RopGEF7 regulates PLETHORA-dependent maintenance of the root stem cell niche in Arabidopsis

Plant Cell

Volumn 23, Issue 8, 2011, Pages 2880-2894

  Chen, Min ^a   Liu, Huili ^a   Kong, Jixiang ^a,d   Yang, Yali ^a   Zhang, Naichao ^a   Li, Ruijing ^a   Yue, Jianbin ^a   Huang, Jiaqing ^a   Li, Chuanyou ^b   Cheung, Alice Y ^c   Tao, Li Zhen ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 80053183750     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.085514     Document Type: Article

References (67)

1. Abel, S., Nguyen, M.D., and Theologis, A. (1995). The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J. Mol. Biol. 251: 533-549.
2. Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C., Nussaume, L., Noh, Y.S., Amasino, R., and Scheres, B. (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119: 109-120.
3. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G., and Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602.
4. Berken, A., Thomas, C., and Wittinghofer, A. (2005). A new family of RhoGEFs activates the Rop molecular switch in plants. Nature 436: 1176-1180.
5. Birnbaum, K., Shasha, D.E., Wang, J.Y., Jung, J.W., Lambert, G.M., Galbraith, D.W., and Benfey, P.N. (2003). A gene expression map of the Arabidopsis root. Science 302: 1956-1960.
6. Bischoff, F., Vahlkamp, L., Molendijk, A., and Palme, K. (2000). Localization of AtROP4 and AtROP6 and interaction with the guanine nucleotide dissociation inhibitor AtRhoGDI1 from Arabidopsis. Plant Mol. Biol. 42: 515-530.
7. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palme, K., and Scheres, B. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44.
8. Bloch, D., Lavy, M., Efrat, Y., Efroni, I., Bracha-Drori, K., Abu-Abied, M., Sadot, E., and Yalovsky, S. (2005). Ectopic expression of an activated RAC in Arabidopsis disrupts membrane cycling. Mol. Biol. Cell 16: 1913-1927.
9. Cheung, A.Y., Duan, Q.H., Costa, S.S., de Graaf, B.H., Di Stilio, V.S., Feijo, J., and Wu, H.M. (2008). The dynamic pollen tube cytoskeleton: Live cell studies using actin-binding and microtubule-binding reporter proteins. Mol. Plant 1: 686-702.
10. Citovsky, V., Lee, L.Y., Vyas, S., Glick, E., Chen, M.H., Vainstein, A., Gafni, Y., Gelvin, S.B., and Tzfira, T. (2006). Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta. J. Mol. Biol. 362: 1120-1131.
11. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
12. Colón-Carmona, A., You, R., Haimovitch-Gal, T., and Doerner, P. (1999). Technical advance: Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J. 20: 503-508.
13. Dhonukshe, P., et al. (2008). Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456: 962-966.
14. Dinneny, J.R., and Benfey, P.N. (2008). Plant stem cell niches: Standing the test of time. Cell 132: 553-557.
15. 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. USA 107: 17821-17826.
16. Friml, J., Benková, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K., Woody, S., Sandberg, G., Scheres, B., Jürgens, G., and Palme, K. (2002). AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108: 661-673.
17. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R., and Jürgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.
18. Fowler, J. E. (2010). Evolution of the ROP GTPase signaling module. In Integrated G Proteins Signaling in Plants, S. Yalovsky, F. Baluska, and A. Jones, eds (New York: Springer), pp. 305-327.
19. Fukaki, H., Wysocka-Diller, J., Kato, T., Fujisawa, H., Benfey, P.N., and Tasaka, M. (1998). Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J. 14: 425-430.
20. Galinha, C., Hofhuis, H., Luijten, M., Willemsen, V., Blilou, I., Heidstra, R., and Scheres, B. (2007). PLETHORA proteins as dosedependent master regulators of Arabidopsis root development. Nature 449: 1053-1057.
21. Grieneisen, V.A., Xu, J., Marée, A.F., Hogeweg, P., and Scheres, B. (2007). Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449: 1008-1013.
22. 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.
23. Hazak, O., Bloch, D., Poraty, L., Sternberg, H., Zhang, J., Friml, J., and Yalovsky, S. (2010). A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol. 8: e1000282.
24. Hejátko, J., Blilou, I., Brewer, P.B., Friml, J., Scheres, B., and Benková, E. (2006). In situ hybridization technique for mRNA detection in whole mount Arabidopsis samples. Nat. Protoc. 1: 1939-1946.
25. Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., Hauser, M.T., and Benfey, P.N. (2000). The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101: 555-567.
26. Hu, X., and Liu, Y. (2006). The construction of RNAi vectors and the use for gene silencing in rice. Mol. Plant Breed. 4: 621-626.
27. Jiang, K., and Feldman, L.J. (2005). Regulation of root apical meristem development. Annu. Rev. Cell Dev. Biol. 21: 485-509.
28. 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.
29. Kessler, S.A., Shimosato-Asano, H., Keinath, N.F., Wuest, S.E., Ingram, G., Panstruga, R., and Grossniklaus, U. (2010). Conserved molecular components for pollen tube reception and fungal invasion. Science 330: 968-971.
30. Klahre, U., Becker, C., Schmitt, A.C., and Kost, B. (2006). Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes. Plant J. 46: 1018-1031.
31. Komori, R., Amano, Y., Ogawa-Ohnishi, M., and Matsubayashi, Y. (2009). Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc. Natl. Acad. Sci. USA 106: 15067-15072.
32. Kornet, N., and Scheres, B. (2009). Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis. Plant Cell 21: 1070-1079.
33. Lavy, M., Bloch, D., Hazak, O., Gutman, I., Poraty, L., Sorek, N., Sternberg, H., and Yalovsky, S. (2007). A novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr. Biol. 17: 947-952.
34. Long, J.A., Ohno, C., Smith, Z.R., and Meyerowitz, E.M. (2006). TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312: 1520-1523.
35. Liu, C.M., and Meinke, D.W. (1998). The titan mutants of Arabidopsis are disrupted in mitosis and cell cycle control during seed development. Plant J. 16: 21-31.
36. Matsuzaki, Y., Ogawa-Ohnishi, M., Mori, A., and Matsubayashi, Y. (2010). Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329: 1065-1067.
37. Nakajima, K., Sena, G., Nawy, T., and Benfey, P.N. (2001). Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413: 307-311.
38. Nawy, T., Lee, J.Y., Colinas, J., Wang, J.Y., Thongrod, S.C., Malamy, J.E., Birnbaum, K., and Benfey, P.N. (2005). Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 17: 1908-1925.
39. Nibau, C., and Cheung, A. (2011). New insights into the functional roles of CrRLKs in the control of plant cell growth and development. Plant Signal. Behav. 6: 655-659.
40. 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.
41. Robert, S., et al. (2010). ABP1 mediates auxin inhibition of clathrindependent endocytosis in Arabidopsis. Cell 143: 111-121.
42. Rodermel, S.R., Abbott, M.S., and Bogorad, L. (1988). Nuclearorganelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 55: 673-681.
43. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P., and Scheres, B. (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463-472.
44. Sabatini, S., Heidstra, R., Wildwater, M., and Scheres, B. (2003). SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17: 354-358.
45. Scheres, B. (2007). Stem-cell niches: Nursery rhymes across kingdoms. Nat. Rev. Mol. Cell Biol. 8: 345-354.
46. Smith, Z.R., and Long, J.A. (2010). Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 464: 423-426.
47. Szemenyei, H., Hannon, M., and Long, J.A. (2008). TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319: 1384-1386.
48. Tao, L.Z., Cheung, A.Y., Nibau, C., and Wu, H.M. (2005). RAC GTPases in tobacco and Arabidopsis mediate auxin-induced formation of proteolytically active nuclear protein bodies that contain AUX/ IAA proteins. Plant Cell 17: 2369-2383.
49. Tao, L.Z., Cheung, A.Y., and Wu, H.M. (2002). Plant Rac-like GTPases are activated by auxin and mediate auxin-responsive gene expression. Plant Cell 14: 2745-2760.
50. Thomas, C., Fricke, I., Scrima, A., Berken, A., and Wittinghofer, A. (2007). Structural evidence for a common intermediate in small G protein-GEF reactions. Mol. Cell 25: 141-149.
51. Trotochaud, A.E., Hao, T., Wu, G., Yang, Z., and Clark, S.E. (1999). The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rhorelated protein. Plant Cell 11: 393-406.
52. Tsukagoshi, H., Busch, W., and Benfey, P.N. (2010). Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606-616.
53. Ulmasov, T., Hagen, G., and Guilfoyle, T.J. (1999). Activation and repression of transcription by auxin-response factors. Proc. Natl. Acad. Sci. USA 96: 5844-5849.
54. Ulmasov, T., Murfett, J., Hagen, G., and Guilfoyle, T.J. (1997). Aux/ IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
55. van den Berg, C., Willemsen, V., Hendriks, G., Weisbeek, P., and Scheres, B. (1997). Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390: 287-289.
56. Weigel, D., and Jürgens, G. (2002). Stem cells that make stems. Nature 415: 751-754.
57. Weijers, D., Franke-van Dijk, M., Vencken, R.J., Quint, A., Hooykaas, P., and Offringa, R. (2001). An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128: 4289-4299.
58. Wu, G., Li, H., and Yang, Z. (2000). Arabidopsis RopGAPs are a novel family of rho GTPase-activating proteins that require the Cdc42/Racinteractive binding motif for rop-specific GTPase stimulation. Plant Physiol. 124: 1625-1636.
59. Wu, H.M., Hazak, O., Cheung, A.Y., and Yalovsky, S. (2011). RAC/ ROP GTPases and auxin signaling. Plant Cell 23: 1208-1218.
60. Wysocka-Diller, J.W., Helariutta, Y., Fukaki, H., Malamy, J.E., and Benfey, P.N. (2000). Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127: 595-603.
61. Xu, T., Wen, M., Nagawa, S., Fu, Y., Chen, J.G., Wu, M.J., Perrot-Rechenmann, C., Friml, J., Jones, A.M., and Yang, Z. (2010). Cell surface-and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143: 99-110.
62. Yalovsky, S., Bloch, D., Sorek, N., and Kost, B. (2008). Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol. 147: 1527-1543.
63. Yang, Z. (2008). Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 24: 551-575.
64. Yang, Z., and Fu, Y. (2007). ROP/RAC GTPase signaling. Curr. Opin. Plant Biol. 10: 490-494.
65. Zhang, D., Wengier, D., Shuai, B., Gui, 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.
66. 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. USA 104: 18830-18835.
67. Zhou, W., Wei, L., Xu, J., Zhai, Q., Jiang, H., Chen, R., Chen, Q., Sun, J., Chu, J., Zhu, L., Liu, C.M., and Li, C. (2010). Arabidopsis Tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22: 3692-3709.