Abstract
Traditionally, calmodulin (CaM) was thought to be a multi-functional receptor for intracellular Ca2+ signals. But in the last ten years, it was found that CaM also exists and acts extracellularly in animal and plant cells to regulate many important physiological functions. Laboratory studies by the authors showed that extracellular CaM in plant cells can stimulate the proliferation of suspension cultured cell and protoplast; regulate pollen germination and pollen tube elongation, and stimulate the light-independent gene expression of Rubisco small subunit (rbcS). Furthermore, we defined the trans-membrane and intracellular signal transduction pathways for extracellular CaM by using a pollen system. The components in this pathway include heterotrimeric G-protein, phospholipase C, IP3, calcium signal and protein phosphorylation etc. Based on our findings, we suggest that extracellular CaM is a polypeptide signal in plants. This idea strongly argues against the traditional concept that there is no intercellular polypeptide signal in plants.
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Cheng, W. Y., Cyclic 3′, 5′-nucleotide phosphodiestrase: demonstration of an activator, Biochm. Biophys. Res. Commun., 1970, 38: 533–538.
Boynton, A. L., Whitfield, J. F., MacManus, J. P., Calmodulin stimulates DNA synthesis by rat liver cells, BBRC, 1980, 95(2): 745–749.
Gorbacherskaya, L. V., Borovkova, T. V., Rybin, U. O. et al., Effect of exogenous calmodulin on lymphocyte proliferation in normal subjects, Bull Exp. Med.Biol., 1983, 95: 361–363.
Wong, P. Y.-K., Lee, W. H., Chao, PH.-W., The role of calmodulin in prostaglandin metabolism, Ann. NY Acad. Sci., 1980, 356: 179–189.
Mac Neil, S., Dawson, R. A., Crocker, G. et al., Effects of extracellular calmodulin and calmodulin antagonists on B16 melanoma cell growth, J. Invest. Dermatol., 1984, 83: 15–19.
Crocker, D. G., Dawson, R. A., Mac Neil, S. et al., An extracellular role for calmodulin-like activity in cell proliferation, Biochem. J., 1988, 253: 877–884.
Polito, V. S., Calmodulin and calmodulin inhibitors: effect on pollen germination and tube growth, in Pollen: Biology and Implications for Plant Breeding (eds. Mulvshy, D. L., Ottaviaro, E.), New York: Elsevier, 1983. 53–60.
Biro, R. L., Sun, D. Y., Roux, S. J. et al., Characterization of oat calmodulin and radioimmunoassay of its subcellular distribution, Plant Physiol., 1984, 75: 382–386.
Terry, M. E., Bonner, B. A., An examination of centrifugation as a method of extracting an extracellular solution from peas, and its use for the study of IAA-induced growth, Plant Physiol., 1980, 66: 321–325.
Josefina, H. N., Aldasars, J. J., Rodriguez, D., Localization of calmodulin on embryonicCice aricium L, in Molecular and Cellular Aspects of Calcium in Plant Development (ed. Trewavas, A. J.), New York, London: Plenum Press, 1985, 313.
Dauwalder, M., Roux, S. J., Hardison, L., Distribution of calmodulin in pea seedling: immunocytochemical localization in plumules and root apices, Planta, 1986, 168: 461–470.
Ye, Z. H., Sun, D. Y., Guo, J. F., Preliminary study on wheat cell wall calmodulin, Chin. Sci. Bull. (in Chinese), 1988, 33(8): 624–626.
Li, J. X., Liu, J. W., Sun, D. Y., Immunoelectron microscopic localization of calmodulin in maize root cell, Cell Res., 1993, 3: 11–19.
Li, J. X., Sun, D. Y., Comparative studies on immunoreactivity of antibodies against plant and animal calmodulin, Acta Botanica Sinica (in Chinese), 1992, 34(4): 257–263.
Ye, Z. H., Guo, J. F., Sun, D. Y., Studies on the cell wall calmodulin and calmodulin-binding protein of wheat etiolated coleoptiles, Acta Phytophysiologica Sinica (in Chinese), 1989, 15(3): 223–229.
Remgard, P., Ekstrom, P. A. R., Ekstrom, A. et al., Calmodulin and in vitro regenerating frog sciatic herves: release and extracellular effects, European J. Neuroscience, 1995, 7: 1386–1392.
Cheung, M. Z., Duo, H. Y., Cheung, G. I., Localization of calmodulin in rabbit pancreas, Chinese J. of Experimental and Clinical Immunology (in Chinese), 1992, 4(6): 13–15.
Dawson, R. A., Mac Neil, S., Mitogenis role for extracellular calmodulin-like activity in normal human umbilical vein endothelial cells, Br. J. Haematol., 1992, 82: 151–160.
Goberdhan, N. J., Dawson, R. A., Freedlander, E. et al., Calmodulin-like protein as an extracellular mitogen for the keranocyte, Br. J. Dermatol., 1993, 129: 678–688.
Woodward, B. J., Lenton, E. A., Mac Neil, S., Requirement of preimplantation human embryos for extracellular calmodulin for development, Human Repro, 1993, 8(2): 272–276.
Houston, D. S., Carson, C., Esmon, C. T., Endothelial cell and extracellular calmodulin inhibited monocyte tumor necrosis factor release and augment neutrophil elastase, The J. of Biol. Chem., 1997, 272(18): 11778–11785.
Li, H. B., Cheng, G., Sun, D. Y., The effects of extracellular calmodulin on the cell proliferation of suspension cultured cell, Chin. Sci. Bull. (in Chinese), 1992, 37(19): 1804–1808.
Sun, D. Y., Li, H. B., Cheng, G., Extracellular calmodulin accelerates the proliferation of suspension cultured cells ofAnglica dahurica, Plant Science, 1994, 99: 1–8.
Bian, Y.Q., Sun, D. Y., The effects of exogenous calmodulin on cell wall regeneration and cell division of protoplasts, Acta Phytophysiologica Sinica (in Chinese), 1994, 20(3): 293–297.
Sun, D. Y., Bian, Y.Q., Zhao, B. H. et al., The effects of extracellular calmodulin on cell wall regeneration and cell division of protoplasts, Plant & Cell Physiology, 1995, 36(1): 133–138.
Ma, L. G., Sun, D. Y., The studies of extracellular action side of calmodulin on initiation and promoting pollen germination and tube growth ofHippeastrum rutilum, Prog. in Nat. Sci. (in Chinese), 1996, 6(4): 505–506.
Ma, L. G., Sun, D. Y., The effects of extracellular calmodulin on initiation ofHippeastrum rutilum pollen germination and tube growth, Planta, 1997, 202: 336–340.
Zhao, H. J., Zhu, Y.X., The effect of extracellular calmodulin on plant cell division and proliferation, Chi. Bioche. J., 1996, 12(6): 413–417.
Sun, Yu, Chen, J., Sun, D. Y., Extracellular calmodulin stimulates the transplasma membrane redox reaction of root protoplasma in Zea mays, Acta Botanica Sinica (in Chinese), 1998, 40(5): 437–441.
Ma, L. G., Fan, Q. S., Yu, Z. Q. et al., Does aluminum inhibit pollen germination via extracellular calmodulin? Plant Cell Physiol., 2000, 41(3): 372–376.
Sun, D. Y., Tang, J., Li, H. B., The presence and biological significance of extracellular calmodulin in cell, Chin. Sci. Bull. (in Chinese), 1995, 40(14): 1153–1159.
Gong, M., Yang, Z., Cao, Z., Involvement of calmodulin in pollen germination and pollen tube growth, Acta Phytophysiologica Sinica, 1994, 20: 240–247.
Zhu, Y.X., Gu, X. S., Zhao, H. J. et al., Extracellular calmodulin stimulates RbcS-GUS expression of etiolated transgenic tobacco plants in full darkness, Plant Growth Regulation, 1998, 25: 23–28.
Cui, S. J., Wang, H. H., Ma, L. G. et al., The effects of extracellular calmodulin of style and pollen on pollen germination and pollen tube growth, Acta Phytophysiologica Sinica (in Chinese), 1998, 42: 320–326.
Ma, L. G., Xu, X. D., Cui, S. J. et al., Effects of extracellular calmodulin on pollen germination and tube growth, Chin. Sci. Bull. (in Chinese), 1998, 43(2): 143–146.
Wanner, L. A., Gruissem, W., Expression dynamics of the tomato rbcS gene family during development, Plant Cell, 1991, 3: 1289–1303.
Sawbridge, T. I., Knight, M. R., Jenkins, G. I., Ontogenetic regulation and photoregulation of members of thePhaseolus vulgaris L. rbcS gene family, Planta, 1996, 198: 31–38.
Zhang, S. Q., Ma, L. G., Sun, D. Y., The effect of extracellular calmodulin on rbcS-3A expression in suspension-cultured tomato cells, Acta Botanica Sinica (in Chinese), 2000, 42(6): 653–655.
Shang, Z. L., Ma, L. G., Wang, X. C. et al., Effect of extracellular calmodulin on the cytosolic Ca2+ concentration in lily pollen grains, Acta Botanica Sinica (in Chinese), 2001, 43(1): 12–17.
Ma, L. G., Xu, X. D., Cui, S. J. et al., The presence of a heterotrimeric G protein and its role in signal transduction of extracellular calmodulin in pollen germination and tube growth, Plant Cell, 1999, 11: 1351–1363.
Guo, Y., Ma, L. G., Zhang, L. et al., The involvement of hetrotrimeric G protein in signal transduction of extracellular calmodulin in regulating rbcS expression, Chin. Sci. Bull., 2000, 45(20): 2195–2200.
Ma, L. G., Xu, X. D., Cui, S. J. et al., The involvement of phosphoinositide signaling pathway in the initiatory effects of extracellular calmodulin on pollen germination and tube growth, Acta Phytophysiologica Sinica (in Chinese), 1998, 24: 196–200.
Wang, X., Cui, S. J., Ma, L. G. et al., The involvement of PLC-IP3 pathway in pollen tube growth by microinjection study, Acta Botanica Sinica (in Chinese), 2000, 42(1): 697–702.
Franklin-Tong, V. E., Signaling and the modulation of pollen tube growth, Plant Cell, 1999, 11: 727–738.
Sun, D. Y., The universality and biological significance of signal molecules with intracellular-extracellular compatible functions, Chin. Sci. Bull. (in Chinese), 1999, 44(19): 1729–1734.
Sun, D. Y., Apoplast —The important signal source for fate decision of cell development, Acta Botanica Sinica (in Chinese), 2000, 42(5): 441–445.
Marx, J., Plants, like animals, may make use of peptide signals, Science, 1996, 237(6): 1338–1339.
Zhang, L. Q., Li, F., Sun, D. Y., The effects of extracellular calmodulin on protein phospherylation in cytoplasmic fraction from suspension-cultured tobacco cells, Acta Phytophysiologica Sinica (in Chinese), 2001, 27(3): 201–206.
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Sun, D., Tang, W. & Ma, L. Extracellular calmodulin: A polypeptide signal in plants?. Sci. China Ser. C.-Life Sci. 44, 449–460 (2001). https://doi.org/10.1007/BF02882387
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DOI: https://doi.org/10.1007/BF02882387