QUIRKY interacts with STRUBBELIG and PAL OF QUIRKY to regulate cell growth anisotropy during Arabidopsis gynoecium development

Development (Cambridge)

Volumn 140, Issue 23, 2013, Pages 4807-4817

  Trehin, Christophe ^a   Schrempp, Sandra ^a,b   Chauvet, Aurélie ^a   Berne Dedieu, Annick ^a   Thierry, Anne Marie ^a   Faure, Jean Emmanuel ^a,c   Negrutiu, Ioan ^a   Morel, Patrice ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITY OF FREIBURG   (Germany)

^c EUROPEAN COMMISSION   (Belgium)

Author keywords

Arabidopsis thaliana; Cell cell communication; Growth anisotropy; Gynoecium architecture; MCTP; PB1 domain; QUIRKY; STRUBBELIG

Indexed keywords

MULTIPROTEIN COMPLEX;

ANISOTROPY; ARABIDOPSIS; ARABIDOPSIS GYNOECIUM; ARTICLE; CELL COMMUNICATION; CELL DIVISION; CELL EXPANSION; CELL GROWTH; CELL MATURATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORTICAL MICROTUBULE; MICROTUBULE; MUTANT; NONHUMAN; PISTIL; PLANT DEVELOPMENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SILIQUE;

ARABIDOPSIS THALIANA; CELL-CELL COMMUNICATION; GROWTH ANISOTROPY; GYNOECIUM ARCHITECTURE; MCTP; PB1 DOMAIN; QUIRKY; STRUBBELIG;

AMINO ACID SEQUENCE; ANISOTROPY; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CELL COMMUNICATION; CELL MEMBRANE; GENE EXPRESSION REGULATION, PLANT; MEMBRANE PROTEINS; MICROTUBULES; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; RECEPTOR PROTEIN-TYROSINE KINASES; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 84887958346     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.091868     Document Type: Article

References (79)

1. Abe, M., Katsumata, H., Komeda, Y. and Takahashi, T. (2003). Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development 130, 635-643.
2. Alvarez-Buylla, E. R., Benítez, M., Corvera-Poir, A., Chaos Cador, Á., de Folter, S., Gamboa de Buen, A., Garay-Arroyo, A., Jaimes-Miranda, F., Pérez-Ruiz, R. V., Piñeyro-Nelson, A. et al. (2010). Flower development. Arabidopsis Book 8, e0127.
3. Bansal, D. and Campbell, K. P. (2004). Dysferlin and the plasma membrane repair in muscular dystrophy. Trends Cell Biol. 14, 206-213.
4. Bichet, A., Desnos, T., Turner, S., Grandjean, O. and Höfte, H. (2001). BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J. 25, 137-148.
5. Burk, D. H., Liu, B., Zhong, R., Morrison, W. H. and Ye, Z. H. (2001). A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13, 807-827.
6. Buschmann, H. and Lloyd, C. W. (2008). Arabidopsis mutants and the network of microtubule-associated functions. Mol. Plant 1, 888-898.
7. Chevalier, D., Batoux, M., Fulton, L., Pfister, K., Yadav, R. K., Schellenberg, M. and Schneitz, K. (2005). STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc. Natl. Acad. Sci. USA 102, 9074-9079.
8. Cho, W. and Stahelin, R. V. (2006). Membrane binding and subcellular targeting of C2 domains. Biochim. Biophys. Acta 1761, 838-849.
9. Craxton, M. (2010). A manual collection of Syt, Esyt, Rph3a, Rph3al, Doc2, and Dblc2 genes from 46 metazoan genomes-an open access resource for neuroscience and evolutionary biology. BMC Genomics 11, 37.
10. De Smet, I., Voss, U., Jürgens, G. and Beeckman, T. (2009). Receptor-like kinases shape the plant. Nat. Cell Biol. 11, 1166-1173.
11. Depège-Fargeix, N., Javelle, M., Chambrier, P., Frangne, N., Gerentes, D., Perez, P., Rogowsky, P. M. and Vernoud, V. (2011). Functional characterization of the HDZIP IV transcription factor OCL1 from maize. J. Exp. Bot. 62, 293-305.
12. Desprez, T., Juraniec, M., Crowell, E. F., Jouy, H., Pochylova, Z., Parcy, F., Höfte, H., Gonneau, M. and Vernhettes, S. (2007). Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104, 15572-15577.
13. Donnelly, P. M., Bonetta, D., Tsukaya, H., Dengler, R. E. and Dengler, N. G. (1999). Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev. Biol. 215, 407-419.
14. Fan, H. Y., Hu, Y., Tudor, M. and Ma, H. (1997). Specific interactions between the K domains of AG and AGLs, members of the MADS domain family of DNA binding proteins. Plant J. 12, 999-1010.
15. Ferrandiz, C., Fourquin, C., Prunet, N., Scutt, C. P., Sundberg, E., Trehin, C. and Vialette-Guiraud, A. C. M. (2010). Carpel development. In Advances in Botanical Research, Vol. 55 (ed. J. C. Kader and M. Delseny), pp. 1-73. London: Academic Press.
16. Fromont-Racine, M., Rain, J. C. and Legrain, P. (1997). Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat. Genet. 16, 277-282.
17. Fulton, L., Batoux, M., Vaddepalli, P., Yadav, R. K., Busch, W., Andersen, S. U., Jeong, S., Lohmann, J. U. and Schneitz, K. (2009). DETORQUEO, QUIRKY, and ZERZAUST represent novel components involved in organ development mediated by the receptor-like kinase STRUBBELIG in Arabidopsis thaliana. PLoS Genet. 5, e1000355.
18. Furutani, I., Watanabe, Y., Prieto, R., Masukawa, M., Suzuki, K., Naoi, K., Thitamadee, S., Shikanai, T. and Hashimoto, T. (2000). The SPIRAL genes are required for directional control of cell elongation in Aarabidopsis thaliana. Development 127, 4443-4453.
19. Geetha, T., Jiang, J. and Wooten, M. W. (2005). Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling. Mol. Cell 20, 301-312.
20. Grebe, M., Xu, J., Möbius, W., Ueda, T., Nakano, A., Geuze, H. J., Rook, M. B. and Scheres, B. (2003). Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr. Biol. 13, 1378-1387.
21. Hamant, O. and Traas, J. (2010). The mechanics behind plant development. New Phytol. 185, 369-385.
22. Harashima, H. and Schnittger, A. (2010). The integration of cell division, growth and differentiation. Curr. Opin. Plant Biol. 13, 66-74.
23. Hu, Q., Shen, W., Huang, H., Liu, J., Zhang, J., Huang, X., Wu, J. and Shi, Y. (2007). Insight into the binding properties of MEKK3 PB1 to MEK5 PB1 from its solution structure. Biochemistry 46, 13478-13489.
24. Ingram, G. C. (2004). Between the sheets: inter-cell-layer communication in plant development. Philos. Trans. R. Soc. B 359, 891-906.
25. Jakoby, M. and Schnittger, A. (2004). Cell cycle and differentiation. Curr. Opin. Plant Biol. 7, 661-669.
26. Jarvis, M. C., Briggs, S. P. H. and Knox, J. P. (2003). Intercellular adhesion and cell separation in plants. Plant Cell Environ. 26, 977-989.
27. Johnson, K. and Lenhard, M. (2011). Genetic control of plant organ growth. New Phytol. 191, 319-333.
28. Kikkawa, U., Kishimoto, A. and Nishizuka, Y. (1989). The protein kinase C family: heterogeneity and its implications. Annu. Rev. Biochem. 58, 31-44.
29. Kuchen, E. E., Fox, S., de Reuille, P. B., Kennaway, R., Bensmihen, S., Avondo, J., Calder, G. M., Southam, P., Robinson, S., Bangham, A. et al. (2012). Generation of leaf shape through early patterns of growth and tissue polarity. Science 335, 1092-1096.
30. Kwak, S. H., Shen, R. and Schiefelbein, J. (2005). Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 307, 1111-1113.
31. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R. et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
32. Lin, L., Zhong, S. H., Cui, X. F., Li, J. and He, Z. H. (2012). Characterization of temperature-sensitive mutants reveals a role for receptor-like kinase SCRAMBLED/STRUBBELIG in coordinating cell proliferation and differentiation during Arabidopsis leaf development. Plant J. 72, 707-720.
33. Lloyd, C. (2011). Dynamic microtubules and the texture of plant cell walls. Int. Rev. Cell Mol. Biol. 287, 287-329.
34. Long, R., Yang, Q., Kang, J., Chao, Y., Wang, P., Wu, M., Qin, Z. and Sun, Y. (2012). Molecular cloning and characterization of a novel stress responsive gene in alfalfa. Biol. Plant. 56, 43-49.
35. Maeda, I., Kohara, Y., Yamamoto, M. and Sugimoto, A. (2001). Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 11, 171-176.
36. Martens, S. and McMahon, H. T. (2008). Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9, 543-556.
37. Mathur, J. (2004). Cell shape development in plants. Trends Plant Sci. 9, 583-590.
38. Mathur, J. and Chua, N. H. (2000). Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. Plant Cell 12, 465-477.
39. Meng, X., Wang, H., He, Y., Liu, Y., Walker, J. C., Torii, K. U. and Zhang, S. (2012). A MAPK cascade downstream of ERECTA receptor-like protein kinase regulates Arabidopsis inflorescence architecture by promoting localized cell proliferation. Plant Cell 24, 4948-4960.
40. Moscat, J., Diaz-Meco, M. T., Albert, A. and Campuzano, S. (2006). Cell signaling and function organized by PB1 domain interactions. Mol. Cell 23, 631-640.
41. Nakajima, K., Furutani, I., Tachimoto, H., Matsubara, H. and Hashimoto, T. (2004). SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16, 1178-1190.
42. Nakamura, K. and Johnson, G. L. (2007). Noncanonical function of MEKK2 and MEK5 PB1 domains for coordinated extracellular signal-regulated kinase 5 and c-Jun N-terminal kinase signaling. Mol. Cell. Biol. 27, 4566-4577.
43. Nakamura, K., Kimple, A. J., Siderovski, D. P. and Johnson, G. L. (2010). PB1 domain interaction of p62/sequestosome 1 and MEKK3 regulates NF-kappaB activation. J. Biol. Chem. 285, 2077-2089.
44. Nath, U., Crawford, B. C., Carpenter, R. and Coen, E. (2003). Genetic control of surface curvature. Science 299, 1404-1407.
45. Ostlund, G., Schmitt, T., Forslund, K., Köstler, T., Messina, D. N., Roopra, S., Frings, O. and Sonnhammer, E. L. L. (2010). InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res. 38, D196-D203.
46. Paredez, A. R., Somerville, C. R. and Ehrhardt, D. W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491-1495.
47. Ponting, C. P., Ito, T., Moscat, J., Diaz-Meco, M. T., Inagaki, F. and Sumimoto, H. (2002). OPR, PC and AID: all in the PB1 family. Trends Biochem. Sci. 27, 10.
48. Posey, A. D., Jr, Demonbreun, A. and McNally, E. M. (2011). Ferlin proteins in myoblast fusion and muscle growth. Curr. Top. Dev. Biol. 96, 203-230.
49. Prunet, N., Morel, P., Thierry, A. M., Eshed, Y., Bowman, J. L., Negrutiu, I. and Trehin, C. (2008). REBELOTE, SQUINT, and ULTRAPETALA1 function redundantly in the temporal regulation of floral meristem termination in Arabidopsis thaliana. Plant Cell 20, 901-919.
50. Ramirez-Parra, E., Desvoyes, B. and Gutierrez, C. (2005). Balance between cell division and differentiation during plant development. Int. J. Dev. Biol. 49, 467-477.
51. Reinhardt, D., Frenz, M., Mandel, T. and Kuhlemeier, C. (2003). Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem. Development 130, 4073-4083.
52. Roeder, A. H. and Yanofsky, M. F. (2006). Fruit development in Arabidopsis. Arabidopsis Book 11, e0075.
53. Rotman, N., Rozier, F., Boavida, L., Dumas, C., Berger, F. and Faure, J. E. (2003). Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr. Biol. 13, 432-436.
54. Sanchez, P., De Carcer, G., Sandoval, I. V., Moscat, J. and Diaz-Meco, M. T. (1998). Localization of atypical protein kinase C isoforms into lysosome-targeted endosomes through interaction with p62. Mol. Cell. Biol. 18, 3069-3080.
55. Savaldi-Goldstein, S. and Chory, J. (2008). Growth coordination and the shoot epidermis. Curr. Opin. Plant Biol. 11, 42-48.
56. Schapire, A. L., Voigt, B., Jasik, J., Rosado, A., Lopez-Cobollo, R., Menzel, D., Salinas, J., Mancuso, S., Valpuesta, V., Baluska, F. et al. (2008). Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20, 3374-3388.
57. Schapire, A. L., Valpuesta, V. and Botella, M. A. (2009). Plasma membrane repair in plants. Trends Plant Sci. 14, 645-652.
58. Schiefelbein, J., Kwak, S. H., Wieckowski, Y., Barron, C. and Bruex, A. (2009). The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J. Exp. Bot. 60, 1515-1521.
59. Schmid, M., Davison, T. S., Henz, S. R., Pape, U. J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D. and Lohmann, J. U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506.
60. Seifert, G. J. and Blaukopf, C. (2010). Irritable walls: the plant extracellular matrix and signaling. Plant Physiol. 153, 467-478.
61. Seyfried, J., Wang, X., Kharebava, G. and Tournier, C. (2005). A novel mitogenactivated protein kinase docking site in the N terminus of MEK5alpha organizes the components of the extracellular signal-regulated kinase 5 signaling pathway. Mol. Cell. Biol. 25, 9820-9828.
62. 2+ binding properties. J. Biol. Chem. 280, 1641-1651.
63. Shoji, T., Narita, N. N., Hayashi, K., Asada, J., Hamada, T., Sonobe, S., Nakajima, K. and Hashimoto, T. (2004). Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiol. 136, 3933-3944.
64. Shpak, E. D., Berthiaume, C. T., Hill, E. J. and Torii, K. U. (2004). Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131, 1491-1501.
65. Stoppin-Mellet, V., Gaillard, J. and Vantard, M. (2006). Katanin's severing activity favors bundling of cortical microtubules in plants. Plant J. 46, 1009-1017.
66. Sumimoto, H., Kamakura, S. and Ito, T. (2007). Structure and function of the PB1 domain, a protein interaction module conserved in animals, fungi, amoebas, and plants. Sci. STKE 2007, re6.
67. Terasawa, H., Noda, Y., Ito, T., Hatanaka, H., Ichikawa, S., Ogura, K., Sumimoto, H. and Inagaki, F. (2001). Structure and ligand recognition of the PB1 domain: a novel protein module binding to the PC motif. EMBO J. 20, 3947-3956.
68. Thitamadee, S., Tuchihara, K. and Hashimoto, T. (2002). Microtubule basis for lefthanded helical growth in Arabidopsis. Nature 417, 193-196.
69. Ueda, K., Matsuyama, T. and Hashimoto, T. (1999). Visualization of microtubules in living cells of transgenic Arabidopsis thaliana. Protoplasma 206, 201-206.
70. Uyttewaal, M., Burian, A., Alim, K., Landrein, B., Borowska-Wykre{ogonek}t, D., Dedieu, A., Peaucelle, A., Ludynia, M., Traas, J., Boudaoud, A. et al. (2012). Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149, 439-451.
71. Vaddepalli, P., Fulton, L., Batoux, M., Yadav, R. K. and Schneitz, K. (2011). Structure-function analysis of STRUBBELIG, an Arabidopsis atypical receptor-like kinase involved in tissue morphogenesis. PLoS ONE 6, e19730.
72. van Zanten, M., Snoek, L. B., Proveniers, M. C. and Peeters, A. J. (2009). The many functions of ERECTA. Trends Plant Sci. 14, 214-218.
73. Walhout, A. J. and Vidal, M. (2001). High-throughput yeast two-hybrid assays for large-scale protein interaction mapping. Methods 24, 297-306.
74. Wilson, M. I., Gill, D. J., Perisic, O., Quinn, M. T. and Williams, R. L. (2003). PB1 domain-mediated heterodimerization in NADPH oxidase and signaling complexes of atypical protein kinase C with Par6 and p62. Mol. Cell 12, 39-50.
75. 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.
76. Yadav, R. K., Fulton, L., Batoux, M. and Schneitz, K. (2008). The Arabidopsis receptor-like kinase STRUBBELIG mediates inter-cell-layer signaling during floral development. Dev. Biol. 323, 261-270.
77. Yamazaki, T., Kawamura, Y., Minami, A. and Uemura, M. (2008). Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20, 3389-3404.
78. Yoo, S. D., Cho, Y. H. and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.
79. Zelazny, E., Santambrogio, M., Pourcher, M., Chambrier, P., Berne-Dedieu, A., Fobis-Loisy, I., Miege, C., Jaillais, Y. and Gaude, T. (2013). Mechanisms governing the endosomal membrane recruitment of the core retromer in Arabidopsis. J. Biol. Chem. 288, 8815-8825.