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AtRabD2b, a Functional Ortholog of the Yeast Ypt1, Controls Various Growth and Developmental Processes in Arabidopsis

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Abstract

Rab1-related guanosine-5′-triphosphatases (GTPases) regulate the intracellular endoplasmic reticulum (ER)-to-Golgi vesicle transport in yeast, mammalian and plant systems. Arabidopsis contains four Rab1 GTPases which are further divided into two functionally distinct subclasses, RabD1 and RabD2. In this study, we investigated the function of an Arabidopsis RabD2b gene. Yeast complementary assay demonstrated that AtRabD2b is a functional counterpart of the yeast Ypt1. The active GTP-bound mutant (AtRabD2b [Q67L]) maintained the complementary ability of ypt1 mutant as wild-type AtRabD2b. Both AtRabD2b and AtRabD2b [Q67L] localize on the Golgi stacks and a second subpopulation of punctate structures in tobacco leaf cells. RT-PCR assay showed that AtRabD2b is ubiquitously expressed in different plant tissues. Transgenic plants overexpressing yellow fluorescent protein (YFP)-AtRabD2b [Q67L] fusion gene exhibited dwarfism, altered morphology of rosette leaves, and upward-pointing siliques in the stems. The downregulation of AtRabD1, AtRabD2b, and AtRabD2c, due to cosuppression of the AtRabD2b gene in the YFP-AtRabD2b [Q67L] transgenic plants, resulted in stunted bushy growth phenotype, very low fertility, and the necrosis at the apical region of the stem. Together, these data indicated that AtRabD2b gene regulates the ER-to-Golgi membrane trafficking as Ypt1 and plays a role in several aspects of plant growth and development.

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References

  • Agarwal P, Reddy MK, Sopory SK, Agarwal PK (2009) Plant rabs: characterization, functional diversity, and role in stress tolerance. Plant Mol Biol Rep 27:417–430

    Article  CAS  Google Scholar 

  • Batoko H, Zheng HQ, Hawes C, Moore I (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12:2201–2218

    Article  PubMed  CAS  Google Scholar 

  • Brembu T, Winge P, Bones AM (2005) The small GTPase AtRAC2/ROP7 is specifically expressed during late stages of xylem differentiation in Arabidopsis. J Exp Bot 56:2465–2476

    Article  PubMed  CAS  Google Scholar 

  • Cheung AY, Wu HM (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59:547–572

    Article  PubMed  CAS  Google Scholar 

  • Chow CM, Neto H, Foucart C, Moore I (2008) Rab-A2 and Rab-A3 GTPases define a trans-golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. Plant Cell 20:101–123

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14:547–558

    Article  PubMed  CAS  Google Scholar 

  • Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45:616–629

    Article  PubMed  CAS  Google Scholar 

  • Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757

    Article  PubMed  CAS  Google Scholar 

  • Jedd G, Richardson C, Litt R, Segev N (1995) The Ypt1 GTPase is essential for the first two steps of the yeast secretory pathway. J Cell Biol 131:583–590

    Article  PubMed  CAS  Google Scholar 

  • Kim GT, Shoda K, Tsuge T, Cho KH, Uchimiya H, Yokoyama R, Nishitani K, Tsukaya H (2002) The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J 21:1267–1279

    Article  PubMed  CAS  Google Scholar 

  • Kotzer AM, Brandizzi F, Neumann U, Paris N, Moore I, Hawes C (2004) AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. J Cell Sci 117:6377–6389

    Article  PubMed  CAS  Google Scholar 

  • Kunz C, Schob H, Leubner-Metzger G, Glazov E, Meins F Jr (2001) Beta-1, 3-glucanase and chitinase transgenes in hybrids show distinctive and independent patterns of posttranscriptional gene silencing. Planta 212:243–249

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Lee HJ, Shin MK, Ryu WS (2004) Versatile PCR-mediated insertion or deletion mutagenesis. Biotechniques 36:398–400

    PubMed  CAS  Google Scholar 

  • Li H, Shen JJ, Zheng ZL, Lin Y, Yang Z (2001) The Rop GTPase switch controls multiple developmental processes in Arabidopsis. Plant Physiol 126:670–684

    Article  PubMed  CAS  Google Scholar 

  • Ma JF, Hou XL, Xiao D, Qi L, Wang F, Sun FF, Wang Q (2010) Cloning and characterization of the BcTuR3 gene related to resistance to turnip mosaic virus (TuMV) from non-heading Chinese cabbage. Plant Mol Biol Rep 28:588–596

    Article  CAS  Google Scholar 

  • Martinez-Trujillo M, Limones-Briones V, Cabrera-Ponce J, Herrera-Estrella L (2004) Improving transformation efficiency of Arabidopsis thaliana by modifying the floral dip method. Plant Mol Biol Rep 22:63–70

    Article  CAS  Google Scholar 

  • Narita NN, Moore S, Horiguchi G, Kubo M, Demura T, Fukuda H, Goodrich J, Tsukaya H (2004) Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J 38:699–713

    Article  PubMed  CAS  Google Scholar 

  • Nelson BK, Cai X, Nebenfuhr A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136

    Article  PubMed  CAS  Google Scholar 

  • Nielsen E, Cheung AY, Ueda T (2008) The regulatory RAB and ARF GTPases for vesicular trafficking. Plant Physiol 147:1516–1526

    Article  PubMed  CAS  Google Scholar 

  • Peng J, Ilarslan H, Wurtele E, Bassham D (2011) AtRabD2b and AtRabD2c have overlapping functions in pollen development and pollen tube growth. BMC Plant Biol 11:25

    Article  PubMed  CAS  Google Scholar 

  • Pereira-Leal JB, Seabra MC (2000) The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily. J Mol Biol 301:1077–1087

    Article  PubMed  CAS  Google Scholar 

  • Pinheiro H, Samalova M, Geldner N, Chory J, Martinez A, Moore I (2009) Genetic evidence that the higher plant Rab-D1 and Rab-D2 GTPases exhibit distinct but overlapping interactions in the early secretory pathway. J Cell Sci 122:3749–3758

    Article  PubMed  CAS  Google Scholar 

  • Plutner H, Cox AD, Pind S, Khosravi-Far R, Bourne JR, Schwaninger R, Der CJ, Balch WE (1991) Rab1b regulates vesicular transport between the endoplasmic reticulum and successive Golgi compartments. J Cell Biol 115:31–43

    Article  PubMed  CAS  Google Scholar 

  • Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172:991–998

    Article  PubMed  CAS  Google Scholar 

  • Qiu JL, Jilk R, Marks MD, Szymanski DB (2002) The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissue development. Plant Cell 14:101–118

    Article  PubMed  CAS  Google Scholar 

  • Rutherford S, Moore I (2002) The Arabidopsis Rab GTPase family: another enigma variation. Curr Opin Plant Biol 5:518–528

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Segev N, Mulholland J, Botstein D (1988) The yeast GTP-binding YPT1 protein and a mammalian counterpart are associated with the secretion machinery. Cell 52:915–924

    Article  PubMed  CAS  Google Scholar 

  • Singer SD, Hily JM, Liu ZR (2010) A 1-kb bacteriophage lambda fragment functions as an Insulator to effectively block enhancer–promoter interactions in Arabidopsis thaliana. Plant Mol Biol Rep 28:69–76

    Article  CAS  Google Scholar 

  • Speth EB, Imboden L, Hauck P, He SY (2009) Subcellular localization and functional analysis of the Arabidopsis GTPase RabE. Plant Physiol 149:1824–1837

    Article  PubMed  CAS  Google Scholar 

  • Stenmark H, Olkkonen VM (2001) The Rab GTPase family. Genome Biol 2(5):REVIEWS3007

    Article  PubMed  CAS  Google Scholar 

  • Tisdale EJ, Bourne JR, Khosravi-Far R, Der CJ, Balch WE (1992) GTP-binding mutants of rab1 and rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex. J Cell Biol 119:749–761

    Article  PubMed  CAS  Google Scholar 

  • Tsuge T, Tsukaya H, Uchimiya H (1996) Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.) Heynh. Development 122:1589–1600

    PubMed  CAS  Google Scholar 

  • Tsukaya H (2006) Mechanism of leaf-shape determination. Annu Rev Plant Biol 57:477–496

    Article  PubMed  CAS  Google Scholar 

  • Venglat SP, Dumonceaux T, Rozwadowski K, Parnell L, Babic V, Keller W, Martienssen R, Selvaraj G, Datla R (2002) The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc Natl Acad Sci 99:4730–4735

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Li J (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59:253–279

    Article  PubMed  CAS  Google Scholar 

  • Wroblewski T, Tomczak A, Michelmore R (2005) Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnol J 3:259–273

    Article  PubMed  CAS  Google Scholar 

  • Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107–117

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Nature Science Foundation of China (30671088). We thank the China Scholarship Council for providing the scholarship and Dr. Qing Lu and Dr. Gang Tian for their cooperation and help. We are grateful to Gautam Mayank for critical review of this manuscript.

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Correspondence to Kede Liu.

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Wang, F., Liu, C., Wei, C. et al. AtRabD2b, a Functional Ortholog of the Yeast Ypt1, Controls Various Growth and Developmental Processes in Arabidopsis. Plant Mol Biol Rep 30, 275–285 (2012). https://doi.org/10.1007/s11105-011-0336-z

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