The Arabidopsis MUM2 gene encodes a β-galactosidase required for the production of seed coat mucilage with correct hydration properties

Plant Cell

Volumn 19, Issue 12, 2007, Pages 4007-4021

  Dean, Gillian H ^a   Zheng, Huanquan ^a,d   Tewari, Jagdish ^b,e   Huang, Jun ^a   Young, Diana S ^a   Yeen, Ting Hwang ^a   Western, Tamara L ^a,d   Carpita, Nicholas C ^c   McCann, Maureen C ^b   Mansfield, Shawn D ^a   Haughn, George W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b PURDUE UNIVERSITY   (United States)

^c PURDUE UNIVERSITY   (United States)

^d MCGILL UNIVERSITY   (Canada)

^e Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOACTIVITY; HYDRATION; PHYSICAL PROPERTIES; PLANT CELL CULTURE; SEED;

ARABIDOPSIS; PECTINACEOUS MUCILAGE; SEED COAT;

GENE ENCODING;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 39149119914     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.050609     Document Type: Article

References (60)

1. Ahn, Y.O., Zheng, M., Bevan, D.R., Esen, A., Shiu, S.H., Benson, J., Peng, H.P., Miller, J.T., Cheng, C.L., Poulton, J.E., Shih, M.C. (2007). Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 35. Phytochemistry 68: 1510-1520.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
4. Balasubramaniam, S., Lee, H.C., Lazan, H., Othman, R., and Ali, Z.M. (2005). Purification and properties of a β-galactosidase from carambola fruit with significant activity towards cell wall polysaccharides. Phytochemistry 66: 153-163.
5. Batoko, H., Zheng, H.Q., Hawes, C., and Moore, I. (2000). A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12: 2201-2217.
6. Beeckman, T., De Rycke, R., Viane, R., and Inzé, D. (2000). Histological study of seed coat development in Arabidopsis thaliana. J. Plant Res. V113: 139-148.
7. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340: 783-795.
8. Blanchard, J.E., Gal, L., He, S., Foisy, J., Warren, R.A., and Withers, S.G. (2001). The identification of the catalytic nucleophiles of two β-galactosidases from glycoside hydrolase family 35. Carbohydr. Res. 333: 7-17.
9. Brummell, D.A. (2006). Cell wall disassembly in ripening fruit. Funct. Plant Biol. 33: 103-119.
10. Carpita, N.C., and McCann, M.C. (1996). Some new methods to study plant polyuronic acids and their esters. In Progress in Glycobiology, R. Townsend and A. Hotchkiss, eds (New York: Marcel Dekker), pp. 595-611.
11. Carpita, N.C., and Shea, D. (1989). Linkage structure of carbohydrates by gas chromatograph-mass spectrometry (GC-MS) of partially methylated alditol acetates. In Analysis of Carbohydrates by GLC and MS, C.J. Biermann and G.D. McGinnis, eds (Boca Raton, FL: CRC Press), pp. 155-216.
12. Chen, L., Carpita, N.C., Reiter, W.D., Wilson, R.H., Jeffries, C., and McCann, M.C. (1998). A rapid method to screen for cell-wall mutants using discriminant analysis of Fourier transform infrared spectra. Plant J. 16: 385-392.
13. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G., and Thompson, J.D. (2003). Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31: 3497-3500.
14. 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.
15. Coutinho, P.M., and Henrissat, B. (2006). Carbohydrate-active enzymes: An integrated database approach. In Recent Advances in Carbohydrate Bioengineering, H.J. Gilbert, G. Davies, B. Henrissat, and B. Svensson, eds (Cambridge, UK: Royal Society of Chemistry), pp. 3-12.
16. Crombie, H.J., Chengappa, S., Hellyer, A., and Reid, J.S.G. (1998). A xyloglucan oligosaccharide-active, transglycosylating-D-glucosidase from the cotyledons of nasturtium (Tropaeolum majus L.) seedlings - Purification, properties and characterization of a cDNA clone. Plant J. 15: 27-38.
17. de Alcantara, P.H.N., Dietrich, S.M.C., and Buckeridge, M.S. (1999). Xyloglucan mobilisation and purification of a (XLLG/XLXG) specific β-galactosidase from cotyledons of Copaifera langsdorffii. Plant Physiol. Biochem. 37: 653-663.
18. Edwards, M., Bowman, Y.J., Dea, I.C., and Reid, J.S. (1988). A β-D-galactosidase from nasturtium (Tropaeolum majus L.) cotyledons. Purification, properties, and demonstration that xyloglucan is the natural substrate. J. Biol. Chem. 263: 4333-4337.
19. Fanutti, C., Gidley, M.J., and Reid, G.J.S. (1991). A xyloglucanoligosaccharide-specific α-D-xylosidase or exo-oligoxyloglucana- xylohydrolase from germinated nasturtium (Tropaeolum majus L.) seeds. Planta 184: 137-147.
20. Fanutti, C., Gidley, M.J., and Reid, J.S.G. (1993). Action of a pure xyloglucan endo-transglycosylase (formerly called xyloglucan-specific endo-(1→4)-beta-D-glucanase) from the cotyledons of germinated nasturtium seeds. Plant J. 3: 691-700.
21. Finn, R.D., et al. (2006). Pfam: Clans, web tools and services. Nucleic Acids Res. 34: D247-D251.
22. Fry, S.C. (2000). The Growing Plant Cell Wall: Chemical and Metabolic Analysis. (Caldwell, NJ: The Blackburn Press).
23. Gibeaut, D.M., and Carpita, N.C. (1991). Cleanup procedure for partially methylated alditol acetate derivatives of polysaccharides. J. Chromatogr. 587: 284-287.
24. Hanke, D.E., and Northcote, D.H. (1975). Molecular visualisation of pectin and DNA by ruthenium red. Biopolymers 14: 1-17.
25. Haughn, G., and Chaudhury, A. (2005). Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci. 10: 472-477.
26. Haughn, G.W., and Somerville, C. (1986). Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol. Gen. Genet. 204: 430-434.
27. Henrissat, B., Callebaut, I., Fabrega, S., Lehn, P., Mornon, J.-P., and Davies, G. (1995). Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. Proc. Natl. Acad. Sci. USA 92: 7090-7094.
28. Hoekema, A., Hirsch, P.R., Hooykaas, P.J.J., and Schilperoort, R.A. (1983). A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303: 179-180.
29. Iglesias, N., Abelenda, J.A., Rodiño, M., Sampedro, J., Revilla, G., and Zarra, I. (2006). Apoplastic glycosidases active against xyloglucan oligosaccharides of Arabidopsis thaliana. Plant Cell Physiol. 47: 55-63.
30. Jander, G., Norris, S.R., Rounsley, S.D., Bush, D.F., Levin, I.M., and Last, R.L. (2002). Arabidopsis map-based cloning in the post-genome era. Plant Physiol. 129: 440-450.
31. Kacurácová, M., Capek, P., Sasinková, V., Wellner, N., and Ebringerová, A. (2000). FT-IR study of plant cell wall model compounds: Pectic polysaccharides and hemicelluloses. Carbohydr Polym. 43: 195-203.
32. Kim, J.B., and Carpita, N.C. (1992). Changes in esterification of the uronic-acid groups of cell-wall polysaccharides during elongation of maize coleoptiles. Plant Physiol. 98: 646-653.
33. Knox, J.P. (2002). Cell and developmental biology of pectins. In Pectins and Their Manipulation, G.B. Seymour and J.P. Knox, eds (Boca Raton, FL: CRC Press), pp. 131-149.
34. Kotake, T., Dina, S., Konishi, T., Kaneko, S., Igarashi, K., Samejima, M., Watanabe, Y., Kimura, K., and Tsumuraya, Y. (2005). Molecular cloning of a β-galactosidase from radish that specifically hydrolyzes β-(1→3)- and β-(1→6)-galactosyl residues of arabinogalactan protein. Plant Physiol. 138: 1563-1576.
35. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
36. Lamport, D.T.A., Kieliszewski, M.J., and Showalter, A.M. (2006). Salt stress upregulates periplasmic arabinogalactan proteins: Using salt stress to analyse AGP function. New Phytol. 169: 479-492.
37. Lazan, H., Ng, S.Y., Goh, L.Y., and Ali, Z.M. (2004). Papaya β-galactosidase/galactanase isoforms in differential cell wall hydrolysis and fruit softening during ripening. Plant Physiol. Biochem. 42: 847-853.
38. Macquet, A., Ralet, M.C., Kronenberger, J., Marion-Poll, A., and North, H.M. (2007a). In-situ, chemical and macromolecular study of the composition of Arabidopsis thaliana seed coat mucilage. Plant Cell Physiol. 48: 984-999.
39. Macquet, A., Ralet, M.-C., Loudet, O., Kronenberger, J., Mouille, G., Marion-Poll, A., and North, H.M. (2007b). A naturally occurring mutation in an Arabidopsis accession affects a β-D-galactosidase that increases the hydrophilic potential of rhamnogalacturonan I in seed mucilage. Plant Cell 19: 3990-4006.
40. McCartney, L., and Knox, J.P. (2002). Regulation of pectic polysaccharide domains in relation to cell development and cell properties in the pea testa. J. Exp. Bot. 53: 707-713.
41. Mulder, N.J., et al. (2005). InterPro, progress and status in 2005. Nucleic Acids Res. 33: D201-D205.
42. O'Neill, M.A., and York, W.S. (2003). The composition and structure of plant primary cell walls. In The Plant Cell Wall, J.K.C. Rose, ed (Boca Raton, FL: CRC Press), pp. 1-54.
43. 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.
44. Pressey, R. (1983). β-Galactosidases in ripening tomatoes. Plant Physiol. 71: 132-135.
45. Ridley, B.L., O'Neill, M.A., and Mohnen, D. (2001). Pectins: Structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57: 929-967.
46. Rose, J.K.C., Catalá, C., Gonzalez-Carranza, Z.H., and Roberts, J.A. (2003). Cell wall disassembly. In The Plant Cell Wall, J.K.C. Rose, ed (Boca Raton, FL: CRC Press), pp. 264-324.
47. Schultz, C., Gilson, P., Oxley, D., Youl, J., and Bacic, A. (1998). GPI-anchors on arabinogalactan-proteins: Implications for signalling in plants. Trends Plant Sci. 3: 426-431.
48. Selvendran, R.R., and Ryden, P. (1990). Isolation and analysis of plant cell walls. In Methods in Plant Biochemistry, Vol. 2: Carbohydrates, P.M. Dey and J.B. Harbourne, eds (San Diego, CA: Academic Press), pp. 549-575.
49. Showalter, A.M. (2001). Arabinogalactan-proteins: structure, expression and function. Cell. Mol. Life Sci. 58: 1399-1417 (CMLS).
50. Usadel, B., Kuschinsky, A.M., Rosso, M.G., Eckermann, N., and Pauly, M. (2004). RHM2 is involved in mucilage pectin synthesis and is required for the development of the seed coat in Arabidopsis. Plant Physiol. 134: 286-295.
51. Vincken, J.P., Schols, H.A., Oomen, R.J.F.J., McCann, M.C., Ulvskov, P., Voragen, A.G.J., and Visser, R.G.F. (2003). If Homogalacturonan were a side chain of Rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiol. 132: 1781-1789.
52. 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.
53. 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.
54. 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.
55. Western, T.L., Young, D.S., Dean, G.H., Tan, W.L., Samuels, A.L., and Haughn, G.W. (2004). MUCILAGE-MODIFIED4 encodes a putative pectin biosynthetic enzyme developmentally regulated by APETALA2, TRANSPARENT TESTA GLABRA1, and GLABRA2 in the Arabidopsis seed coat. Plant Physiol. 134: 296-306.
56. Willats, W.G.T., McCartney, L., and Knox, J.P. (2001a). In-situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana. Planta 213: 37-44.
57. Willats, W.G.T., McCartney, L., Mackie, W., and Knox, J.P. (2001b). Pectin: Cell biology and prospects for functional analysis. Plant Mol. Biol. 47: 9-27.
58. 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.
59. Zheng, H., Kunst, L., Hawes, C., and Moore, I. (2004). A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus. Plant J. 37: 398-414.
60. Zheng, H., Rowland, O., and Kunst, L. (2005). Disruptions of the Arabidopsis enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. Plant Cell 17: 1467-1481.