Arabidopsis Rho-related GTPases: differential gene expression in pollen and polar localization in fission yeast.

The Rho small GTP-binding proteins are versatile, conserved molecular switches in eukaryotic signal transduction. Plants contain a unique subfamily of Rho-GTPases called Rop (Rho-related GTPases from plants). Our previous studies involving injection of antibodies indicated that the pea Rop GTPase Rop1Ps is critical for pollen tube growth. In this study we show that overexpression of an apparent Arabidopsis ortholog of Rop1Ps, Rop1At, induces isotropic cell growth in fission yeast (Schizosaccharomyces pombe) and that green fluorescence protein-tagged Rop1At displays polar localization to the site of growth in yeast. We found that Rop1At and two other Arabidopsis Rops, Rop3At and Rop5At, are all expressed in mature pollen. All three pollen Rops fall into the same subgroup as Rop1Ps and diverge from those Rops that are not expressed in mature pollen, suggesting a coupling of the structural conservation of Rop GTPases to their gene expression in pollen. However, pollen-specific transcript accumulation for Rop1At is much higher than that for Rop3At and Rop5At. Furthermore, Rop1At is specifically expressed in anthers, whereas Rop3At and Rop5At are also expressed in vegetative tissues. In transgenic plants containing the Rop1At promoter:GUS fusion gene, GUS is specifically expressed in mature pollen and pollen tubes. We propose that Rop1At may play a predominant role in the regulation of polarized cell growth in pollen, whereas its close relatives Rop3At and Rop5At may be functionally redundant to Rop1At in pollen.

[1]  C. Wilson,et al.  A developmentally regulated MAP kinase activated by hydration in tobacco pollen. , 1997, The Plant cell.

[2]  E. Lam,et al.  Targeted disruption in Arabidopsis , 1997, Nature.

[3]  Zhenbiao Yang,et al.  Inhibition of Pollen Tube Elongation by Microinjected Anti-Rop1Ps Antibodies Suggests a Crucial Role for Rho-Type GTPases in the Control of Tip Growth. , 1997, The Plant cell.

[4]  M. Hirshberg,et al.  Rac Binding to p67 phox , 1997, The Journal of Biological Chemistry.

[5]  P. K. Hepler,et al.  POLLEN GERMINATION AND TUBE GROWTH. , 1997, Annual review of plant physiology and plant molecular biology.

[6]  D. Prasher,et al.  Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Y. M. Jin,et al.  Promoter sequences of two homologous pectin esterase genes from Chinese cabbage (Brassica campestris L. ssp. pekinensis) and pollen-specific expression of the GUS gene driven by a promoter in tobacco plants. , 1997, Molecules and cells.

[8]  P. Auvinen,et al.  Endosome dynamics regulated by a Rho protein , 1996, Nature.

[9]  A. Ridley,et al.  Rho: theme and variations , 1996, Current Biology.

[10]  S. Ramachandran,et al.  Identification of plant cytoskeletal, cell cycle-related and polarity-related proteins using Schizosaccharomyces pombe. , 1996, The Plant journal : for cell and molecular biology.

[11]  S. Ramachandran,et al.  Arabidopsis profilins are functionally similar to yeast profilins: identification of a vascular bundle-specific profilin and a pollen-specific profilin. , 1996, The Plant journal : for cell and molecular biology.

[12]  J. McDowell,et al.  The Arabidopsis thaliana ACT4/ACT12 actin gene subclass is strongly expressed throughout pollen development. , 1996, The Plant journal : for cell and molecular biology.

[13]  M. Sussman,et al.  Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[14]  S. Schmid,et al.  Regulation of receptor-mediated endocytosis by Rho and Rac , 1996, Nature.

[15]  K. Nagata,et al.  THE RHO GTPASE REGULATES PROTEIN KINASE ACTIVITY , 1996 .

[16]  J. McDowell,et al.  Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. , 1996, The Plant journal : for cell and molecular biology.

[17]  D. Larochelle,et al.  A novel member of the rho family of small GTP-binding proteins is specifically required for cytokinesis , 1996, The Journal of cell biology.

[18]  John,et al.  The Arabidopsis Profilin Gene Family (Evidence for an Ancient Split between Constitutive and Pollen-Specific Profilin Genes) , 1996, Plant physiology.

[19]  S. Gilroy,et al.  PRK1, a receptor‐like kinase of Petunia inflata, is essential for postmeiotic development of pollen , 1996 .

[20]  Zhenbiao Yang,et al.  Localization of a Rho GTPase Implies a Role in Tip Growth and Movement of the Generative Cell in Pollen Tubes. , 1996, The Plant cell.

[21]  J. McDowell,et al.  Structure and evolution of the actin gene family in Arabidopsis thaliana. , 1996, Genetics.

[22]  J. McDowell,et al.  Conserved expression of the Arabidopsis ACT1 and ACT 3 actin subclass in organ primordia and mature pollen. , 1996, The Plant cell.

[23]  K. Feldmann,et al.  Sequence-based identification of T-DNA insertion mutations in Arabidopsis: actin mutants act2-1 and act4-1. , 1995, The Plant journal : for cell and molecular biology.

[24]  R. Schilperoort,et al.  Plant Molecular Biology Manual , 1995, Springer Netherlands.

[25]  J. Chant,et al.  GTPase cascades choreographing cellular behavior: Movement, morphogenesis, and more , 1995, Cell.

[26]  C. Nobes,et al.  Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia , 1995, Cell.

[27]  L. Crossland,et al.  Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Y. Jan,et al.  Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. , 1994, Genes & development.

[29]  P. J. Miller,et al.  Cdc42p GTPase is involved in controlling polarized cell growth in Schizosaccharomyces pombe , 1994, Molecular and cellular biology.

[30]  P. Hussey,et al.  The profilin multigene family of maize: differential expression of three isoforms. , 1993, The Plant journal : for cell and molecular biology.

[31]  S. McCormick,et al.  Male Gametophyte Development. , 1993, The Plant cell.

[32]  J. P. Mascarenhas.  Molecular Mechanisms of Pollen Tube Growth and Differentiation. , 1993, The Plant cell.

[33]  J. Watson,et al.  Molecular cloning and characterization of rho, a ras-related small GTP-binding protein from the garden pea. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Forsburg.  Comparison of Schizosaccharomyces pombe expression systems. , 1993, Nucleic acids research.

[35]  P. Adamson,et al.  Intracellular localization of the P21rho proteins , 1992, The Journal of cell biology.

[36]  Anne J. Ridley,et al.  The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors , 1992, Cell.

[37]  Anne J. Ridley,et al.  The small GTP-binding protein rac regulates growth factor-induced membrane ruffling , 1992, Cell.

[38]  H. Prentice,et al.  High efficiency transformation of Schizosaccharomyces pombe by electroporation. , 1992, Nucleic acids research.

[39]  C J Marshall,et al.  A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. , 1991, The EMBO journal.

[40]  R. Wing,et al.  Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. , 1991, Genes & development.

[41]  D. Voytas,et al.  The structure, distribution and evolution of the Ta1 retrotransposable element family of Arabidopsis thaliana. , 1990, Genetics.

[42]  J. Bowman,et al.  Early flower development in Arabidopsis. , 1990, The Plant cell.

[43]  J. Mol,et al.  Pollen- and anther-specific chi promoters from petunia: tandem promoter regulation of the chiA gene. , 1990, The Plant cell.

[44]  M. Van Montagu,et al.  Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Bevan,et al.  GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants. , 1987, The EMBO journal.

[46]  L. Willmitzer,et al.  Improved method for the isolation of RNA from plant tissues. , 1987, Analytical biochemistry.

[47]  A. Coleman,et al.  Applications of fluorochromes to pollen biology. I. Mithramycin and 4',6-diamidino-2-phenylindole (DAPI) as vital stains and for quantitation of nuclear DNA. , 1985, Stain technology.

[48]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[49]  A. Hall,et al.  Small GTP-binding proteins and the regulation of the actin cytoskeleton. , 1994, Annual review of cell biology.

[50]  D. Twell.  Molecular and Cellular Aspects of Plant Reproduction: The diversity and regulation of gene expression in the pathway of male gametophyte development , 1994 .

[51]  P. Adamson,et al.  Intracellular Localization of the P 2 lrh ~ Proteins , 1992 .