Cellulose synthesis via the FEI2 RLK/SOS5 pathway and CELLULOSE SYNTHASE 5 is required for the structure of seed coat mucilage in Arabidopsis

Plant Journal

Volumn 68, Issue 6, 2011, Pages 941-953

  Harpaz Saad, Smadar ^a   McFarlane, Heather E ^b,c   Xu, Shouling ^a   Divi, Uday K ^b   Forward, Bronwen ^b   Western, Tamara L ^b   Kieber, Joseph J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

AGP; cellulose; mucilage; pectin; receptor like kinases; seed

Indexed keywords

AGP; ARABIDOPSIS; ARABIDOPSIS ROOTS; ARABIDOPSIS THALIANA; CELLULOSE SYNTHASE; CELLULOSE SYNTHESIS; EXTRACELLULAR; GPI-ANCHORED PROTEIN; INNER LAYER; ISOFORMS; MUCILAGE; PECTIN; PRIMARY CELL WALL; RECEPTOR-LIKE KINASE; SECRETORY CELLS; SEED COATS; SEED DEVELOPMENT; SEED SURFACES;

BIOSYNTHESIS; CELL CULTURE; CELLULOSE; ENZYMES; FLOWCHARTING; HYDRATION; PLANTS (BOTANY); SEED;

ADHESIVES;

ARABIDOPSIS PROTEIN; CELL SURFACE RECEPTOR; CELLULOSE; CELLULOSE SYNTHASE; GLUCOSYLTRANSFERASE; PECTIN; PROTEIN SERINE THREONINE KINASE;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PLANT GENE; PLANT ROOT; PLANT SEED;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOSYNTHETIC PATHWAYS; CELLULOSE; GENE EXPRESSION; GENES, PLANT; GLUCOSYLTRANSFERASES; MUTATION; PECTINS; PLANT ROOTS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; SEEDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 83555163697     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04760.x     Document Type: Article

References (46)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657. (Pubitemid 36927950)
2. Anderson, C.T., Carroll, A., Akhmetova, L., and, Somerville, C., (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol. 152, 787-796.
3. Arsovski, A.A., Popma, T.M., Haughn, G.W., Carpita, N.C., McCann, M.C., and, Western, T.L., (2009) AtBXL1 encodes a bifunctional β-d-xylosidase/ α-l-arabinofuranosidase required for pectic rabinan modification in Arabidpsis mucilage secretory cells. Plant Physiol. 150, 1219-1234.
4. 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.
5. Beeckman, T., Przemeck, G.K.H., Stamatiou, G., Lau, R., Terryn, N., De Rycke, R., Inze, D., and, Berleth, T., (2002) Genetic complexity of cellulose synthase A gene function in Arabidopsis embryogenesis. Plant Physiol. 130, 1883-1893. (Pubitemid 36035185)
6. Blake, A.W., McCartney, L., Flint, J.E., Bolam, D.N., Boraston, A.B., Gilbert, H.J., and, Knox, J.P., (2006) Understanding the biological rationale for the diversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes. J. Biol. Chem. 281, 29321-29329. (Pubitemid 44507075)
7. 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. (Pubitemid 47502958)
8. Dubois, M., Gilled, K., Hamilton, J.K., Rebers, P.A., and, Smith, F., (1956) Colorimetric method for the determination of sugars and related substances. Anal. Chem. 28, 350-356.
9. Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., McCann, M., Rayon, C., Vernhettes, S., and, Höfte, H., (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell, 12, 2409-2424.
10. Guerriero, G., Fugelstad, J., and, Bulone, V., (2010) What do we really know about cellulose biosynthesis in higher plants? J. Integr. Plant Biol. 52, 161-175.
11. 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.
12. Gutterman, Y., and, Shem-Tov, S., (1996) Structure and function of the mucilaginous seed coats of Plantago coronopus inhabiting the Negev Desert of Israel. J. Plant Sci. 44, 125-133. (Pubitemid 27040160)
13. Hanke, D.E., and, Northcote, D.H., (1975) Molecular visualization of pectin and DNA by ruthenium red. Biopolymers, 14, 1-17.
14. Harholt, J., Suttangkakul, A., and, Vibe Scheller, H., (2010) Biosynthesis of pectin. Plant Physiol. 153, 384-395.
15. Haughn, G., and, Chaudhury, A., (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci. 10, 472-477. (Pubitemid 41395268)
16. Hématy, K., and, Höfte, H., (2008) Novel receptor kinases involved in growth regulation. Curr. Opin. Plant Biol. 11, 321-328.
17. Huang, J., Bowles, D., Esfandiari, E., Dean, G., Carpita, N.C., and, Haughn, G.W., (2011) The Arabidopsis transcription factor LUH/MUM1 is required for extrusion of seed coat mucilage. Plant Physiol. 156, 491-502.
18. Le, B.H., Cheng, C., Bui, A.Q., et al. (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl Acad. Sci. USA, 107, 8063-8070.
19. Macquet, A., Ralet, M.-C., Kronenberger, J., Marion-Poll, A., and, North, H.M., (2007) In situ, chemical and macromolecular study of the composition of Arabidopsis thaliana seed coat mucilage. Plant Cell Physiol. 48, 984-999. (Pubitemid 47216629)
20. Mutwil, M., Debolt, S., and, Persson, S., (2008) Cellulose synthesis: a complex complex. Curr. Opin. Plant Biol. 11, 252-257.
21. Naran, R., Chen, G., and, Carpita, N.C., (2008) Novel rhamnogalacturonan I and arabinoxylan polysaccharides of flax seed mucilage. Plant Physiol. 148, 132-141. (Pubitemid 352847582)
22. Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H., and, Höfte, H., (1998) A plasma membrane-bound putative endo-1,4-β-d- glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17, 5563-5576. (Pubitemid 28445968)
23. Pattathil, S., Avci, U., Baldwin, D., et al. (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol. 153, 514-525.
24. Penfield, S., Meissner, R.C., Shoue, D.A., Carpita, N.C., and, Bevan, M.W., (2001) MYB61 is required for mucilage deposition and extrusion in the Arabidopsis seed coat. Plant Cell, 13, 2777-2791. (Pubitemid 34088640)
25. Persson, S., Paredez, A., Carroll, A., Palsdottir, H., Doblin, M., Poindexter, P., Khitrov, N., Auer, M., and, Somerville, C.R., (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc. Natl Acad. Sci. USA, 104, 15566-15571. (Pubitemid 47502957)
26. Rautengarten, C., Usadel, B., Neumetzler, L., Hartmann, J., Büssis, D., and, Altmann, T., (2008) A subtilisin-like serine protease essential for mucilage release from Arabidopsis seed coats. Plant J. 54, 466-480. (Pubitemid 351585493)
27. Sato, S., Kato, T., Kakegawa, K., et al. (2001) Role of the putative membrane-bound endo-1,4-β-gucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol. 42, 251-263. (Pubitemid 32320196)
28. Schindelman, G., Morikami, A., Jung, J., Baskin, T.I., Carpita, N.C., Derbyshire, P., McCann, M.C., and, Benfey, P.N., (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev. 15, 1115-1127. (Pubitemid 32417304)
29. Shi, H., Kim, Y., Guo, Y., Stevenson, B., and, Zhu, J.-K., (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell, 15, 19-32. (Pubitemid 36137659)
30. Somerville, C., (2006) Cellulose synthesis in higher plants. Annu. Rev. Cell. Dev. Biol. 22, 53-78.
31. Steinwand, B.J., and, Kieber, J.J., (2010) The role of receptor-like kinases in regulating cell wall function. Plant Physiol. 153, 479-484.
32. Stork, J., Harris, D., Griffiths, J., Williams, B., Beisson, F., Li-Beisson, Y., Mendu, V., Haughn, G., and, DeBolt, S., (2010) CELLULOSE SYNTHASE9 serves a nonredundant role in secondary cell wall synthesis in Arabidopsis epidermal testa cells. Plant Physiol. 153, 580-589.
33. Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K., and, Turner, S.R., (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl Acad. Sci. USA, 100, 1450-1455. (Pubitemid 36184022)
34. Turner, S.R., and, Somerville, C.R., (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell, 9, 689-701. (Pubitemid 28104500)
35. Walker, M., Tehseen, M., Doblin, M.S., Pettolino, F.A., Wilson, S.M., Bacic, A., and, Golz, J.F., (2011) The transcriptional regulator LEUNIG-HOMOLOG regulates mucilage release from the Arabidopsis testa. Plant Physiol. 156, 46-60.
36. Western, T.L., (2006) Changing spaces: the Arabidopsis mucilage secretory cells as a novel system to dissect cell wall production in differentiating cells. Can. J. Bot. 84, 622-630. (Pubitemid 44310416)
37. Western, T.L., Skinner, D.J., and, Haughn, G.W., (2000) Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiol. 122, 345-356.
38. Western, T.L., Burn, J., Tan, W.L., Skinner, D.J., Martin-McCaffrey, L., Moffatt, B.A., and, Haughn, G.W., (2001) Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in Arabidopsis. Plant Physiol. 127, 998-1011. (Pubitemid 33112160)
39. Willats, W.G.T., McCartney, L., and, Knox, J.P., (2001) In-situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana. Planta, 213, 37-44. (Pubitemid 32507449)
40. Windsor, J.B., Symonds, V.V., Mendenhall, J., and, Lloyd, A.M., (2000) Arabidopsis seed coat development: morphological differentiation of the outer integument. Plant J. 22, 483-493. (Pubitemid 30427757)
41. 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.
42. Xu, S.L., Rahman, A., Baskin, T.I., and, Kieber, J.J., (2008) Two leucine-rich repeat receptor kinases mediate signaling linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell, 20, 3065-3079.
43. Young, R.E., McFarlane, H.E., Hahn, M.G., Western, T.L., Haughn, G.W., and, Samuels, A.L., (2008) Analysis of the Golgi apparatus in Arabidopsis seed coat cells during polarized secretion of pectin-rich mucilage. Plant Cell, 20, 1623-1638. (Pubitemid 352844167)
44. Zuo, J., Niu, Q., Nishizawa, N., Wu, Y., Kost, B., and, Chua, N., (2000) KORRIGAN, an Arabidopsis endo-1,4-β-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell, 12, 1137-1152. (Pubitemid 30622718)
45. Zykwinska, A.W., Ralet, M.-C.J., Garnier, C.D., and, Thibault, J.-F.J., (2005) Evidence for in vitro binding of pectin side chains to cellulose. Plant Physiol. 139, 397-407. (Pubitemid 43951622)
46. Zykwinska, A., Gaillard, C., Buléon, A., Pontoire, B., Garnier, C., Thibault, J.-F., and, Ralet, M.-C., (2006) Assessment of in vitro binding of isolated pectic domains to cellulose by adsorption isotherms, electron microscopy, and x-ray diffraction methods. Biomacromolecules, 8, 223-232. (Pubitemid 46140496)