Signal Transduction: From Receptor Kinase Activation to Transcriptional Networks Regulating Plant Development , 2011, Plant Cell.

[8]  M. Aluru,et al.  A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. , 2011, The Plant journal : for cell and molecular biology.

[9]  Zhi-Yong Wang,et al.  Brassinosteroid signal transduction from receptor kinases to transcription factors. , 2010, Annual review of plant biology.

[10]  R. Vierstra The ubiquitin–26S proteasome system at the nexus of plant biology , 2009, Nature Reviews Molecular Cell Biology.

[11]  Qian Qian,et al.  Natural variation at the DEP1 locus enhances grain yield in rice , 2009, Nature Genetics.

[12]  D. Goring,et al.  The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. , 2009, Journal of experimental botany.

[13]  H. Kitano,et al.  Study of novel d1 alleles, defective mutants of the α subunit of heterotrimeric G-protein in rice , 2009 .

[14]  J. Kudla,et al.  Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. , 2008, The Plant journal : for cell and molecular biology.

[15]  J. Gough,et al.  Classification, expression pattern, and E3 ligase activity assay of rice U-box-containing proteins. , 2008, Molecular plant.

[16]  W. Kim,et al.  Arabidopsis PUB22 and PUB23 Are Homologous U-Box E3 Ubiquitin Ligases That Play Combinatory Roles in Response to Drought Stress[W] , 2008, The Plant Cell Online.

[17]  Jin‐Gui Chen,et al.  Loss-of-function mutations in the Arabidopsis heterotrimeric G-protein alpha subunit enhance the developmental defects of brassinosteroid signaling and biosynthesis mutants. , 2008, Plant & cell physiology.

[18]  Jin‐Gui Chen Heterotrimeric G-proteins in plant development. , 2008, Frontiers in bioscience : a journal and virtual library.

[19]  K. Chong,et al.  Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice , 2007, Proceedings of the National Academy of Sciences.

[20]  Alan M. Jones,et al.  The plant heterotrimeric G-protein complex. , 2007, Annual review of plant biology.

[21]  Lei Wang,et al.  Heterotrimeric G protein α subunit is involved in rice brassinosteroid response , 2006, Cell Research.

[22]  Alan M. Jones,et al.  Differential Roles of Arabidopsis Heterotrimeric G-Protein Subunits in Modulating Cell Division in Roots1[W] , 2006, Plant Physiology.

[23]  Bin Han,et al.  GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein , 2006, Theoretical and Applied Genetics.

[24]  Y. Kamiya,et al.  ELONGATED UPPERMOST INTERNODE Encodes a Cytochrome P450 Monooxygenase That Epoxidizes Gibberellins in a Novel Deactivation Reaction in Rice[W] , 2006, The Plant Cell Online.

[25]  Masatomo Kobayashi,et al.  Dissection of the phosphorylation of rice DELLA protein, SLENDER RICE1. , 2005, Plant & cell physiology.

[26]  Jennifer Moon,et al.  The Ubiquitin-Proteasome Pathway and Plant Development , 2004, The Plant Cell Online.

[27]  Alan M. Jones,et al.  Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. , 2004, Current opinion in plant biology.

[28]  H. Leung,et al.  Spotted leaf11, a Negative Regulator of Plant Cell Death and Defense, Encodes a U-Box/Armadillo Repeat Protein Endowed with E3 Ubiquitin Ligase Activityw⃞ , 2004, The Plant Cell Online.

[29]  N. Chua,et al.  Structure and Biochemical Function of a Prototypical Arabidopsis U-box Domain* , 2004, Journal of Biological Chemistry.

[30]  Junli Zhou,et al.  The F-Box Protein AhSLF-S2 Controls the Pollen Function of S-RNase–Based Self-Incompatibility , 2004, The Plant Cell Online.

[31]  H. Kumagai,et al.  Characterization of heterotrimeric G protein complexes in rice plasma membrane. , 2004, The Plant journal : for cell and molecular biology.

[32]  G. Bishop Brassinosteroid Mutants of Crops , 2003, Journal of Plant Growth Regulation.

[33]  Z. Hong,et al.  A Rice Brassinosteroid-Deficient Mutant, ebisu dwarf (d2), Is Caused by a Loss of Function of a New Member of Cytochrome P450 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014712. , 2003, The Plant Cell Online.

[34]  J. B. Reid,et al.  The LKA gene is a BRASSINOSTEROID INSENSITIVE 1 homolog of pea. , 2003, The Plant journal : for cell and molecular biology.

[35]  K. Yoneyama,et al.  A Semidwarf Phenotype of Barley uzu Results from a Nucleotide Substitution in the Gene Encoding a Putative Brassinosteroid Receptor , 2003, Plant Physiology.

[36]  R. Mullen,et al.  ARC1 Is an E3 Ubiquitin Ligase and Promotes the Ubiquitination of Proteins during the Rejection of Self-Incompatible Brassica Pollen Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009845. , 2003, The Plant Cell Online.

[37]  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.

[38]  Yukihisa Shimada,et al.  Loss-of-function of a rice brassinosteroid biosynthetic enzyme, C-6 oxidase, prevents the organized arrangement and polar elongation of cells in the leaves and stem. , 2002, The Plant journal : for cell and molecular biology.

[39]  K. Shimamoto,et al.  The heterotrimeric G protein α subunit acts upstream of the small GTPase Rac in disease resistance of rice , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  N. Chua,et al.  SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals , 2002, Nature.

[41]  S. Assmann Heterotrimeric and Unconventional GTP Binding Proteins in Plant Cell Signaling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001792. , 2002, The Plant Cell Online.

[42]  S. Prat,et al.  Gibberellins Signal Nuclear Import of PHOR1, a Photoperiod-Responsive Protein with Homology to Drosophila armadillo , 2001, Cell.

[43]  K. Shirasu,et al.  The U-box protein family in plants. , 2001, Trends in plant science.

[44]  M. Matsuoka,et al.  slender Rice, a Constitutive Gibberellin Response Mutant, Is Caused by a Null Mutation of the SLR1 Gene, an Ortholog of the Height-Regulating Gene GAI/RGA/RHT/D8 , 2001, Plant Cell.

[45]  M. Matsuoka,et al.  Rice dwarf mutant d1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  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.

[47]  T. Komari,et al.  Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. , 1994, The Plant journal : for cell and molecular biology.

[48]  K. Mori,et al.  Brassinolide and homobrassinolide promotion of lamina inclination of rice seedlings , 1981 .

[49]  K. Takeda Internode elongation and dwarfism in some gramineous plants , 1979 .

[50]  Chengcai Chu,et al.  Brassinosteroid signaling and application in rice. , 2012, Journal of genetics and genomics = Yi chuan xue bao.

[51]  M. Mori,et al.  Brassinosteroid signaling in rice , 2011 .

[52]  Shamsul Hayat,et al.  Brassinosteroids: A Class of Plant Hormone , 2010 .

[53]  H. Kitano,et al.  Study of novel d1 alleles, defective mutants of the alpha subunit of heterotrimeric G-protein in rice. , 2009, Genes & genetic systems.

[54]  H. Kitano,et al.  Function of the alpha subunit of rice heterotrimeric G protein in brassinosteroid signaling. , 2009, Plant & cell physiology.

[55]  K. Chong,et al.  Heterotrimeric G protein alpha subunit is involved in rice brassinosteroid response. , 2006, Cell research.

[56]  M. Matsuoka,et al.  Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice , 2006, Nature Biotechnology.