Arabidopsis COG Complex Subunits COG3 and COG8 Modulate Golgi Morphology, Vesicle Trafficking Homeostasis and Are Essential for Pollen Tube Growth

PLoS Genetics

Volumn 12, Issue 7, 2016, Pages

  Tan, Xiaoyun ^a   Cao, Kun ^a   Liu, Feng ^a   Li, Yingxin ^a   Li, Pengxiang ^a   Gao, Caiji ^b   Ding, Yu ^b   Lan, Zhiyi ^a   Shi, Zhixuan ^a   Rui, Qingchen ^a   Feng, Yihong ^a   Liu, Yulong ^a   Zhao, Yanxue ^a   Wu, Chengyun ^a   Zhang, Qian ^a   Li, Yan ^a   Jiang, Liwen ^b   Bao, Yiqun ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; PROTEIN COG3; PROTEIN COG8; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; BACTERIAL DNA; MUTANT PROTEIN; PROTEIN SUBUNIT; T-DNA; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ARTICLE; CELL MIGRATION; CELL STRUCTURE; CELL VACUOLE; COG3 GENE; COG8 GENE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE INSERTION; GENE LOCATION; GENE MUTATION; GOLGI COMPLEX; GOLGI MEMBRANE; HOMEOSTASIS; MALE; NONHUMAN; PHENOTYPE; PLANT CELL; PLANT DEVELOPMENT; PLANT GENE; PLANT GROWTH; POLLEN; PROMOTER REGION; PROTEIN FUNCTION; REGULATORY MECHANISM; ARABIDOPSIS; CELL MEMBRANE; CELL WALL; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; POLLEN TUBE; PROTEIN SUBUNIT; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; CELL WALL; DNA, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; GLYCOSYLATION; GOLGI APPARATUS; MEMBRANE PROTEINS; MUTANT PROTEINS; POLLEN; POLLEN TUBE; PROTEIN SUBUNITS; PROTEIN TRANSPORT;

EID: 84982792097     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006140     Document Type: Article

References (57)

1. McCormick S, (2004) Control of male gametophyte development. Plant Cell16 Suppl: S142–153. 15037731
2. Hepler PK, Vidali L, Cheung AY, (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol17: 159–187. 11687487
3. Chebli Y, Kroeger J, Geitmann A, (2013) Transport logistics in pollen tubes. Mol Plant6: 1037–1052. doi: 10.1093/mp/sst07323686949
4. Rounds CM, Bezanilla M, (2013) Growth mechanisms in tip-growing plant cells. Annu Rev Plant Biol64: 243–265. doi: 10.1146/annurev-arplant-050312-12015023451782
5. Derksen J, Rutten T, Lichtscheidl IK, Win AHND, Pierson ES, et al. (1995) Quantitative analysis of the distribution of organelles in tobacco pollen tubes: implications for exocytosis and endocytosis. Protoplasma188: 267–276.
6. Moscatelli A, Ciampolini F, Rodighiero S, Onelli E, Cresti M, et al. (2007) Distinct endocytic pathways identified in tobacco pollen tubes using charged nanogold. J Cell Sci120: 3804–3819. 17940063
7. Bove J, Vaillancourt B, Kroeger J, Hepler PK, Wiseman PW, et al. (2008) Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy and fluorescence recovery after photobleaching. Plant Physiol147: 1646–1658. doi: 10.1104/pp.108.12021218508956
8. Zonia L, Munnik T, (2008) Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. J Exp Bot59: 861–873. doi: 10.1093/jxb/ern00718304978
9. Cheung AY, Wu HM, (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol59: 547–572. doi: 10.1146/annurev.arplant.59.032607.09292118444907
10. de Graaf BH, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, et al. (2005) Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell17: 2564–2579. 16100336
11. Szumlanski AL, Nielsen E, (2009) The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell21: 526–544. doi: 10.1105/tpc.108.06027719208902
12. Hala M, Cole R, Synek L, Drdova E, Pecenkova T, et al. (2008) An Exocyst complex functions in plant cell growth in Arabidopsis and Tobacco. Plant Cell20: 1330–1345. doi: 10.1105/tpc.108.05910518492870
13. Drdova EJ, Synek L, Pecenkova T, Hala M, Kulich I, et al. (2013) The exocyst complex contributes to PIN auxin efflux carrier recycling and polar auxin transport in Arabidopsis. Plant J73: 709–719. doi: 10.1111/tpj.1207423163883
14. Wu J, Tan X, Wu C, Cao K, Li Y, et al. (2013) Regulation of cytokinesis by exocyst subunit SEC6 and KEULE in Arabidopsis thaliana. Mol Plant6: 1863–1876. doi: 10.1093/mp/sst08223702595
15. Richter S, Muller LM, Stierhof YD, Mayer U, Takada N, et al. (2012) Polarized cell growth in Arabidopsis requires endosomal recycling mediated by GBF1-related ARF exchange factors. Nat Cell Biol14: 80–86.
16. Cheung AY, Chen CYH, Glaven RH, de Graaf BHJ, Vidali L, et al. (2002) Rab2 GTPase regulates vesicle trafficking between the endoplasmic reticulum and the Golgi bodies and is important to pollen tube growth. Plant Cell14: 945–962. 11971147
17. Stefano G, Renna L, Chatre L, Hanton SL, Moreau P, et al. (2006) In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J46: 95–110. 16553898
18. Ito Y, Uemura T, Nakano A, (2014) Formation and maintenance of the Golgi apparatus in plant cells. Int Rev Cell Mol Biol310: 221–287. doi: 10.1016/B978-0-12-800180-6.00006-224725428
19. Ram RJ, Li B, Kaiser CA, (2002) Identification of Sec36p, Sec37p, and Sec38p: components of yeast complex that contains Sec34p and Sec35p. Mol Biol Cell13: 1484–1500. 12006647
20. Ungar D, Oka T, Krieger M, Hughson FM, (2006) Retrograde transport on the COG railway. Trends in Cell Biology16: 113–120. 16406524
21. Zolov SN, Lupashin VV, (2005) Cog3p depletion blocks vesicle-mediated Golgi retrograde trafficking in HeLa cells. J Cell Biol168: 747–759. 15728195
22. Sohda M, Misumi Y, Yamamoto A, Nakamura N, Ogata S, et al. (2010) Interaction of Golgin-84 with the COG complex mediates the intra-Golgi retrograde transport. Traffic11: 1552–1566. doi: 10.1111/j.1600-0854.2010.01123.x20874812
23. Willett R, Ungar D, Lupashin V, (2013) The Golgi puppet master: COG complex at center stage of membrane trafficking interactions. Histochem Cell Biol140: 271–283. doi: 10.1007/s00418-013-1117-623839779
24. Latijnhouwers M, Hawes C, Carvalho C, (2005) Holding it all together? Candidate proteins for the plant Golgi matrix. Curr Opin Plant Biol8: 632–639. 16194619
25. Pimpl P, Movafeghi A, Coughlan S, Denecke J, Hillmer S, et al. (2000) In situ localization and in vitro induction of plant COPI-coated vesicles. Plant Cell12: 2219–2236. 11090220
26. Donohoe BS, Kang BH, Staehelin LA, (2007) Identification and characterization of COPIa- and COPIb-type vesicle classes associated with plant and algal Golgi. Proc Natl Acad Sci U S A104: 163–168. 17185411
27. Contreras I, Ortiz-Zapater E, Castilho LM, Aniento F, (2000) Characterization of Cop I coat proteins in plant cells. Biochem Biophys Res Commun273: 176–182. 10873582
28. Couchy I, Bolte S, Crosnier MT, Brown S, Satiat-Jeunemaitre B, (2003) Identification and localization of a beta-COP-like protein involved in the morphodynamics of the plant Golgi apparatus. J Exp Bot54: 2053–2063. 12885863
29. Takeuchi M, Ueda T, Yahara N, Nakano A, (2002) Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J31: 499–515. 12182707
30. Matheson LA, Hanton SL, Rossi M, Latijnhouwers M, Stefano G, et al. (2007) Multiple roles of ADP-ribosylation factor 1 in plant cells include spatially regulated recruitment of coatomer and elements of the Golgi matrix. Plant Physiol143: 1615–1627. 17307898
31. Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, et al. (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J15: 441–447. 9750355
32. Brandizzi F, Snapp EL, Roberts AG, Lippincott-Schwartz J, Hawes C, (2002) Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photo bleaching. Plant Cell14: 1293–1309. 12084828
33. Ramirez IB, Lowe M, (2009) Golgins and GRASPs: holding the Golgi together. Semin Cell Dev Biol20: 770–779. doi: 10.1016/j.semcdb.2009.03.01119508854
34. Renna L, Hanton SL, Stefano G, Bortolotti L, Misra V, et al. (2005) Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein. Plant Mol Biol58: 109–122. 16028120
35. Latijnhouwers M, Gillespie T, Boevink P, Kriechbaumer V, Hawes C, et al. (2007) Localization and domain characterization of Arabidopsis golgin candidates. J Exp Bot58: 4373–4386. doi: 10.1093/jxb/erm30418182439
36. Kang BH, Staehelin LA, (2008) ER-to-Golgi transport by COPII vesicles in Arabidopsis involves a ribosome-excluding scaffold that is transferred with the vesicles to the Golgi matrix. Protoplasma234: 51–64. doi: 10.1007/s00709-008-0015-618810574
37. Ishikawa T, Machida C, Yoshioka Y, Ueda T, Nakano A, et al. (2008) EMBRYO YELLOW gene, encoding a subunit of the conserved oligomeric Golgi complex, is required for appropriate cell expansion and meristem organization in Arabidopsis thaliana. Genes Cells13: 521–535. doi: 10.1111/j.1365-2443.2008.01186.x18422605
38. Ostertag M, Stammler J, Douchkov D, Eichmann R, Huckelhoven R, (2013) The conserved oligomeric Golgi complex is involved in penetration resistance of barley to the barley powdery mildew fungus. Mol Plant Pathol14: 230–240. doi: 10.1111/j.1364-3703.2012.00846.x23145810
39. Preuss D, Rhee SY, Davis RW, (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science264: 1458–1460. 8197459
40. Zinkl GM, Zwiebel BI, Grier DG, Preuss D, (1999) Pollen-stigma adhesion in Arabidopsis: a species-specific interaction mediated by lipophilic molecules in the pollen exine. Development126: 5431–5440. 10556067
41. Song X-F, Yang C-Y, Liu J, Yang W-C, (2006) RPA, a class II ARFGAP Protein, activates ARF1 and U5 and plays a role in root hair development in Arabidopsis. Plant Physiology141: 966–976. 16731582
42. Wang W, Wang L, Chen C, Xiong G, Tan XY, et al. (2011) Arabidopsis CSLD1 and CSLD4 are required for cellulose deposition and normal growth of pollen tubes. J Exp Bot62: 5161–5177. doi: 10.1093/jxb/err22121765162
43. Crofts A.J., Leborgne-Castel N., Hillmer S., Robinson D.G., Phillipson B., Carlsson L.E., et al. (1999) Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant Cell11: 2233–2248. 10559446
44. Gao C, Yu CK, Qu S, San MW, Li KY, et al. (2012) The Golgi-localized Arabidopsis endomembrane protein12 contains both endoplasmic reticulum export and Golgi retention signals at its C terminus. Plant Cell24: 2086–2104. doi: 10.1105/tpc.112.09605722570441
45. Wang L, Wang W, Wang YQ, Liu YY, Wang JX, et al. (2013) Arabidopsis galacturonosyltransferase (GAUT) 13 and GAUT14 have redundant functions in pollen tube growth. Mol Plant6: 1131–1148. doi: 10.1093/mp/sst08423709340
46. Nebenfuhr A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, et al. (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol121: 1127–1142. 10594100
47. Chebli Y, Kaneda M, Zerzour R, Geitmann A, (2012) The cell wall of the Arabidopsis pollen tube—spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol160: 1940–1955. doi: 10.1104/pp.112.19972923037507
48. Bosch M, Hepler PK, (2005) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell17: 3219–3226. 16322606
49. Dardelle F, Lehner A, Ramdani Y, Bardor M, Lerouge P, et al. (2010) Biochemical and immunocytological characterizations of Arabidopsis pollen tube cell wall. Plant Physiol153: 1563–1576. doi: 10.1104/pp.110.15888120547702
50. Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, et al. (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell17: 584–596. 15659637
51. Gu F, Nielsen E, (2013) Targeting and regulation of cell wall synthesis during tip growth in plants. J Integr Plant Biol55: 835–846. doi: 10.1111/jipb.1207723758901
52. Staehelin LA, Moore I, (1995) The plant Golgi apparatus: Structure, functional organization and trafficking mechanisms. Annu Rev Plant Physiol Plant MolBiol46: 261–288.
53. Richter S, Geldner N, Schrader J, Wolters H, Stierhof YD, et al. (2007) Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature448: 488–492. 17653190
54. Teh OK, Moore I, (2007) An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature448: 493–496. 17653191
55. Alexander MP, (1969) Differential staining of aborted and nonaborted pollen. Stain Technol44: 117–122. 4181665
56. Liu CM, Meinke DW, (1998) The titan mutants of Arabidopsis are disrupted in mitosis and cell cycle control during seed development. The Plant Journal16: 21–31. 9807824
57. Backues S.K., Korasick D.A., Heese A., Bednarek S.Y., (2010) The Arabidopsis dynamin-related protein2 family is essential for gametophyte development. Plant Cell22: 3218–3231. doi: 10.1105/tpc.110.07772720959563