Abstract
The suspensor functions early in embryogenesis to provide physical support, nutrition, and growth regulators to the developing embryo proper. In most plants, the suspensor is derived from the basal cell produced following asymmetric division of the zygote. Cellular differences between the suspensor and embryo proper may result from morphogenetic gradients established prior to division of the zygote. The suspensor develops rapidly with respect to the embryo proper and becomes the first differentiated embryonic structure produced during seed development. The suspensor later undergoes programmed cell death and is not present in mature seeds. Several abnormal suspensor mutants of Arabidopsis have been identified in which the suspensor fails to undergo programmed cell death and instead proliferates to form a structure with features characteristic of the embryo proper. Analysis of these mutants suggests that communication with the embryo proper is required early in embryogenesis for maintenance of suspensor cell identity and later in suspensor development for initiation of programmed cell death. The pattern of embryogenic transformation observed in these mutants indicates that suspensor cells have the potential to recapitulate the entire spectrum of developmental programs normally restricted to the embryo proper. During normal development, interactions with the embryo proper appear to inhibit embryogenic programs, allowing suspensor cell identity to be maintained. Based on these observations, we propose that negative regulation of developmental potential plays a major role in suspensor cell differentiation and that the suspensor may serve as a valuable system for addressing mechanisms of cell differentiation and cellular communication during plant development.
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References
Aeschbacher, R.A., Schiefelbein, J.W., and Benfey, P.N. (1994) The genetic and molecular basis of root development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 25–45.
Akhundova, G.G., Grinikh, L.I., and Shevchenko, V.V. (1978) Development of Arabidopsis thaliana embryos after gamma irradiation of plants in the generative phase. Ontogenez. 9: 514–519.
Alpi, A., Tognoni, F., and D’Amato, F. (1975) Growth regulator levels in embryo and suspensor of Phaseolus coccineus at two stages of development. Planta 127: 153–162.
Barton, M.K., and Poethig, R.S. (1993) Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant. Development 119: 823–831.
Benfey, P.N., Linstead, P.J., Roberts, K., Schiefelbein, J.W., Hauser, M.-T., and Aeschbacher, R.A. (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119: 57–70.
Bennici, A., and Cionini, P.G. (1979) Cytokinins and in vitro development of Phaseolus coccineus embryos. Planta 147: 27–29.
Berleth, T., and Jürgens, G. (1993) The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118: 575–587.
Bhalla, P.L., Singh, M.B., and Malik, C.R (1981) Studies on the comparative biosynthetic activities of embryo and suspensor in Tropaeolum majus L. Z. Pflanzenphysiol. 103: 115–119.
Brady, T., and Combs, S.H. (1988) The suspensor is a major route of nutrients into proembryo, globular and heart stage Phaseolus vulgaris embryos. In: Cresti, M., Gorie, P., and Pacini, E. (eds), Sexual Reproduction in Higher Plants, pp. 531–536. Springer-Verlag, Berlin.
Brown, J.D., and Beggs, J.D. (1992) Roles of PRP8 protein in the assembly of splicing complexes. EMBO J. 11: 3721–3729.
Ceccarelli, N., Lorenzi, R., and Alpi, A. (1981) Gibberellin biosynthesis in Phaseolus coccineus suspensor. Z. Pflanzenphysiol. 102: 37–44.
Cionini, P.G., Bennici, A., Alpi, A., and D’Amato, F. (1976) Suspensor, gibberellin and in vitro development of Phaseolus coccineus embryos. Planta 131.115–117.
Clark, J.K., and Sheridan, W.F. (1991) Isolation and characterization of 51 embryo-specific mutations of maize. Plant Cell 3: 935–951.
Clutter, M., Brady, T., Walbot, V., and Sussex, I. (1974) Macromolecular synthesis during plant embryogeny: Cellular rates of RNA synthesis in diploid and polytene cells in bean embryos. J. Cell Biol. 63: 1097–1102.
Cooke, T.J., and Cohen, J.D. (1993) The role of auxin in plant embryogenesis. Plant Cell 5: 1494–1495.
Cory, S. (1994) Fascinating death factor. Nature 367: 317–318.
DeLong, A., Calderon-Urrea, A., and Dellaporta, S.L. (1993) Sex determination gene TAS-SELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74: 757–768.
Devreux, M. (1963) Effets de l’irradiation gamma chronique sur l’embryogenese de Capsella bursa-pastoris Moench. In: VI Cong. Nucl. (Roma), Energ. Nucl. Argic, CNEN Vallecchi, pp. 198–217.
Devreux, M., and Scarascia Mugnozza, G.T. (1962) Action des rayons gamma sur les premiers stades de developpement de l’embryon de Nicotiana rustica L. Caryologia 15: 279–291.
Ellis, R.E., Yuan, J., and Horvitz, H.R. (1991) Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7: 663–698.
Goldberg, R.B., de Paiva, G., and Yadegari, R. (1994) Plant embryogenesis: Zygote to seed. Science 266: 605–614.
Greenberg, J.T., and Ausubel, F.M. (1993) Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J. 4: 327–341.
Greenberg, J.T., Guo, A., Klessig, D.F., and Ausubel, F.M. (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77: 551–563.
Haccius, B. (1963) Restitution in acidity-damaged plant embryos — regeneration or regulation? Phytomorphology 13: 107–115.
Haccius, B., and Reichert, H. (1964) Restitutionserscheinungen an pflanzlichen meristemen nach Röntgenbestrahlung. II. Adventiv-embryonie nach samenbestrahlung von Eranthis hiemalis. Planta 62: 355–372.
Jürgens, G. (1994) Pattern formation in the embryo. In: Meyerowitz, E.M., and Somerville, C.R. (eds) Arabidopsis, pp. 297–312. Cold Spring Harbor Laboratory Press, Plainview, New York.
Jürgens, G., Mayer, U., Torres Ruiz, R.A., Berleth, T., and Miséra, S. (1991) Genetic analysis of pattern formation in the Arabidopsis embryo. Development Suppl. 1: 27–38.
Koncz, C., Chua, N.-H., and Schell, J. (1992) Methods in Arabidopsis Research. World Scientific Publishing Co., Singapore.
Lersten, N.R. (1983) Suspensors in Leguminosae. Bot. Rev. 49: 233–257.
Lorenzi, R., Bennici, A., Cionini, P.G., Alpi, A., and D’Amato, F. (1978) Embryo-suspensor relations in Phaseolus coccineus: cytokinins during seed development. Planta 143: 59–62.
Maheshwari, P. (1950) An Introduction to the Embryology of Angiosperms. McGraw-Hill, New York.
Mansfield, S.G., and Briarty, L.G. (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can. J. Bot. 69: 461–476.
Mansfield, S.G., Briarty, L.G., and Erni, S. (1991) Early embryogenesis in Arabidopsis thaliana. I. The mature embryo sac. Can. J. Bot. 69: 447–460.
Mayer, U., Berleth, T., Torres Ruiz, R.A., Miséra, S., and Jürgens, G. (1993a) Pattern formation during Arabidopsis embryo development. In: Amasino, R.M. (ed) Cellular Communication in Plants, pp. 93–98. Plenum Press, New York.
Mayer, U., Büttner, G., and Jürgens, G. (1993b) Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117: 149–162.
Meinke, D.W. (1995) Molecular genetics of plant embryogenesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 369–394.
Meyerowitz, E.M., and Somerville, C.R. (1994) Arabidopsis. Cold Spring Harbor Laboratory Press, Plainview, New York.
Nagl, W. (1990) Translocation of putrescine in the ovule, suspensor and embryo of Phaseolus coccineus. J. Plant Physiol. 136: 587–591.
Natesh, S., and Rau, M.A. (1984) The embryo. In: Johri, B.M. (ed) Embryology of Angiosperms, pp. 377–443. Springer-Verlag, Berlin.
Picciarelli, P., Alpi, A., Piselli, L., and Scalet, M. (1984) Gibberellin-like activity in suspensors of Tropaeolum majus L. and Cytisus laburnum L. Planta 162: 566–568.
Pritchard, H.N. (1964) A cytochemical study of embryo development in Stellaria media. Amer. J. Bot. 51:472–479.
Przybyllok, T., and Nagl, W. (1977) Auxin concentration in the embryo and suspensors of Tropaeolum majus, as determined by mass fragmentation (single ion detection). Z. Pflanzenphysiol. 84: 463–465.
Raghavan, V. (1986) Embryogenesis in Angiosperms. Cambridge University Press, Cambridge, U.K.
Schiefelbein, J.W., and Benfey, P.N. (1994) Root development in Arabidopsis. In: Meyerowitz, E.M., and Somerville, C.R. (eds) Arabidopsis, pp. 335–353. Cold Spring Harbor Laboratory Press, Plainview, New York.
Schulz, P., and Jensen, W.A. (1969) Capsella embryogenesis: the suspensor and the basal cell. Protoplasma 67: 139–163.
Schwartz, B.W., Yeung, E.C., and Meinke, D.W. (1994) Disruption of morphogenesis and transformation of the suspensor in abnormal suspensor mutants of Arabidopsis. Development 120: 3235–3245.
Schwartz, L.M., Smith, S.W., Jones, M.E.E., and Osborne, B.A. (1993) Do all programmed cell deaths occur via apoptosis? Proc. Natl. Acad. Sci. USA 90: 980–984.
Sussex, I., Clutter, M., Walbot, V., and Brady, T. (1973) Biosynthetic activity of the suspensor of Phaseolus coccineus. Caryologia 25 (suppl.): 262–272.
Topping, J.F., Agyeman, F., Henricot, B., and Lindsey, K. (1994) Identification of molecular markers of embryogenesis in Arabidopsis thaliana by promoter trapping. Plant J. 5: 895–903.
Vaux, D.L., Haecker, G., and Strasser, A. (1994) An evolutionary perspective on apoptosis. Cell 76: 777–779.
Vernon, D.M., and Meinke, D.W. (1994) Embryogenic transformation of the suspensor in twin, a polyembryonic mutant of Arabidopsis. Devel. Biol. 165: 566–573.
Vernon, D.M., and Meinke, D.W. (1995) Late embryo-defective mutants of Arabidopsis. Dev. Genet. 16:311–320.
Walbot, V, Brady, T., Clutter, M., and Sussex, I. (1972) Macromolecular synthesis during plant embryogeny: rates of RNA synthesis in Phaseolus coccineus embryos and suspensors. Devel. Biol. 29: 104–111.
Wardlaw, C.W. (1955) Embryogenesis in Plants. Methuen & Co., LTD, London.
West, M.A.L., and Harada, J.J. (1993) Embryogenesis in higher plants: an overview. Plant Cell 5: 1361–1369.
Wyllie, A.H., Kerr, J.F.R., and Currie, A.R. (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251–306.
Yadegari, R., de Paiva, G.R., Laux, T., Koltunow, A.M., Apuya, N., Zimmerman, J.L., Fischer, R.L., Harada, J.J., and Goldberg, R.B. (1994) Cell differentiation and morphogenesis are uncoupled in Arabidopsis raspberry embryos. Plant Cell 6: 1713–1729.
Yeung, E.C. (1980) Embryogeny of Phaseolus: The role of the suspensor. Z. Pflanzenphysiol. 96: 17–28.
Yeung, E.C., and Meinke, D.W. (1993) Embryogenesis in angiosperms: development of the suspensor. Plant Cell 5: 1371–1381.
Yeung, E.C., and Sussex, I.M. (1979) Embryogeny of Phaseolus coccineus: The suspensor and the growth of the embryo-proper in vitro. Z. Pflanzenphysiol. 91: 423–433.
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Schwartz, B.W., Vernon, D.M., Meinke, D.W. (1997). Development of the Suspensor: Differentiation, Communication, and Programmed Cell Death During Plant Embryogenesis. In: Larkins, B.A., Vasil, I.K. (eds) Cellular and Molecular Biology of Plant Seed Development. Advances in Cellular and Molecular Biology of Plants, vol 4. Springer, Dordrecht. https://doi.org/10.1007/978-94-015-8909-3_2
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DOI: https://doi.org/10.1007/978-94-015-8909-3_2
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