AtPRK2 promotes ROP1 activation via RopGEFs in the control of polarized pollen tube growth

Molecular Plant

Volumn 6, Issue 4, 2013, Pages 1187-1201

  Chang, Fang ^a,b,c   Gu, Ying ^c,d   Ma, Hong ^a   Yang, Zhenbiao ^c  

^a FUDAN UNIVERSITY   (China)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

AtPRK2; Auto inhibition; Polarity growth; ROP GTPase; RopGEF1

Indexed keywords

ARABIDOPSIS; NICOTIANA TABACUM;

EID: 84870521785     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sss103     Document Type: Article

References (46)

1. Berken, A., Thomas, C., and Wittinghofer, A. (2005). A new family of RhoGEFs activates the Rop molecular switch in plants. Nature. 436, 1176-1180.
2. Chang, F., Yan, A., Zhao, L., Wu, W., and Yang, Z. (2007). A putative calcium-permeable Cyclic Nucleotide-Gated Channel, CNGC18, regulates polarized pollen tube growth. J. Int. Plant Biol. 49, 1261-1270.
3. Chen, M., Liu, H., Kong, J., Yang, Y., Zhang, N., Li, R., Yue, J., Huang, J., Li, C., Cheung, A.Y., et al. (2011). RopGEF7 regulates PLETHORA-dependent maintenance of the root stem cell niche in Arabidopsis. Plant Cell. 23, 2880-2894.
4. Cheung, A.Y., and Wu, H.M. (2008). Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu. Rev. Plant Biol. 59, 547-572.
5. Duan, Q.H., 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.
6. Edgar, R.C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 5, 113.
7. 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.
8. Fu, Y., Wu, G., and Yang, Z. (2001). Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J. Cell Biol. 152, 1019-1032.
9. Fu, Y., Xu, T., Zhu, L., Wen, M., and Yang, Z. (2009). A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr. Biol. 19, 1827-1832.
10. Gu, Y., Fu, Y., Dowd, P., Li, S.D., Vernoud, V., Gilroy, S., and Yang Z.B. (2005). A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J. Cell Biol. 169, 127-138.
11. Gu, Y., Li, S., Lord, E.M., and Yang, Z. (2006). Members of a novel class of Arabidopsis Rho guanine nucleotide exchange factors control Rho GTPase-dependent polar growth. Plant Cell. 18, 366-381.
12. Gu, Y., Vernoud, V., Fu, Y., and Yang, Z. (2003). ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J. Exp. Bot. 54, 93-101.
13. Gu, Y., Wang, Z., and Yang, Z. (2004). ROP/RAC GTPase: an old new master regulator for plant signaling. Curr. Opin. Plant Biol. 7, 527-536.
14. Hwang, J.U., Gu, Y., Lee, Y.J., and Yang, Z. (2005). Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol. Biol. Cell. 16, 5385-5399.
15. Hwang, J.U., Vernoud, V., Szumlanski, A., Nielsen, E., and Yang, Z. (2008). A tip-localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr. Biol. 18, 1907-1916.
16. Hwang, J.U., Wu, G., Yan A., Lee, Y.J., Grierson, C.S., and Yang, Z. (2010). Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity. J. Cell Sci. 123, 340-350.
17. Johnson, M.A., and Preuss, D. (2003). On your mark, get set, GROW! LePRK2-LAT52 interactions regulate pollen tube growth. Trends Plant Sci. 8, 97-99.
18. Jones, M.A., Raymond, M.J., Yang, Z., and Smirnoff, N. (2007). NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J. Exp. Bot, 58, 1261-1270.
19. Jones, M.A., Shen, J.J., Fu, Y., Li, H., Yang, Z., and Grierson, C.S. (2002). The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell. 14, 763-776.
20. Kaothien, P., Ok, S.H., Shuai, B., Wengier, D., Cotter, R., Kelley, D., Kiriakopolos, S., Muschietti, J., and McCormick, S. (2005). Kinase partner protein interacts with the LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. Plant J. 42, 492-503.
21. Kim, H.U., Cotter, R., Johnson, S., Senda, M., Dodds, P., Kulikauskas, R., Tang, W.H., Ezcurra, I., Herzmark, P., and McCormick, S. (2002). New pollen-specific receptor kinases identified in tomato, maize and Arabidopsis: the tomato kinases show overlapping but distinct localization patterns on pollen tubes. Plant Mol. Biol. 50, 1-16.
22. Lee, Y.J., and Yang, Z. (2008). Tip growth: signaling in the apical dome. Curr. Opin. Plant Biol. 11, 662-671.
23. Lee, Y.J., Szumlanski, A., Nielsen, E., and Yang, Z. (2008). Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J. Cell Biol. 181, 1155-1168.
24. Li, H., Lin, Y., Heath, R.M., Zhu, M.X., and Yang, Z. (1999). Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell. 11, 1731-1742.
25. Lin, Y., and Yang, Z. (1997). Inhibition of pollen tube elongation by microinjected anti-Rop1Ps antibodies suggests a crucial role for Rho-type GTPases in the control of tip growth. Plant Cell. 9, 1647-1659.
26. Lin, Y., Wang, Y., Zhu, J.K., and Yang, Z. (1996). Localization of a Rho GTPase implies a role in tip growth and movement of the generative cell in pollen tubes. Plant Cell. 8, 293-303.
27. Margarit, S.M., Sondermann, H., Hall, B.E., Nagar, B., Hoelz, A., Pirruccello, M., Bar-Sagi, D., and Kuriyan, J. (2003). Structural evidence for feedback activation by Ras.GTP of the Ras-specific nucleotide exchange factor SOS. Cell. 112, 685-695.
28. Mu, J.H., Lee, H.S., and Kao, T.H. (1994). Characterization of a pollen-expressed receptor-like kinase gene of Petunia inflata and the activity of its encoded kinase. Plant Cell. 6, 709-721.
29. Muschietti, J., Eyal, Y., and McCormick, S. (1998). Pollen tube localization implies a role in pollen-pistil interactions for the tomato receptor-like protein kinases LePRK1 and LePRK2. Plant Cell. 10, 319-330.
30. Riely, B.K., He, H., Venkateshwaran, M., Sarma, B., Schraiber, J., Ane, J.M., and Cook, D.R. (2011). Identification of legume RopGEF gene families and characterization of a Medicago trun-catula RopGEF mediating polar growth of root hairs. Plant J. 65, 230-243.
31. Shin, D.H., Cho, M.H., Kim, T.L., Yoo, J., Kim, J. I., Han, Y. J., Song, P. S., Jeon, J. S., Bhoo, S. H., Hahn, and T. R. (2010) A small GTPase activator protein interacts with cytoplasmic phytochromes in regulating root development. J. Biol. Chem. 285, 32151-32159.
32. Shpak, E.D., Lakeman, M.B., and Torii, K.U. (2003). Dominantnegative receptor uncovers redundancy in the Arabidopsis ERECTA leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell. 15, 1095-1110.
33. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Bio. Evol. 28, 2731-2739.
34. Tang, W., Ezcurra, I., Muschietti, J., and McCormick, S. (2002). A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell. 14, 2277-2287.
35. Tang, W., Kelley, D., Ezcurra, I., Cotter, R., and McCormick, S. (2004). LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. Plant J. 39, 343-353.
36. Wengier, D., Valsecchi, I., Cabanas, M.L., Tang, W.H., McCormick, S., and Muschietti, J. (2003). The receptor kinases LePRK1 and LePRK2 associate in pollen and when expressed in yeast, but dissociate in the presence of style extract. Proc. Natl Acad. Sci. U S A. 100, 6860-6865.
37. Wu, G., Gu, Y., Li, S., and Yang, Z. (2001). A genome-wide analysis of Arabidopsis ROP-interactive CRIB motif genome-wide analysis of f is of ormic GTPase targets. Plant Cell. 13, 2841ell.
38. Xu, T., Wen, M, Nagava, S., Fu, Y., Chen, J., Wu, M., Rechenmann, C., Frimi, J., Jones, A.M., and Yang, Z. (2010). Cell surface-and rho GTPase-based auxin signaling controls cellular interdigita-tion in Arabidopsis. Cell. 143, 99-110.
39. Yamaguchi, K., Imai, K., Akamatsu, A., Mihashi, M., Hayashi, N., Shimanoto, K., and Kawasaki, T. (2012). SWAP70 functions as a Rac/Rop guanine nucleotide-exchange factor in rice. Plant J. 70, 389-397.
40. Yang, Z. (2002). Small GTPases: versatile signaling switches in plants. Plant Cell. 14 Suppl., S375-S388.
41. Yang, Z. (2008). Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 24, 551-575.
42. Yang, Z., and Fu, Y. (2007). ROP/RAC GTPase signaling. Curr. Opin. Plant Biol. 10, 490-494.
43. Yoo, J.H., Park, J.H., Cho, S.H., Yoo, S.C., Li, J., Zhang, H., Kim, K.S., Koh, H.J., and Paek, N.C. (2011). The rice bright green leaf (bgl) locus encodes OsRopGEF10, which activates the development of small cuticular papillae on leaf surfaces. Plant Mol. Biol. 77, 631-641.
44. Zhang, D., Wengier, D., Shuai, B., Cui, C.P., Muschietti, J., McCormick, S., and Tang, W.H. (2008). The pollen receptor kinase LePRK2 mediates growth-promoting signals and positively regulates pollen germination and tube growth. Plant Physiol. 148, 1368-1379.
45. Zhang, Y., and McCormick, S. (2007). A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 104, 18830-18835.
46. Zheng, Z.L., Nafisi, M., Tam, A., Li, H., Crowell, D.N., Chary, S.N., Schroeder, J.I., Shen, J., and Yang, Z. (2002). Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis. Plant Cell. 14, 2787-2797.