Emerging roles of small GTPases in secondary cell wall development

Frontiers in Plant Science

Volumn 5, Issue AUG, 2014, Pages

  Oda, Yoshihisa ^a,b,c   Fukuda, Hiroo ^d  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cytoskeleton; Rab GTPase; ROP GTPase; Secondary cell wall; Xylem

Indexed keywords

EID: 84907325888     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00428     Document Type: Review

References (60)

1. Akamatsu, A., Wong, H. L., Fujiwara, M., Okuda, J., Nishide, K., Uno, K., et al. (2013). An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe 13, 465-476. doi: 10. 1016/j. chom. 2013. 03. 007.
2. Bloch, D., Lavy, M., Efrat, Y., Efroni, I., Bracha-Drori, K., Abu-Abied, M., et al. (2005). Ectopic expression of an activated RAC in Arabidopsis disrupts membrane cycling. Mol. Biol. Cell 16, 1913-1927. doi: 10. 1091/mbc. E04-07-0562.
3. Brembu, T., Winge, P., and Bones, A. M. (2005). The small GTPase AtRAC2/ROP7 is specifically expressed during late stages of xylem differentiation in Arabidopsis. J. Exp. Bot. 56, 2465-2476. doi: 10. 1093/jxb/eri239.
4. Chang, F., Gu, Y., Ma, H., and Yang, Z. (2013). AtPRK2 promotes ROP1 activation via RopGEFs in the control of polarized pollen tube growth. Mol. Plant 6, 1187-1201. doi: 10. 1093/mp/sss103.
5. Cole, R. A., Synek, L., Zarsky, V., and Fowler, J. E. (2005). SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol. 138, 2005-2018. doi: 10. 1104/pp. 105. 062273.
6. Craddock, C., Lavagi, I., and Yang, Z. (2012). New insights into Rho signaling from plant ROP/Rac GTPases. Trends Cell Biol. 22, 492-501. doi: 10. 1016/j. tcb. 2012. 05. 002.
7. Crowell, E. F., Bischoff, V., Desprez, T., Rolland, A., Stierhof, Y. D., Schumacher, K., et al. (2009). Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21, 1141-1154. doi: 10. 1105/tpc. 108. 065334.
8. de Graaf, B. H., Cheung, A. Y., Andreyeva, T., Levasseur, K., Kieliszewski, M., and Wu, H. M. (2005). Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 17, 2564-2579. doi: 10. 1105/tpc. 105. 033183.
9. Demura, T., and Ye, Z. H. (2010). Regulation of plant biomass production. Curr. Opin. Plant Biol. 13, 299-304. doi: 10. 1016/j. pbi. 2010. 03. 002.
10. Duan, Q., Kita, D., Li, C., Cheung, A. Y., and Wu, H. M. (2010). FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc. Natl. Acad. Sci. U. S. A. 107, 17821-17826. doi: 10. 1073/pnas. 1005366107.
11. Falconer, M. M., and Seagull, R. W. (1985). Xylogenesis in tissue-culture-taxol effects on microtubule reorientation and lateral association in differentiating cells. Protoplasma 128, 157-166. doi: 10. 1007/Bf01276337.
12. Foucart, C., Jauneau, A., Gion, J. M., Amelot, N., Martinez, Y., Panegos, P., et al. (2009). Overexpression of EgROP1, a Eucalyptus vascular-expressed Rac-like small GTPase, affects secondary xylem formation in Arabidopsis thaliana. New Phytol. 183, 1014-1029. doi: 10. 1111/j. 1469-8137. 2009. 02910. x.
13. Fu, Y., Gu, Y., Zheng, Z., Wasteneys, G., and Yang, Z. (2005). Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120, 687-700. doi: 10. 1016/j. cell. 2004. 12. 026.
14. Gu, F., and Nielsen, E. (2013). Targeting and regulation of cell wall synthesis during tip growth in plants. J. Integr. Plant Biol. 55, 835-846. doi: 10. 1111/jipb. 12077.
15. Gutierrez, M. G., Munafo, D. B., Beron, W., and Colombo, M. I. (2004). Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J. Cell Sci. 117, 2687-2697. doi: 10. 1242/jcs. 01114.
16. Gutierrez, R., Lindeboom, J. J., Paredez, A. R., Emons, A. M., and Ehrhardt, D. W. (2009). Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat. Cell Biol. 11, 797-806. doi: 10. 1038/ncb1886.
17. Hala, M., Cole, R., Synek, L., Drdova, E., Pecenkova, T., Nordheim, A., et al. (2008). An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20, 1330-1345. doi: 10. 1105/tpc. 108. 059105.
18. He, B., and Guo, W. (2009). The exocyst complex in polarized exocytosis. Curr. Opin. Cell Biol. 21, 537-542. doi: 10. 1016/j. ceb. 2009. 04. 007.
19. Huang, G. Q., Li, E., Ge, F. R., Li, S., Wang, Q., Zhang, C. Q., et al. (2013). Arabidopsis RopGEF4 and RopGEF10 are important for FERONIA-mediated developmental but not environmental regulation of root hair growth. New Phytol. 200, 1089-1101. doi: 10. 1111/nph. 12432.
20. Jager, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Saftig, P., et al. (2004). Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 117, 4837-4848. doi: 10. 1242/jcs. 01370.
21. Kirisako, T., Baba, M., Ishihara, N., Miyazawa, K., Ohsumi, M., Yoshimori, T., et al. (1999). Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147, 435-446. doi: 10. 1083/jcb. 147. 2. 435.
22. Ko, J. H., Beers, E. P., and Han, K. H. (2006). Global comparative transcriptome analysis identifies gene network regulating secondary xylem development in Arabidopsis thaliana. Mol. Genet. Genomics 276, 517-531. doi: 10. 1007/s00438-006-0157-1.
23. Kwon, S. I., Cho, H. J., Jung, J. H., Yoshimoto, K., Shirasu, K., and Park, O. K. (2010a). The Rab GTPase RabG3b functions in autophagy and contributes to tracheary element differentiation in Arabidopsis. Plant J. 64, 151-164. doi: 10. 1111/j. 1365-313X. 2010. 04315. x.
24. Kwon, S. I., Cho, H. J., and Park, O. K. (2010b). Role of Arabidopsis RabG3b and autophagy in tracheary element differentiation. Autophagy 6, 1187-1189. doi: 10. 4161/auto. 6. 8. 13429.
25. Kwon, S. I., Cho, H. J., Lee, J. S., Jin, H., Shin, S. J., Kwon, M., et al. (2011). Overexpression of constitutively activeArabidopsis RabG3b promotes xylem development in transgenic poplars. Plant Cell Environ. 34, 2212-2224. doi: 10. 1111/j. 1365-3040. 2011. 02416. x.
26. Lavy, M., Bloch, D., Hazak, O., Gutman, I., Poraty, L., Sorek, N., et al. (2007). A Novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr. Biol. 17, 947-952. doi: 10. 1016/j. cub. 2007. 04. 038.
27. Li, S., Chen, M., Yu, D., Ren, S., Sun, S., Liu, L., et al. (2013). EXO70A1-mediated vesicle trafficking is critical for tracheary element development in Arabidopsis. Plant Cell 25, 1774-1786. doi: 10. 1105/tpc. 113. 112144.
28. Li, S., Gu, Y., Yan, A., Lord, E., and Yang, Z. B. (2008). RIP1 (ROP Interactive Partner 1)/ICR1 marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen growth. Mol. Plant 1, 1021-1035. doi: 10. 1093/mp/ssn051.
29. Li, S., Van Os, G. M., Ren, S., Yu, D., Ketelaar, T., Emons, A. M., et al. (2010). Expression and functional analyses of EXO70 genes in Arabidopsis implicate their roles in regulating cell type-specific exocytosis. Plant Physiol. 154, 1819-1830. doi: 10. 1104/pp. 110. 164178.
30. Mao, G., Buschmann, H., Doonan, J. H., and Lloyd, C. W. (2006). The role of MAP65-1 in microtubule bundling during Zinnia tracheary element formation. J. Cell Sci. 119, 753-758. doi: 10. 1242/jcs. 02813.
31. McFarlane, H. E., Doring, A., and Persson, S. (2014). The cell biology of cellulose synthesis. Annu. Rev. Plant Biol. 65, 69-94. doi: 10. 1146/annurev-arplant-050213-040240.
32. Mitsuda, N., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2005). The NAC transcription factors NST1 and NST2 ofArabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17, 2993-3006. doi: 10. 1105/tpc. 105. 036004.
33. Nagawa, S., Xu, T., and Yang, Z. (2010). RHO GTPase in plants: conservation and invention of regulators and effectors. Small GTPases 1, 78-88. doi: 10. 4161/sgtp. 1. 2. 14544.
34. Nakanomyo, I., Kost, B., Chua, N. H., and Fukuda, H. (2002). Preferential and asymmetrical accumulation of a Rac small GTPase mRNA in differentiating xylem cells of Zinnia elegans. Plant Cell Physiol. 43, 1484-1492. doi: 10. 1093/pcp/pcf170.
35. Nibau, C., Wu, H. M., and Cheung, A. Y. (2006). RAC/ROP GTPases: 'hubs' for signal integration and diversification in plants. Trends Plant Sci. 11, 309-315. doi: 10. 1016/j. tplants. 2006. 04. 003.
36. Oda, Y., and Fukuda, H. (2012a). Initiation of cell wall pattern by a Rho-and microtubule-driven symmetry breaking. Science 337, 1333-1336. doi: 10. 1126/science. 1222597.
37. Oda, Y., and Fukuda, H. (2012b). Secondary cell wall patterning during xylem differentiation. Curr. Opin. Plant Biol. 15, 38-44. doi: 10. 1016/j. pbi. 2011. 10. 005.
38. Oda, Y., and Fukuda, H. (2013a). The dynamic interplay of plasma membrane domains and cortical microtubules in secondary cell wall patterning. Front. Plant Sci. 4: 511. doi: 10. 3389/fpls. 2013. 00511.
39. Oda, Y., and Fukuda, H. (2013b). Rho of plant GTPase signaling regulates the behavior of Arabidopsis kinesin-13A to establish secondary cell wall patterns. Plant Cell 25, 4439-4450. doi: 10. 1105/tpc. 113. 117853.
40. Oda, Y., and Fukuda, H. (2013c). Spatial organization of xylem cell walls by ROP GTPases and microtubule-associated proteins. Curr. Opin. Plant Biol. 16, 743-748. doi: 10. 1016/j. pbi. 2013. 10. 010.
41. Oda, Y., and Hasezawa, S. (2006). Cytoskeletal organization during xylem cell differentiation. J. Plant Res. 119, 167-177. doi: 10. 1007/s10265-006-0260-8.
42. Oda, Y., Iida, Y., Kondo, Y., and Fukuda, H. (2010). Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Curr. Biol. 20, 1197-1202. doi: 10. 1016/j. cub. 2010. 05. 038.
43. Oda, Y., Mimura, T., and Hasezawa, S. (2005). Regulation of secondary cell wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiol. 137, 1027-1036. doi: 10. 1104/pp. 104. 052613.
44. Park, S., Szumlanski, A. L., Gu, F., Guo, F., and Nielsen, E. (2011). A role for CSLD3 during cell-wall synthesis in apical plasma membranes of tip-growing root-hair cells. Nat. Cell Biol. 13, 973-980. doi: 10. 1038/ncb2294.
45. Pesquet, E., Korolev, A. V., Calder, G., and Lloyd, C. W. (2010). The microtubule-associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr. Biol. 20, 744-749. doi: 10. 1016/j. cub. 2010. 02. 057.
46. Robinson, N. G., Guo, L., Imai, J., Toh, E. A., Matsui, Y., and Tamanoi, F. (1999). Rho3 of Saccharomyces cerevisiae, which regulates the actin cytoskeleton and exocytosis, is a GTPase which interacts with Myo2 and Exo70. Mol. Cell. Biol. 19, 3580-3587.
47. Rounds, C. M., and Bezanilla, M. (2013). Growth mechanisms in tip-growing plant cells. Annu. Rev. Plant Biol. 64, 243-265. doi: 10. 1146/annurev-arplant-050312-120150.
48. Synek, L., Schlager, N., Elias, M., Quentin, M., Hauser, M. T., and Zarsky, V. (2006). AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J. 48, 54-72. doi: 10. 1111/j. 1365-313X. 2006. 02854. x.
49. Szumlanski, A. L., and Nielsen, E. (2009). The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell 21, 526-544. doi: 10. 1105/tpc. 108. 060277.
50. Wen, T. J., Hochholdinger, F., Sauer, M., Bruce, W., and Schnable, P. S. (2005). The roothairless1 gene of maize encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol. 138, 1637-1643. doi: 10. 1104/pp. 105. 062174.
51. Wightman, R., and Turner, S. R. (2008). The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J. 54, 794-805. doi: 10. 1111/j. 1365-313X. 2008. 03444. x.
52. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G. V., and Provart, N. J. (2007). An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718. doi: 10. 1371/journal. pone. 0000718.
53. Wu, H., Turner, C., Gardner, J., Temple, B., and Brennwald, P. (2010). The Exo70 subunit of the exocyst is an effector for both Cdc42 and Rho3 function in polarized exocytosis. Mol. Biol. Cell 21, 430-442. doi: 10. 1091/mbc. E09-06-0501.
54. Xu, T., Dai, N., Chen, J., Nagawa, S., Cao, M., Li, H., et al. (2014). Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343, 1025-1028. doi: 10. 1126/science. 1245125.
55. Xu, T., Wen, M., Nagawa, S., Fu, Y., Chen, J. G., Wu, M. J., et al. (2010). Cell surface-and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99-110. doi: 10. 1016/j. cell. 2010. 09. 003.
56. Yang, Z. (2008). Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 24, 551-575. doi: 10. 1146/annurev. cellbio. 23. 090506. 123233.
57. Yang, Z., and Fu, Y. (2007). ROP/RAC GTPase signaling. Curr. Opin. Plant Biol. 10, 490-494. doi: 10. 1016/j. pbi. 2007. 07. 005.
58. Ye, Z. H., Freshour, G., Hahn, M. G., Burk, D. H., and Zhong, R. (2002). Vascular development in Arabidopsis. Int. Rev. Cytol. 220, 225-256. doi: 10. 1016/S0074-7696(02)20007-8.
59. Zarsky, V., Kulich, I., Fendrych, M., and Pecenkova, T. (2013). Exocyst complexes multiple functions in plant cells secretory pathways. Curr. Opin. Plant Biol. 16, 726-733. doi: 10. 1016/j. pbi. 2013. 10. 013.
60. Zhong, R. Q., Burk, D. H., Morrison, W. H., and Ye, Z. H. (2002). A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14, 3101-3117. doi: 10. 1105/Tpc. 005801.