5.9
CiteScore
5.9
Impact Factor
Volume 39 Issue 2
Feb.  2012
Turn off MathJax
Article Contents

Arabidopsis AtVPS15 Plays Essential Roles in Pollen Germination Possibly by Interacting with AtVPS34

doi: 10.1016/j.jgg.2012.01.002
More Information
  • Corresponding author: E-mail address: qingenji@pku.edu.cn (Genji Qin); E-mail address: qulj@pku.edu.cn (Li-Jia Qu)
  • Received Date: 2011-12-29
  • Accepted Date: 2012-01-05
  • Rev Recd Date: 2012-01-04
  • Available Online: 2012-01-13
  • Publish Date: 2012-02-20
  • VPS15 protein is a component of the phosphatidylinositol 3-kinase complex which plays a pivotal role in the development of yeast and mammalian cells. The knowledge about the function of its homologue in plants remains limited. Here we report that AtVPS15, a homologue of yeast VPS15p in Arabidopsis, plays an essential role in pollen germination. Homozygous T-DNA insertion mutants of AtVPS15 could not be obtained from the progenies of self-pollinated heterozygous mutants. Reciprocal crosses between atvps15 mutants and wild-type Arabidopsis revealed that the T-DNA insertion was not able to be transmitted by male gametophytes. DAPI staining, Alexander's stain and scanning electron microscopic analysis showed that atvps15 heterozygous plants produced pollen grains that were morphologically indistinguishable from wild-type pollen, whereas in vitro germination experiments revealed that germination of the pollen grains was defective. GUS staining analysis of transgenic plants expressing the GUS reporter gene driven by the AtVPS15 promoter showed that AtVPS15 was mainly expressed in pollen grains. Finally, DUALmembrane yeast two-hybrid analysis demonstrated that AtVPS15 might interact directly with AtVPS34. These results suggest that AtVPS15 is very important for pollen germination, possibly through modulation of the activity of PI3-kinase.
  • loading
  • [1]
    Alexander, M.P. Differential staining of aborted and nonaborted pollen Stain Technol., 44 (1969),pp. 117-122
    [2]
    Alonso, J.M., Stepanova, A.N. Methods Mol. Biol., 236 (2003),pp. 177-188
    [3]
    Bankaitis, V.A., Johnson, L.M., Emr, S.D. Isolation of yeast mutants defective in protein targeting to the vacuole Proc. Natl. Acad. Sci. USA, 83 (1986),pp. 9075-9079
    [4]
    Budovskaya, Y.V., Hama, H., DeWald, D.B. et al. The C terminus of the Vps34p phosphoinositide 3-kinase is necessary and sufficient for the interaction with the Vps15p protein kinase J. Biol. Chem., 277 (2002),pp. 287-294
    [5]
    Cantley, L.C. The phosphoinositide 3-kinase pathway Science, 296 (2002),pp. 1655-1657
    [6]
    Chrispeels, M.J., Crawford, N.M., Schroeder, J.I. Proteins for transport of water and mineral nutrients across the membranes of plant cells Plant Cell, 11 (1999),pp. 661-676
    [7]
    Christoforidis, S., Miaczynska, M., Ashman, K. et al. Phosphatidylinositol-3-OH kinases are Rab5 effectors Nat. Cell Biol., 1 (1999),pp. 249-252
    [8]
    Clamp, M., Cuff, J., Searle, S.M. et al. The Jalview Java alignment editor Bioinformatics, 20 (2004),pp. 426-427
    [9]
    Copenhaver, G.P., Keith, K.C., Preuss, D. Tetrad analysis in higher plants. A budding technology Plant Physiol., 124 (2000),pp. 7-16
    [10]
    Deng, Y., Wang, W., Li, W.Q. et al. J. Integr. Plant Biol., 52 (2010),pp. 829-843
    [11]
    Earley, K.W., Haag, J.R., Pontes, O. et al. Gateway-compatible vectors for plant functional genomics and proteomics Plant J., 45 (2006),pp. 616-629
    [12]
    Fimia, G.M., Stoykova, A., Romagnoli, A. et al. Ambra1 regulates autophagy and development of the nervous system Nature, 447 (2007),pp. 1121-1125
    [13]
    Franklin-Tong, V.E., Drobak, B.K., Allan, A.C. et al. Plant Cell, 8 (1996),pp. 1305-1321
    [14]
    Fruman, D.A., Meyers, R.E., Cantley, L.C. Phosphoinositide kinases Annu. Rev. Biochem., 67 (1998),pp. 481-507
    [15]
    Fujiki, Y., Yoshimoto, K., Ohsumi, Y. Plant Physiol., 143 (2007),pp. 1132-1139
    [16]
    Funderburk, S.F., Wang, Q.J., Yue, Z. The Beclin 1-VPS34 complex – at the crossroads of autophagy and beyond Trends Cell Biol., 20 (2010),pp. 355-362
    [17]
    Goldberg, J. Structural basis for activation of ARF GTPase: mechanisms of guanine nucleotide exchange and GTP-myristoyl switching Cell, 95 (1998),pp. 237-248
    [18]
    Guo, Y., Qin, G., Gu, H. et al. Plant Cell, 21 (2009),pp. 3518-3534
    [19]
    Hanakam, F., Gerisch, G., Lotz, S. et al. Binding of hisactophilin I and II to lipid membranes is controlled by a pH-dependent myristoyl-histidine switch Biochemistry, 35 (1996),pp. 11036-11044
    [20]
    Harrison-Lowe, N.J., Olsen, L.J. Autophagy, 4 (2008),pp. 339-348
    [21]
    Herman, P.K., Stack, J.H., Emr, S.D. A genetic and structural analysis of the yeast Vps15 protein kinase: evidence for a direct role of Vps15p in vacuolar protein delivery EMBO J., 10 (1991),pp. 4049-4060
    [22]
    Herman, P.K., Stack, J.H., DeModena, J.A. et al. A novel protein kinase homolog essential for protein sorting to the yeast lysosome-like vacuole Cell, 64 (1991),pp. 425-437
    [23]
    Hermida-Matsumoto, L., Resh, M.D. Human immunodeficiency virus type 1 protease triggers a myristoyl switch that modulates membrane binding of Pr55(gag) and p17MA J. Virol., 73 (1999),pp. 1902-1908
    [24]
    Holsters, M., de Waele, D., Depicker, A. et al. Mol. Gen. Genet., 163 (1978),pp. 181-187
    [25]
    Ikeda, S., Nasrallah, J.B., Dixit, R. et al. Science, 276 (1997),pp. 1564-1566
    [26]
    Itakura, E., Kishi, C., Inoue, K. et al. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG Mol. Biol. Cell, 19 (2008),pp. 5360-5372
    [27]
    Jefferson, R.A., Kavanagh, T.A., Bevan, M.W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants EMBO J., 6 (1987),pp. 3901-3907
    [28]
    Johnson, S.A., McCormick, S. Plant Physiol., 126 (2001),pp. 685-695
    [29]
    Johnsson, N., Varshavsky, A. Proc. Natl. Acad. Sci. USA, 91 (1994),pp. 10340-10344
    [30]
    Kihara, A., Noda, T., Ishihara, N. et al. J. Cell Biol., 152 (2001),pp. 519-530
    [31]
    Kihara, A., Kabeya, Y., Ohsumi, Y. et al. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network EMBO Rep., 2 (2001),pp. 330-335
    [32]
    Krichevsky, A., Kozlovsky, S.V., Tian, G.W. et al. How pollen tubes grow Dev. Biol., 303 (2007),pp. 405-420
    [33]
    Lee, Y., Kim, E.S., Choi, Y. et al. Plant Physiol., 147 (2008),pp. 1886-1897
    [34]
    Letunic, I., Doerks, T., Bork, P. SMART 6: recent updates and new developments Nucleic Acids Res., 37 (2009),pp. D229-D232
    [35]
    Li, H., Lin, Y., Heath, R.M. et al. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx Plant Cell, 11 (1999),pp. 1731-1742
    [36]
    Liang, C., Lee, J.S., Inn, K.S. et al. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking Nat. Cell Biol., 10 (2008),pp. 776-787
    [37]
    Liu, J., Zhang, Y., Qin, G. et al. Plant Cell, 20 (2008),pp. 1538-1554
    [38]
    Livak, K.J., Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods, 25 (2001),pp. 402-408
    [39]
    Matsunaga, K., Saitoh, T., Tabata, K. et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages Nat. Cell Biol., 11 (2009),pp. 385-396
    [40]
    Mayfield, J.A., Preuss, D. Nat. Cell Biol., 2 (2000),pp. 128-130
    [41]
    McLaughlin, S., Aderem, A. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions Trends Biochem. Sci., 20 (1995),pp. 272-276
    [42]
    Muschietti, J., Dircks, L., Vancanneyt, G. et al. LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization Plant J., 6 (1994),pp. 321-338
    [43]
    Needleman, S.B., Wunsch, C.D. A general method applicable to the search for similarities in the amino acid sequence of two proteins J. Mol. Biol., 48 (1970),pp. 443-453
    [44]
    Obara, K., Sekito, T., Ohsumi, Y. Mol. Biol. Cell, 17 (2006),pp. 1527-1539
    [45]
    Obermeyer, G., Weisenseel, M.H. Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes Eur. J. Cell Biol., 56 (1991),pp. 319-327
    [46]
    Obrdlik, P., El-Bakkoury, M., Hamacher, T. et al. Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 12242-12247
    [47]
    Olsen, H.B., Kaarsholm, N.C. Structural effects of protein lipidation as revealed by LysB29-myristoyl, des(B30) insulin Biochemistry, 39 (2000),pp. 11893-11900
    [48]
    Panaretou, C., Domin, J., Cockcroft, S. et al. Characterization of p150, an adaptor protein for the human phosphatidylinositol (PtdIns) 3-kinase. Substrate presentation by phosphatidylinositol transfer protein to the p150.Ptdins 3-kinase complex J. Biol. Chem., 272 (1997),pp. 2477-2485
    [49]
    Petiot, A., Faure, J., Stenmark, H. et al. PI3P signaling regulates receptor sorting but not transport in the endosomal pathway J. Cell Biol., 162 (2003),pp. 971-979
    [50]
    Pierson, E.S., Miller, D.D., Callaham, D.A. et al. Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media Plant Cell, 6 (1994),pp. 1815-1828
    [51]
    Preuss, D., Rhee, S.Y., Davis, R.W. Science, 264 (1994),pp. 1458-1460
    [52]
    Preuss, D., Lemieux, B., Yen, G. et al. Genes Dev., 7 (1993),pp. 974-985
    [53]
    Qi, Q., Rajala, R.V., Anderson, W. et al. J. Biol. Chem., 275 (2000),pp. 9673-9683
    [54]
    Qin, G., Ma, Z., Zhang, L. et al. Cell Res., 17 (2007),pp. 249-263
    [55]
    Qin, G., Gu, H., Zhao, Y. et al. Plant Cell, 17 (2005),pp. 2693-2704
    [56]
    Rathore, K.S., Cork, R.J., Robinson, K.R. Dev. Biol., 148 (1991),pp. 612-619
    [57]
    Regan, S.M., Moffatt, B.A. Plant Cell, 2 (1990),pp. 877-889
    [58]
    Resh, M.D. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins Biochim. Biophys. Acta., 1451 (1999),pp. 1-16
    [59]
    Robinson, J.S., Klionsky, D.J., Banta, L.M. et al. Mol. Cell. Biol., 8 (1988),pp. 4936-4948
    [60]
    Roth, M.G. Phosphoinositides in constitutive membrane traffic Physiol. Rev., 84 (2004),pp. 699-730
    [61]
    Rothman, J.H., Stevens, T.H. Protein sorting in yeast: mutants defective in vacuole biogenesis mislocalize vacuolar proteins into the late secretory pathway Cell, 47 (1986),pp. 1041-1051
    [62]
    Schu, P.V., Takegawa, K., Fry, M.J. et al. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting Science, 260 (1993),pp. 88-91
    [63]
    Schultz, J., Milpetz, F., Bork, P. et al. SMART, a simple modular architecture research tool: identification of signaling domains Proc. Natl. Acad. Sci. USA, 95 (1998),pp. 5857-5864
    [64]
    Stack, J.H., Emr, S.D. Vps34p required for yeast vacuolar protein sorting is a multiple specificity kinase that exhibits both protein kinase and phosphatidylinositol-specific PI 3-kinase activities J. Biol. Chem., 269 (1994),pp. 31552-31562
    [65]
    Stack, J.H., Herman, P.K., Schu, P.V. et al. A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole EMBO J., 12 (1993),pp. 2195-2204
    [66]
    Stagljar, I., Korostensky, C., Johnsson, N. et al. Proc. Natl. Acad. Sci. USA, 95 (1998),pp. 5187-5192
    [67]
    Stein, M.P., Cao, C., Tessema, M. et al. Interaction and functional analyses of human VPS34/p150 phosphatidylinositol 3-kinase complex with Rab7 Methods Enzymol., 403 (2005),pp. 628-649
    [68]
    Sun, Q., Fan, W., Chen, K. et al. Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase Proc. Natl. Acad. Sci. USA, 105 (2008),pp. 19211-19216
    [69]
    Thoresen, S.B., Pedersen, N.M., Liestol, K. et al. A phosphatidylinositol 3-kinase class III sub-complex containing VPS15, VPS34, Beclin 1, UVRAG and BIF-1 regulates cytokinesis and degradative endocytic traffic Exp. Cell Res., 316 (2010),pp. 3368-3378
    [70]
    Towler, D.A., Gordon, J.I., Adams, S.P. et al. The biology and enzymology of eukaryotic protein acylation Annu. Rev. Biochem., 57 (1988),pp. 69-99
    [71]
    Volinia, S., Dhand, R., Vanhaesebroeck, B. et al. A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system EMBO J., 14 (1995),pp. 3339-3348
    [72]
    Walhout, A.J., Temple, G.F., Brasch, M.A. et al. GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes Methods Enzymol., 328 (2000),pp. 575-592
    [73]
    Weigel, D., Glazebrook, J.
    [74]
    Welters, P., Takegawa, K., Emr, S.D. et al. Proc. Natl. Acad. Sci. USA, 91 (1994),pp. 11398-11402
    [75]
    Wu, R., Li, S., He, S. et al. Plant Cell, 23 (2011),pp. 3392-3411
    [76]
    Wu, Y., Yan, J., Zhang, R. et al. Plant Cell, 22 (2010),pp. 3745-3763
    [77]
    Xing, S., Qin, G., Shi, Y. et al. J. Integr. Plant Biol., 49 (2007),pp. 368-381
    [78]
    Xu, N., Gao, X.Q., Zhao, X.Y. et al. Plant Mol. Biol., 77 (2011),pp. 251-260
    [79]
    Yang, X.Y., Li, J.G., Pei, M. et al. Plant Cell Rep., 26 (2007),pp. 219-228
    [80]
    Zhang, H., Qu, X., Bao, C. et al. Plant Cell, 22 (2010),pp. 2749-2767
    [81]
    Zhang, Y., Li, S., Zhou, L.Z. et al. Plant J., 68 (2011),pp. 1081-1092
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (65) PDF downloads (0) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return