The Yin and Yang of cell wall integrity control: Brassinosteroid and FERONIA signaling

Plant and Cell Physiology

Volumn 56, Issue 2, 2015, Pages 224-231

  Höfte, Herman ^a,b  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b AGROPARISTECH   (France)

Author keywords

Brassinosteroid; Cellulose; Feedback signaling; Pectin; Receptor kinases

Indexed keywords

BRASSINOSTEROID; VEGETABLE PROTEIN;

BIOLOGICAL MODEL; CELL WALL; METABOLISM; PLANT DEVELOPMENT; SIGNAL TRANSDUCTION;

BRASSINOSTEROIDS; CELL WALL; MODELS, BIOLOGICAL; PLANT DEVELOPMENT; PLANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84928748786     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcu182     Document Type: Review

References (59)

1. Andeme-Onzighi, C., Sivaguru, M., Judy-March, J., Baskin, T.I. and Driouich, A. (2002) The reb1-1 mutation of Arabidopsis alters the morphology of trichoblasts, the expression of arabinogalactanproteins and the organization of cortical microtubules. Planta 215: 949-958.
2. Arsovski, A.A., Haughn, G.W. and Western, T.L. (2010) Seed coat mucilage cells of Arabidopsis thaliana as a model for plant cell wall research. Plant Signal. Behav. 5: 796-801.
3. Atmodjo, M.A., Hao, Z. and Mohnen, D. (2013) Evolving views of pectin biosynthesis. Ann. Rev. Plant Biol. 64: 747-779.
4. Bishop, G.J., Nomura, T., Yokota, T., Harrison, K., Noguchi, T., Fujioka, S. et al. (1999) The tomato DWARF enzyme catalyses C-6 oxidation in brassinosteroid biosynthesis. Proc. Natl Acad. Sci. USA 96: 1761-1766.
5. Boisson-Dernier, A., Kessler, S.A. and Grossniklaus, U. (2011) The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals. J. Exp. Bot. 62: 1581-1591.
6. Boisson-Dernier, A., Lituiev, D.S., Nestorova, A., Franck, C.M., Thirugnanarajah, S. and Grossniklaus, U. (2013) ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol. 11: e1001719.
7. Boyer, J.S. (2009) Cell wall biosynthesis and the molecular mechanism of plant enlargement. Funct. Plant Biol. 36: 383-394.
8. Cabrera, J.C., Boland, A., Messiaen, J., Cambier, P. and Van Cutsem, P. (2008) Egg box conformation of oligogalacturonides: the timedependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18: 473-482.
9. Carpita, N. and McCann, M. (2000) The cell wall. In Biochemistry and Molecular Biology of Plants. Edited by Buchanan, B., Gruissem, W. and Jones, R. pp. 52-108. American Soiciety of Plant Physiology, Rockville, MD.
10. Denness, L., McKenna, J.F., Segonzac, C., Wormit, A., Madhou, P., Bennett, M. et al. (2011) Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species-and jasmonic acid-dependent process in Arabidopsis. Plant Physiol. 156: 1364-1374.
11. Duan, Q., Kita, D., Johnson, E.A., Aggarwal, M., Gates, L., Wu, H.M. et al. (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat. Commun. 5: 3129.
12. 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.
13. Dumais, J. (2013) Modes of deformation of walled cells. J. Exp. Bot. 64: 4681-4695.
14. Escobar-Restrepo, J.M., Huck, N., Kessler, S., Gagliardini, V., Gheyselinck, J., Yang, W.C. et al. (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317: 656-660.
15. Ferrari, S., Savatin, D.V., Sicilia, F., Gramegna, G., Cervone, F. and De Lorenzo, G. (2013) Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front. Plant Sci. 4: 49.
16. Fridman, Y., Elkouby, L., Holland, N., Vragovic, K., Elbaum, R. and Savaldi-Goldstein, S. (2014) Root growth is modulated by differential hormonal sensitivity in neighboring cells. Genes Dev. 28: 912-920.
17. Fry, S.C. (1998) Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochem. J. 332: 507-515.
18. Griffiths, J.S., Tsai, A.Y., Xue, H., Voiniciuc, C., Sola, K., Seifert, G.J. et al. (2014) SALT-OVERLY SENSITIVE5 mediates Arabidopsis seed coat mucilage adherence and organization through pectins. Plant Physiol. 165: 991-1004.
19. Guo, H., Li, L., Ye, H., Yu, X., Algreen, A. and Yin, Y. (2009) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 106: 7648-7653.
20. Haruta, M., Sabat, G., Stecker, K., Minkoff, B.B. and Sussman, M.R. (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343: 408-411.
21. Hematy, K., Sado, P.E., Van Tuinen, A., Rochange, S., Desnos, T., Balzergue, S. et al. (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17: 922-931.
22. Keegstra, K., Talmadge, K.W., Bauer, W.D. and Albersheim, P. (1973) The structure of plant cell walls: III. A model of the walls of suspensioncultured sycamore cells based on the interconnections of the macromolecular components. Plant Physiol. 51: 188-197.
23. Kessler, S.A., Shimosato-Asano, H., Keinath, N.F., Wuest, S.E., Ingram, G., Panstruga, R. et al. (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330: 968-971.
24. Kohorn, B.D. and Kohorn, S.L. (2012) The cell wall-associated kinases, WAKs, as pectin receptors. Front. Plant Sci. 3: 88.
25. McKenna, S.T., Kunkel, J.G., Bosch, M., Rounds, C.M., Vidali, L., Winship, L.J. et al. (2009) Exocytosis precedes and predicts the increase in growth in oscillating pollen tubes. Plant Cell 21: 3026-3040.
26. Mendu, V., Griffiths, J.S., Persson, S., Stork, J., Downie, A.B., Voiniciuc, C. et al. (2011) Subfunctionalization of cellulose synthases in seed coat epidermal cells mediates secondary radial wall synthesis and mucilage attachment. Plant Physiol. 157: 441-453.
27. Mirabet, V., Das, P., Boudaoud, A. and Hamant, O. (2011) The role of mechanical forces in plant morphogenesis. Annu. Rev. Plant Biol. 62: 365-385.
28. Monshausen, G.B. and Haswell, E.S. (2013) A force of nature: molecular mechanisms of mechanoperception in plants. J. Exp. Bot. 64: 4663-4680.
29. Ngo, Q.A., Vogler, H., Lituiev, D.S., Nestorova, A. and Grossniklaus, U. (2014) A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev. Cell 29: 491-500.
30. Park, Y.B. and Cosgrove, D.J. (2012) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol. 158: 1933-1943.
31. Pearce, G., Moura, D.S., Stratmann, J. and Ryan, C.A. Jr (2001) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc. Natl Acad. Sci. USA 98: 12843-12847.
32. Peaucelle, A., Braybrook, S. and Hofte, H. (2012) Cell wall mechanics and growth control in plants: the role of pectins revisited. Front. Plant Sci. 3: 121.
33. Peaucelle, A., Braybrook, S.A., Le Guillou, L., Bron, E., Kuhlemeier, C. and Hofte, H. (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr. Biol. 21: 1720-1726.
34. Peaucelle, A., Louvet, R., Johansen, J.N., Hofte, H., Laufs, P., Pelloux, J. et al. (2008) Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Curr. Biol. 18: 1943-1948.
35. Pelletier, S., Van Orden, J., Wolf, S., Vissenberg, K., Delacourt, J., Ndong, Y.A. et al. (2010) A role for pectin de-methylesterification in a developmentally regulated growth acceleration in dark-grown Arabidopsis hypocotyls. New Phytol. 188: 726-739.
36. Pelloux, J., Rusterucci, C. and Mellerowicz, E.J. (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci. 12: 267-277.
37. Ralet, M.C., Crepeau, M.J., Vigouroux, J., Tran, J., Berger, A., Salle, C. et al. (2014) Mucilage attachment to Arabidopsis seeds provides evidence of a novel link between cellulose and pectin. 10e Congrès Réseau Français des Parois 7-9 July 2014, Amiens, France.
38. Rojas, E.R., Hotton, S. and Dumais, J. (2011) Chemically mediated mechanical expansion of the pollen tube cell wall. Biophys. J. 101: 1844-1853.
39. Savaldi-Goldstein, S., Peto, C. and Chory, J. (2007) The epidermis both drives and restricts plant shoot growth. Nature 446: 199-202.
40. Schopfer, P. (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J. 28: 679-688.
41. Senechal, F., Wattier, C., Rusterucci, C. and Pelloux, J. (2014) Homogalacturonan-modifying enzymes: structure, expression, and roles in plants. J. Exp. Bot. 65: 5125-5160.
42. Shih, H.W., Miller, N.D., Dai, C., Spalding, E.P. and Monshausen, G.B. (2014) The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr. Biol. 24: 1887-1892.
43. Sullivan, S., Ralet, M.C., Berger, A., Diatloff, E., Bischoff, V., Gonneau, M. et al. (2011) CESA5 is required for the synthesis of cellulose with a role in structuring the adherent mucilage of Arabidopsis seeds. Plant Physiol. 156: 1725-1739.
44. Sun, Y., Fan, X.Y., Cao, D.M., Tang, W., He, K., Zhu, J.Y. et al. (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19: 765-777.
45. Tan, L., Eberhard, S., Pattathil, S., Warder, C., Glushka, J., Yuan, C. et al. (2013) An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell 25: 270-287.
46. Uyttewaal, M., Burian, A., Alim, K., Landrein, B., Borowska-Wykret, D., Dedieu, A. et al. (2012) Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149: 439-451.
47. Vissenberg, K., Van Sandt, V., Fry, S.C. and Verbelen, J.P. (2003) Xyloglucan endotransglucosylase action is high in the root elongation zone and in the trichoblasts of all vascular plants from Selaginella to Zea mays. J. Exp. Bot. 54: 335-344.
48. Wang, M., Yuan, D., Gao, W., Li, Y., Tan, J. and Zhang, X. (2013) A comparative genome analysis of PME and PMEI families reveals the evolution of pectin metabolism in plant cell walls. PLoS One 8: e72082.
49. Winship, L.J., Obermeyer, G., Geitmann, A. and Hepler, P.K. (2010) Under pressure, cell walls set the pace. Trends Plant Sci. 15: 363-369.
50. Wolf, S., Hematy, K. and Hofte, H. (2012a) Growth control and cell wall signaling in plants. Annu. Rev. Plant Biol. 63: 381-407.
51. Wolf, S. and Hofte, H. (2014) Growth control: a saga of cell walls, ROS, and peptide receptors. Plant Cell 26: 1848-1856.
52. Wolf, S., Mravec, J., Greiner, S., Mouille, G. and Hofte, H. (2012b) Plant cell wall homeostasis is mediated by brassinosteroid feed-back signalling. Curr. Biol. 22: 1732-1737.
53. Wolf, S., van der Does, D., Ladwig, F., Sticht, C., Kolbeck, A., Schurholz, A.K. et al. (2014) A receptor-like protein mediates the response to pectin modification by activating brassinosteroid signaling. Proc. Natl Acad. Sci. USA 111: 15261-15266.
54. Yadegari, R. and Drews, G.N. (2004) Female gametophyte development. Plant Cell 16 (Suppl): S133-S141.
55. Yu, F., Qian, L., Nibau, C., Duan, Q., Kita, D., Levasseur, K. et al. (2012) FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc. Natl Acad. Sci. USA 109: 14693-14698.
56. Zablackis, E., Huang, J., Muller, B., Darvill, A.G. and Albersheim, P. (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol. 107: 1129-1138.
57. Zhao, Z., Crespi, V.H., Kubicki, J.D., Cosgrove, D.J. and Zhong, L. (2013) Molecular dynamics simulation study of xyloglucan adsorption on cellulose surfaces: effects of surface hydrophobicity and side-chain variation. Cellulose 21: 1025-1039.
58. Zhu, J.Y., Sae-Seaw, J. and Wang, Z.Y. (2013) Brassinosteroid signalling. Development 140: 1615-1620.
59. Zykwinska, A.W., Ralet, M.C., Garnier, C.D. and Thibault, J.F. (2005) Evidence for in vitro binding of pectin side chains to cellulose. Plant Physiol. 139: 397-407.