Skip to main content
Log in

Plant callose synthase complexes

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Synthesis of callose (β-1,3-glucan) in plants has been a topic of much debate over the past several decades. Callose synthase could not be purified to homogeneity and most partially purified cellulose synthase preparations yielded β-1,3-glucan in vitro, leading to the interpretation that cellulose synthase might be able to synthesize callose. While a rapid progress has been made on the genes involved in cellulose synthesis in the past five years, identification of genes for callose synthases has proven difficult because cognate genes had not been identified in other organisms. An Arabidopsis gene encoding a putative cell plate-specific callose synthase catalytic subunit (CalS1) was recently cloned. CalS1 shares high sequence homology with the well-characterized yeast β-1,3-glucan synthase and transgenic plant cells over-expressing CalS1 display higher callose synthase activity and accumulate more callose. The callose synthase complex exists in at least two distinct forms in different tissues and interacts with phragmoplastin, UDP-glucose transferase, Rop1 and, possibly, annexin. There are 12 CalS isozymes in Arabidopsis, and each may be tissue-specific and/or regulated under different physiological conditions responding to biotic and abiotic stresses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  • Amor, Y., Haigler, C.H., Johnson, S., Wainscott, M. and Delmer, D.P. 1995. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc. Natl. Acad. Sci. USA 92: 9353–9357.

    Google Scholar 

  • Arioli, T., Peng, L., Betzner, A.S., Burn, J., Wittke, W., Herth, W., Camilleri, C., Hofte, H., Plazinski, J., Birch, R., Cork, A., Glover, J., Redmond, J. and Williamson, R.E. 1998. Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279: 717–720.

    Google Scholar 

  • Carpita, N. and Vergara, C. 1998. A recipe for cellulose. Science 279: 672–673.

    Google Scholar 

  • Cui, X., Shin, H. and Brown, M. 1999. A novel gene from cotton shows homology to the yeast β-1,3-glucan synthase subunit FKS1. Abstracts of the meeting of the American Society of Plant Physiology (Baltimore, MD), p.62.

  • Delmer, D.P. 1999. Cellulose biosynthesis: exciting times for a difficult field of study. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 245–276.

    Google Scholar 

  • Delmer, D.P., Solomon, M. and Read, S.M. 1991. Direct photolabeling with [32P]UDP-glucose for identification of a subunit of cotton fiber callose synthase. Plant Physiol. 95: 556–563.

    Google Scholar 

  • Dhugga, K.S. and Ray, P.M. 1994. Purification of 1,3-β-D-glucansynthase activity from pea tissue: two polypeptides of 55 kDa and 70 kDa copurify with enzyme activity. Eur. J. Biochem. 220: 943–953.

    Google Scholar 

  • Doblin, M.S., De Melis, L., Newbigin, E., Bacic, A. and Read, S.M. 2001. Pollen tubes of Nicotiana alata express two genes from different β-glucan synthase families. Plant Physiol. 125: 2040–2052.

    Google Scholar 

  • Douglas, C.M., Foor, F., Marrinan J.A., Morin, N., Nielsen, J.B., Dahl, A.M., Mazur, P., Baginsky, W., Li, W., El-Sherbeini, M., Clemas, J.A., Mandala, S.M., Frommer, E.R. and Kurtz, M.B. 1994. The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-β-D-glucansynthase. Proc. Natl. Acad. Sci. USA 91: 12907–12911.

    Google Scholar 

  • Dumas, C. and Knox, R.B. 1983. Callose and determination of pistil viability and incompatibility. Theor. Appl. Genet. 67: 1–10.

    Google Scholar 

  • el-Sherbeini, M. and Clemas, J.A. 1995. Cloning and characterization of GNS1: a Saccharomyces cerevisiae gene involved in synthesis of 1,3-β-glucan in vitro.J. Bact. 177: 3227–3234.

    Google Scholar 

  • Frost, D.J., Read, S.M., Drake, R.R., Haley, B.E. and Wasserman, B.P. 1990. Identification of the UDP-glucose-binding polypeptide of callose synthase from Beta vulgaris L. by photoaffinity labeling with 5-azido-UDP-glucose. J. Biol. Chem. 265: 2162–2167.

    Google Scholar 

  • Fu, Y., Wu, G. Yang, Z. 2001. Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J. Cell Biol. 152: 1019–1032.

    Google Scholar 

  • Gibeaut, D.M. and Carpita, N.C. 1994. Biosynthesis of plant cell wall polysaccharides. FASEB J. 8: 904–915.

    Google Scholar 

  • Gu, X. and Verma, D.P.S. 1996. Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants. EMBO J. 15: 695–704.

    Google Scholar 

  • Gu, X. and Verma, D.P.S. 1997. Dynamics of phragmoplastin in living cells during cell plate formation and uncoupling of cell elongation from the plane of cell division. Plant Cell 9: 157–169.

    Google Scholar 

  • Heinemann, U., Ay, J., Gaiser, O., Muller, J.J. and Ponnuswamy, M.N. 1996. Enzymology and folding of natural and engineered bacterial β-glucanases studied by X-ray crystallography. J. Biol. Chem. 377: 447–454.

    Google Scholar 

  • Henrissat, B. and Davies, G.J. 2000. Glycoside hydrolases and glycosyltransferases. Families, modules, and implications for genomics. Plant Physiol. 124: 1515–1519.

    Google Scholar 

  • Hoj, P.B. and Fincher, G.B. 1995. Molecular evolution of plant β–glucan endohydrolases. Plant J. 7: 367–379.

    Google Scholar 

  • Holland, N., Holland, D., Helentjaris, T., Dhugga, K.S., Xoconostle-Cazares, B. and Delmer, D.P. 2000. A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol. 123: 1313–1324.

    Google Scholar 

  • Hong, Z., Delauney, A.J. and Verma, D.P.S. 2001. A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell 13: 755–768.

    Google Scholar 

  • Hong, Z., Zhang, Z., Olson, J.M. and Verma, D.P.S. 2001. A novel UDP-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate. Plant Cell 13: 769–779.

    Google Scholar 

  • Hu, C.A., Delauney, A.J. and Verma, D.P. 1992. A bifunctional enzyme (Δ1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc. Natl. Acad. Sci. USA 89: 9354–9358.

    Google Scholar 

  • Jacob, S.R. and Northcote, D.H. 1985. In vitro glucan synthesis by membranes of celery petioles: the role of the membrane in determining the type of linkage formed. J. Cell Sci. Suppl. 2: 1–11.

    Google Scholar 

  • Kamat, U., Garg, R. and Sharma, C.B. 1992. Purification to homogeneity and characterization of a 1,3-β-glucan (callose) synthase from germinating Arachis hypogaea cotyledons. Arch. Biochem. Biophys. 298: 731–739.

    Google Scholar 

  • Kauss, H. 1996. Callose synthesis. In: M. Smallwood, J.P. Knox and D.J. Bowles (Eds.) Membranes: Specialized Functions in Plants, Bios Scientific Publishers, Guildford, UK, pp. 77–92.

    Google Scholar 

  • Kelly, R., Register, E., Hsu, M.J., Kurtz, M. and Nielsen, J. 1996. Isolation of a gene involved in 1,3-β-glucan synthesis in Aspergillus nidulans and purification of the corresponding protein. J. Bact. 178: 4381–4391.

    Google Scholar 

  • Kudlicka, K. and Brown, R.M. 1997. Cellulose and callose biosynthesis in higher plants. I. Solubilization and separation of (1→3)-and (1→4)-β-glucan synthase activities from mung bean. Plant Physiol. 115: 643–656.

    Google Scholar 

  • Li, H., Bacic, A. and Read, S.M. 1997. Activation of pollen tube callose synthase by detergents: evidence for different mechanisms of action. Plant Physiol. 114: 1255–1265.

    Google Scholar 

  • Li, H., Lin, Y., Heath, R.M., Zhu, M.X. and Yang, Z. 1999. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11: 1731–1742.

    Google Scholar 

  • Li, L. and Brown, R.M, Jr. 1993. β-Glucan synthesis in the cotton fiber. II. Regulation and kinetic properties of-βglucan synthases. Plant Physiol. 101: 1143–1148.

    Google Scholar 

  • Lukowitz, W., Nickle, T.C., Meinke, D.W., Last, R.L., Con-klin, P.L. and Somerville, C.R. 2001. Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc. Natl. Acad. Sci. USA 98: 2262–2267.

    Google Scholar 

  • Matthysse, A.G., White, S. and Lightfoot, R. 1995. Mechanism of cellulose synthesis in Agrobacterium tumefaciens. J. Bact. 177: 1076–1081.

    Google Scholar 

  • Mazur, P., Morin, N., Baginsky, W., el-Sherbeini, M., Clemas, J.A., Nielsen, J.B. and Foor, F. 1995. Differential expression and function of two homologous subunits of yeast 1,3-β-D-glucan synthase. Mol. Cell. Biol. 15: 5671–5681.

    Google Scholar 

  • McCormack, B.A., Gregory, A.C., Kerry, M.E., Smith, C. and Bolwell, G.P. 1997. Purification of an elicitor induced glucan synthase (callose synthase) from suspension cultures of French bean (Phaseolus vulgaris): purification and immunolocation of a probable Mr-65000 subunit of the enzyme. Planta 203: 196–203.

    Google Scholar 

  • Nakai, T., Tonouchi, N., Konishi, T., Kojima, Y., Tsuchida, T., Yoshinaga, F., Sakai, F. and Hayashi, T. 1999. Enhancement of cellulose production by expression of sucrose synthase in Acetobacter xylinum. Proc. Natl. Acad. Sci. USA 96: 14–18.

    Google Scholar 

  • Pear, J.R., Kawagoe, Y., Schreckengost, W.E., Delmer, D.P. and Stalker, D.M. 1996. Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc. Natl. Acad. Sci. USA 93: 12637–12642.

    Google Scholar 

  • Qadota, H., Python, C.P., Inoue, S.B., Arisawa, M., Anraku, Y., Zheng, Y., Watanabe, T., Levin, D.E. and Ohya, Y. 1996. Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-β-glucan synthase. Science 272: 279–281.

    Google Scholar 

  • Read, S.M. and Delmer, D.P. 1987. Inhibition of mung bean UDP-glucose: (1→3)-β-glucan synthase by UDP-pyridoxal: evidence for an active-site amino group. Plant Physiol. 85: 1008–1015.

    Google Scholar 

  • Richmond, T.A. and Somerville, C.R. 2001. The cellulose synthase superfamily. Plant Physiol. 124: 495–498.

    Google Scholar 

  • Samuels, A.L., Giddings, T.H. and Staehelin, L.A. 1995. Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J. Cell Biol. 130: 1345–1357.

    Google Scholar 

  • Saxena, I.M. and Brown, R.M. Jr. 2000. Cellulose synthases and related enzymes. Curr. Opin. Plant Biol. 3: 523–531.

    Google Scholar 

  • Saxena, I.M., Brown, R.M. Jr., Fevre, M., Geremia, R.A. and Henrissat, B. 1995.Multidomain architecture of β-glycosyl transferases: implications for mechanism of action. J. Bact. 177: 1419–1424.

    Google Scholar 

  • Scherp, P., Grotha, R. and Kutschera, U. 2001. Occurrence and phylogenetic significance of cytokinesis-related callose in green algae, bryophytes, ferns and seed plants. Plant Cell Rep. 20: 143–149.

    Google Scholar 

  • Schlupmann, H., Bacic, A. and Read, S.R. 1993. A novel callose synthase from pollen tubes of Nicotiana. Planta 191: 470–481.

    Google Scholar 

  • Shin, H. and Brown, R.M. 1999. GTPase activity and biochemical characterization of a recombinant cotton fiber annexin. Plant Physiol. 119: 925–934.

    Google Scholar 

  • Stasinopoulos, S.J., Fisher, P.R., Stone, B.A. and Stanisich, V.A. 1999. Detection of two loci involved in (1→3)-β-glucan (curdlan) biosynthesis by Agrobacterium sp. ATCC31749, and comparative sequence analysis of the putative curdlan synthase gene. Glycobiology 9: 31–41.

    Google Scholar 

  • Stone, B.A. and Clarke, A.E. 1992. Chemistry and physiology of higher plant 1,3-β-glucans (callose). In: B.A. Stone and A.E. Clarke (Eds.) Chemistry and Biology of (1-3)-β–Glucans, La Trobe University Press, Bundoora, Australia, pp. 365–429.

    Google Scholar 

  • Subbaiah, C.C. and Sachs, M.M. 2001. Altered patterns of sucrose synthase phosphorylation and localization precede callose induction and root tip death in anoxic maize seedlings. Plant Physiol. 125: 585–594.

    Google Scholar 

  • Taylor, N.G., Laurie, S. and Turner, S.R. 2000. Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12: 2529–2540.

    Google Scholar 

  • Taylor, N.G., Scheible, W.R., Cutler, S., Somerville, C.R. and Turner, S.R. 1999. The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11: 769–780.

    Google Scholar 

  • Turner, A., Bacic, A., Harris, P.J. and Read, S.M. 1998. Membrane fractionation and enrichment of callose synthase from pollen tubes of Nicotiana alata Link et Otto. Planta 205: 380–388.

    Google Scholar 

  • Verma, D.P.S. 2001. Cytokinesis and building of the cell plate in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 751–784.

    Google Scholar 

  • Wasserman, B.P., Wu, A. and Harriman, R.W. 1992. Probing the molecular architecture of (1,3)-β-glucan (callose) synthase: polypeptide depletion studies. Biochem. Soc. Trans. 20: 18–22.

    Google Scholar 

  • Wu, L., Joshi, C.P. and Chiang, V.L. 2000. A xylem-specific cellulose synthase gene from aspen (Populus tremuloides) is responsive to mechanical stress. Plant J. 22: 495–502.

    Google Scholar 

  • Zhang, Z., Hong, Z. and Verma, D.P.S. 2000. Phragmoplastin polymerizes into spiral coiled structures via intermolecular interaction of two self-assembly domains. J. Biol. Chem. 275: 8779–8784.

    Google Scholar 

  • Zheng, Z.L. and Yang, Z. 2000. The Rop GTPase: an emerging signaling switch in plants. Plant Mol Biol. 44: 1–9.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verma, D.P.S., Hong, Z. Plant callose synthase complexes. Plant Mol Biol 47, 693–701 (2001). https://doi.org/10.1023/A:1013679111111

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1013679111111

Navigation