Plant Molecular Biology

, Volume 44, Issue 3, pp 267–281 | Cite as

Programmed cell death in plant reproduction

  • Hen-ming Wu
  • Alice Y. Cheung
Article

Abstract

Reproductive development is a rich arena to showcase programmed cell death in plants. After floral induction, the first act of reproductive development in some plants is the selective killing of cells destined to differentiate into an unwanted sexual organ. Production of functional pollen grains relies significantly on deterioration and death of the anther tapetum, a tissue whose main function appears to nurture and decorate the pollen grains with critical surface molecules. Degeneration and death in a number of anther tissues result ultimately in anther rupture and dispersal of pollen grains. Female sporogenesis frequently begins with the death of all but one of the meiotic derivatives, with surrounding nucellar cells degenerating in concert with embryo sac expansion. Female tissues that interact with pollen undergo dramatic degeneration, including death, to ensure the encounter of compatible male and female gametes. Pollen and pistil interact to kill invading pollen from an incompatible source. Most observations on cell death in reproductive tissues have been on the histological and cytological levels. We discuss various cell death phenomena in reproductive development with a view towards understanding the biochemical and molecular mechanisms that underlie these processes.

fertilization male sterility pollination sex determination tapetum 

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References

  1. Aarts, M.G.M., Hodge, R., Kalantidis, K., Florack, D., Wilson, Z.A., Mulligan, B.J., Stiekema, W.J., Scott, R. and Pereira, A. 1997. The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J. 12: 615–623.Google Scholar
  2. Ainsworth, C., Crossley, S., Buchanan-Wollaston, V., Thangavalu, M. and Parker, J. 1995. Male and female flowers of the dioecious plant sorrel show different patterns of MADs box gene expression. Plant Cell 7: 1593–1598.Google Scholar
  3. Alnemri, E.S., Livingston, D.J., Nicholson, D.W., Salvesen, G., Thornberry, N.A., Wong, W.W. and Yuan, J. 1996. Human ICE/CED-3 protease nomenclature. Cell 87: 171.Google Scholar
  4. Ameisen, J.D. 1996. The origin of programmed cell death. Science 272: 1278–1279.Google Scholar
  5. Allen, R.T., Cluck, M.W. and Agrawal, D.K. 1998. Mechanisms controlling cellular suicide: role of Bcl1 and caspases. Cell. Mol. Life Sci. 54: 427–445.Google Scholar
  6. Bahrami, A.R. and Gray, J.E. 1999. Expression of a proteasome α-type subunit gene during tobacco development and senescence. Plant. Mol. Biol. 39: 325–333.Google Scholar
  7. Barlow, P.W. 1982. Cell death: an integral part of plant development. In: M.B. Jackson, B. Grout and I.A. Mackenzie (Eds.), Growth Regulators in Plant Senescence, Wantage, Oxon British Plant Growth Regulator Group, pp. 27–45.Google Scholar
  8. Beals, T.P. and Goldberg, R.B. 1997. A novel cell ablation strategy blocks tobacco anther dehiscence. Plant Cell 9: 1527–1545.Google Scholar
  9. Bedinger, P. 1992. The remarkable biology of pollen. Plant Cell 4: 879–887.Google Scholar
  10. Bell, P.R. 1996. Megaspore abortion: a consequence of selective apoptosis? Int. J. Plant Sci. 157: 1–7.Google Scholar
  11. Bell, J. and Hicks, G. 1976. Transmitting tissue in the pistil of tobacco: light and electron microscopic observations. Planta 131: 187–200.Google Scholar
  12. Bensen, R.J., Johal, G.S., Crane, V.D., Tossberg, J.T., Schnable, P.S., Meeley, R.B. and Briggs, S.P. 1995. Cloning and characterization of the maize An1 gene. Plant Cell 7: 75–84.Google Scholar
  13. Bonner, L.J. and Dickinson, H.G. 1989. Anther dehiscence in Lycopersicon esculentum. I. Structural aspects. New Phytol. 113: 97–115.Google Scholar
  14. Buckner, B., Janick-Buckner, D., Gray, J. and Johal, G.S. 1998. Cell-death mechanisms in maize. Trend Plant Sci. 3: 218–223.Google Scholar
  15. Calderon-Urrea, A. and Dellaporta, S.L. 1999. Cell death and cell protection genes determine the fate of pistils in maize. Development 126: 435–441.Google Scholar
  16. Callis, J. and Bedinger, P. 1994. Developmentally regulated loss of ubiquitin and ubiquitinated proteins during pollen maturation in maize. Proc. Natl. Acad. Sci. USA. 91: 6074–6077.Google Scholar
  17. Callis, J., Raasch, J.A. and Vierstra, R.D. 1990. Ubiquitin extension proteins of Arabidopsis thaliana. J. Biol. Chem. 265: 12486–12493.Google Scholar
  18. Cercos, M. and Carbonnell, J. 1993. Purification and characterization of a thiol-protease induced during the senescence of unpollinated ovaries of Pisum sativum. Physiol. Plant. 88: 267–274.Google Scholar
  19. Cercos, M., Santamaria, S. and Carbonnell, J. 1999. Cloning and characterization of TPE4A, a thiol-protease gene induced during ovary senescence and seed germination in pea. Plant Physiol. 119: 1341–1348.Google Scholar
  20. Chapman, G.P. 1987. The tapetum. Int. Rev. Cytol. 107: 111–125.Google Scholar
  21. Chaubal, R. and Reger, B.J. 1992a. Calcium in the synergid cells and other regions of pearl millet ovaries. Sex. Plant Reprod. 5: 34–46.Google Scholar
  22. Chaubal, R. and Reger, B.J. 1992b. The dynamics of calcium distribution in the synergid cells of wheat after pollination. Sex. Plant Reprod. 5: 206–213.Google Scholar
  23. Cheng, P.C., Greyson, R.I. and Walden, D.B. 1983. Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Am. J. Bot. 70: 450–462.Google Scholar
  24. Cheung, A.Y. 1996a. Pollen-pistil interactions during pollen tube growth. Trends Plant Sci. 1: 45–51.Google Scholar
  25. Cheung, A.Y. 1996b. The pollen tube growth pathway: its molecular and biochemical contributions and responses to pollination. Sex. Plant Reprod. 9: 330–336.Google Scholar
  26. Cheung, A.Y. and Wu, H-M. 1998. Arabinogalactan proteins in plant sexual reproduction. Protoplasma 208: 87–98.Google Scholar
  27. Cheung, A.Y., Wang, H. and Wu, H-M. 1995. A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82: 383–393.Google Scholar
  28. Cheung, A.Y., Zhan, X.-y., Wong, E., Wang, H. and Wu, H.M. 2000. Transcriptional, post-transcriptional and posttranslational regulation of a transmitting tissue-specific pollen tube growthpromoting arabinogalactan protein. In: E.A. Nothnagel, A. Bacic and A.E. Clarke (Eds.), Cell and Developmental Biology of Arabinogalactan-proteins, Kluwer Academic Publishers, Boston, pp. 133–148.Google Scholar
  29. Cheung, A.Y, Wu, H.-M., Di Stilio, V., Glaven, R., Chen, C., Wong, E., Ogdahl, J. and Estavillo, A. 2000. Pollen-pistil interactions in Nicotiana tabacum. Ann. Bot. 85, 29–37.Google Scholar
  30. Christensen, C.A., Subramanian, S. and Drews, G.N. 1998. Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev. Biol. 202: 136–151.Google Scholar
  31. Clouse, S.D. 1996. Molecular genetic studies confirm the role of brassinosterioids in plant growth and development. Plant J. 10: 1–8.Google Scholar
  32. Cresti, M., Keijzer, C.J., Tiezzi, A., Ciampolini, F. and Focardi, S. 1986. Stigma of Nicotiana: ultrastructural and biochemical studies. Am. J. Bot. 73: 1713–1722.Google Scholar
  33. Cryns, V. and Yuan, J. 1998. Proteases to die for. Genes Dev. 12: 1551–1570.Google Scholar
  34. Domingo, D., Roberts, K., Stacey, N.J., Connerton, I., Ruiz-Teran, F. and McCann, M.C. 1998. A pectate lyase from Zinnia elegans is auxin inducible. Plant J. 13: 17–28.Google Scholar
  35. Dawson, J., Wilson, Z.A., Aarts, M.G.M., Braithwaite, A.F., Briarty, L.G. and Milligan, B.J. 1993. Microspore and pollen development in six male-sterile mutants of Arabidopsis thaliana. Can. J. Bot. 71: 629–638.Google Scholar
  36. de Graaf, B.H.J., Knuiman, B. and Mariani, C. 1998. The PELPs in the transmitting tissue of Nicotiana tabacum are translocated through the pollen walls in vivo. XVth International Congress on Sexual Plant Reproduction, p. 29.Google Scholar
  37. de Jong, A.J., Cordewener, J., Lo Schiavo, F., Terzi, M., Vandekerckhove, J., van Kammen, A. and de Vries, S.C. 1992. A carrot somatic embryo mutation is rescued by chitinase. Plant Cell 4: 425–433.Google Scholar
  38. de Jong, A.J., Heidstra, R., Spaink, H.P., Hartog, V., Meijer, E.A., Hendriks, T., Lo Schiavo, F., Terzi, M., Bisseling, T., van Kammen, A. and de Vries, S.C. 1993. Rhizobium liposaccharides rescue a carrot somatic embryo mutant. Plant Cell 5: 615–620.Google Scholar
  39. Del Pozo, O. and Lam, E. 1998. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol. 8: 1129–1132.Google Scholar
  40. DeLong, A., Calderon-Urrea, A. and Dellaporta, S.L. 1993. Sex determination gene TASSELSEED2 of maize encodes a shortchain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74: 757–768.Google Scholar
  41. Dewey, R.E., Levings, C.S. III and Timothy, D.H. 1986. Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell 44: 439–449.Google Scholar
  42. Dewey, R.E., Timothy, D.H. and Levings, C.S. III. 1987. A mitochondrial protein associated with cytoplasmic male sterility in the T-cytoplasm of maize. Proc. Natl. Acad. Sci. USA 84: 5374-5378.Google Scholar
  43. Dewey, R.E., Siedow, J.N., Timothy, D.H. and Levings, C.S. III. 1988. A 13 kilodalton maize mitochondrial protein in E. coli confers sensitivity to Bipolaris maydis toxin. Science 239: 293–295.Google Scholar
  44. Domingo, C., Roberts, K., Stacey, N., Connerton, I., Tuiz-Teran, F. and McCann, M.C. 1998. A pectate lyase from Zinnia elegans is auxin inducible. Plant J. 13: 17–28.Google Scholar
  45. Earnshaw, W.C. 1999. A cellular poison cupboard. Nature 397: 387–389.Google Scholar
  46. Eberband, S., Doubrava, N., Marfa, V., Mohnen, D., Southwick, A., Darvill, A. and Albersheim, P. 1989. Pectic cell wall fragments regulate tobacco thin-cell-layer explant morphogenesis. Plant Cell 1: 747–755.Google Scholar
  47. Faro, C., Ramalho-Santos, M., Viera, M., Mendes, A., Simoes, I., Andrade, R., Verissimo, P., Lin, X., Tang, J. and Pires, E. 1999. Cloning and characterization of a cDNA encoding cardosin A, an RGD-containing plant aspartic proteinase. J. Biol. Chem. 274: 28724–28729.Google Scholar
  48. Fisher, D.B. and Jensen, W.A. 1969. Cotton embryogenesis: the identification of the X-bodies in the degenerated synergid. Planta 84: 122–133.Google Scholar
  49. Franklin-Tong, V. 1999. Signaling and the modulation of pollen tube growth. Plant Cell 11: 727–738.Google Scholar
  50. Gagliardi, D. and Leaver, C.J. 1999. Polyadenylation accelerates the degradation of the mitochondrial mRNA associated with cytoplasmic male sterility in sunflower. EMBO J. 18: 3757–3766.Google Scholar
  51. Geitmann, A. 1999. Cell death of self-incompatible pollen tubes: necrosis or apoptosis? In: M. Cresti, G. Cai and A. Moscatelli (Eds.), Fertilization in Higher Plants: Molecular and Cytological Aspects, Springer-Verlag, Berlin/Heidelberg, pp. 113–137.Google Scholar
  52. Goldberg, R.B., Beals, T.P. and Sanders, P.M. 1993. Anther development: basic principles and practical applications. Plant Cell 5: 1217–1229.Google Scholar
  53. Goldman, M.H.S., Goldberg, R.B. and Mariani, C. 1994. Female sterile tobacco plants are produced by stigma-specific cell ablation. EMBO J. 13: 2976–2984.Google Scholar
  54. Granell, A., Cercos, M. and Carbonell, J. 1998. Plant cysteine proteases in germination and senescence. In: A.J. Barret, N.D. Rawlings and J.F. Woessner (Eds.), Handbook of Proteolytic Enzymes, Academic Press, London, pp. 578–583.Google Scholar
  55. Gray, J., Close, P.S., Briggs, S.P. and Johal, G.S. 1997. A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89: 25–31.Google Scholar
  56. Green, P.J. 1994. The ribonuclease of higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 421–445.Google Scholar
  57. Green, D.R. and Reed, J.C. 1998. Mitochondria and apoptosis. Science 281: 1309–1312.Google Scholar
  58. Greenberg, J.T. 1996. Programmed cell death: a way of life for plants. Proc. Natl. Acad. Sci. USA. 93: 12094–12097.Google Scholar
  59. Hagashiyama, T., Kuroiwa, H., Kawano, S. and Kuroiwa, R. 1998. Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri. Plant Cell 10: 2019–2031.Google Scholar
  60. Hardenack, S., Ye, D., Saedler, H. and Grant, S. 1994. Comparison of MADS box gene expression in developing male and female flowers of the dioecious plant White campion. Plant Cell 6: 1775–1787.Google Scholar
  61. Harikrishna, K., Jampates-Beale, R., Milligan, S.B. and Gasser, C.S. 1996. An endochitinase gene expressed at high levels in the stylar transmitting tissue of tomatoes. Plant Mol. Biol. 30: 899–911.Google Scholar
  62. Herrero, M. 1992. From pollination to fertilization in fruit trees. Plant Growth Regul. 11: 27–32.Google Scholar
  63. Herrero, M. and Dickinson, H.G. 1979. Pollen-pistil incompatibility in Petunia hybrida: changes in the pistil following compatible and incompatible intraspecific crosses. J. Cell Sci. 36: 1–18.Google Scholar
  64. Herrero, M. and Dickinson, H.G. 1981. Pollen tube development in Petunia hybrida following compatible and incompatible intraspecific matings. J. Cell Sci. 47: 365–383.Google Scholar
  65. Holden, M.J. and Sze, H. 1987. Dissipation of the membrane potential in susceptible corn mitochondria by the toxin of Helminthosporium maydis, race T, and toxin analogs. Plant Physiol. 84: 670–676.Google Scholar
  66. Hölskamp, M., Kopczak, S.D. Horejsi, T.F., Kihl, B.K. and Pruitt, R.E. 1995a. Identification of genes required for pollen-stigma recognition in Arabidopsis thaliana. Plant J. 8: 703–714.Google Scholar
  67. Hölskamp, M, Schneitz, K. and Pruitt, R.E. 1995b. Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 7: 57–64.Google Scholar
  68. Horner, H.T. and Wagner, B.L. 1992. Association of four different calcium crystals in the anther connective tissue and hypodermal stomium of Capsicum annuum (Solanaceae) during microsporogenesis. Am. J. Bot. 79: 531–541.Google Scholar
  69. Huang, B.-Q. and Russell, S.D. 1992a. Female germ unit: organization, isolation and function. Int. Rev. Cytol. 140: 233–293.Google Scholar
  70. Huang, B.-Q. and Russell, S.D. 1992b. Synergid degeneration in Nicotiana: a quantitiative, fluorochromatic and chlorotetracycline study. Sex. Plant Reprod. 5: 151–155.Google Scholar
  71. Huang, B.-Q. and Russell, S.D. 1994. Fertilization in Nicotiana tabacum: cytoskeletal modifications in the embryo sac during synergid degeneration. Planta 194: 200–214.Google Scholar
  72. Huang, B.-Q., Strout, G.W. and Russell, S.D. 1993. Fertilization in Nicotiana tabacum: ultrastructural organization of propane-jetfrozen embryo sacs in vivo. Planta 191: 256–264.Google Scholar
  73. Irish, E. and Nelson, T. 1989. Sex determination in monoecious and dioecious plants. Plant Cell 1: 737–744.Google Scholar
  74. Izhar, S. and Frankel, R. 1971. Mechanism of male sterility in Petunia: the relationship between pH, callase activity in the anthers, and the breakdown of the microsporogenesis. Theor. Appl. Genet. 41: 104–108.Google Scholar
  75. Jensen, W.A. and Fisher, D.B. 1968. Cotton embryogenesis: the entrance and discharge of the pollen tube in the embryo sac. Planta 78: 158–183.Google Scholar
  76. Juarez, C. and Banks, J.A. 1998. Sex determination in plants. Curr. Opin. Plant Biol. 1: 68–72.Google Scholar
  77. Kandasamy, M.M. and Kristen, U. 1987. Developmental aspects of ultrastructure, histochemistry and receptivity of the stigma of Nicotiana sylvestris. Am. J. Bot. 60: 427–437.Google Scholar
  78. Koltunow, A.M., Truettner, J., Cox, K.H., Wallroth, M. and Goldberg, R.B. 1990. Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2: 1201–1224.Google Scholar
  79. Kroh, M., Miki-Hirosige, H., Rosen, W. and Loewus, F. 1970. Incorporation of label into pollen tube walls from myo-inositol labeled Lilium longiflorum pistils. Plant Physiol. Lancaster 45: 92–94.Google Scholar
  80. Labraca, C. and Loewus, F. 1973. The nutritional role of pistil exudate in pollen tube wall formation in Lilium longiflorum. II. Production and utilization of exudate from the stigma and stylar canal. Plant Physiol. 52: 87–92.Google Scholar
  81. Lantin, S., O'Brien, M. and Matton, D.P. 1999. Pollination and wounding of the style induce the expression of a developmentally regulated pistil dioxygenase at a distance in the ovary. Plant Mol. Biol. 41: 371–386.Google Scholar
  82. Lebel-Hardenack, S., and Grant, S.R. 1997. Genetics of sex determination in flowering plants. Trends Plant Sci. 2: 130–136.Google Scholar
  83. Lebel-Hardenack, S., Ye, D., Koutnikova, H., Saedler, H. and Grant, S.R. 1997. Conserved expression of a TASSELSEED2 homolog in the tapetum of the dioecious Silene latifolia and Arabidopsis thaliana. Plant J. 12: 515–526.Google Scholar
  84. Leung, D.W.M. 1992. Involvement of plant chitinase in sexual reproduction of higher plants. Phytochemistry 31: 1899–1900.Google Scholar
  85. Levine, A., Pennell, R.I., Alvarez, M.E., Palmer, R. and Lamb, C. 1996. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6: 427–437.Google Scholar
  86. Levings, C.S. III. 1993. Thoughts on cytoplasmic male sterility in cms-T maize. Plant Cell 5: 1285–1290.Google Scholar
  87. Li, D., Blakey, C.A., Dewald, C. and Dellaporta, S.L. 1997. Evidence for a common sex determination mechanism for pistil abortion in maize and in its wild relative Tripsacum. Proc. Natl. Acad. Sci. USA 94: 4217–4222.Google Scholar
  88. Li, J., Nagpal, P., Cook, R.K., Elich, T., Lopez, E., Pepper, A., Poole, D. and Chory, J. 1996. Molecular characterization of DET2 mutant in Arabidopsis. Science 272: 398–401.Google Scholar
  89. Li, Y-Q., Southworth, D., Linskens, H.F., Mulcahy, D.L. and Cresti, M. 1995. Localization of ubiquitin in anthers and pistils of Nicotiana. Sex. Plant Reprod. 8: 123–128.Google Scholar
  90. Lind, J.L., Bonig, I., Clarke, A.E. and Anderson, M.A. 1996. A style-specific 120 kD glycoprotein enters pollen tubes of Nicotiana alata in vivo. Sex. Plant Reprod. 9: 75–86.Google Scholar
  91. Liu, X., Zou, H., Slaughter, C. and Wang, X. 1997. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89: 175–184.Google Scholar
  92. Loukides, C.A., Broadwater, A.H. and Bedinger, P.A. 1995. Two new male-sterile mutants of Zea mays (Poaceae) with abnormal tapetal cell morphology. Am. J. Bot. 82: 1017–1023.Google Scholar
  93. Ma, H. 1994. The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Dev. 8: 745–756.Google Scholar
  94. Mandava, N.B. 1988. Plant growth promoting brassinosteroids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39: 23–52.Google Scholar
  95. Mariani, C., de Beuckeleer, M., Truettner, J., Leemans, J. and Goldberg, R.B. 1990. Induction of male sterility in plants by a chimaeric ribonuclease gene. Nature 347: 737–741.Google Scholar
  96. Mascarenhas, J.P. 1990. Gene activity during pollen development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41: 317–338.Google Scholar
  97. Matton, D.P., Nass, N., Clarke, A.E. and Newbingen, E. 1994. Selfincompatibility: how plants avoid illegitimate offspring. Proc. Natl. Acad. Sci. USA 91: 1992–1997.Google Scholar
  98. McCabe, P.F., Valentine, T.A., Forsberg, L.S. and Pennell, R.I. 1997. Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9: 2225–2241.Google Scholar
  99. McClure, B.A., Gray, J.E., Anderson, M.A. and Clarke, A.E. 1990. Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347: 757–760.Google Scholar
  100. McCormick, S. 1993. Male gametophyte development. Plant Cell 5: 1265–1275.Google Scholar
  101. Milligan, S.R. and Gasser, C.S. 1995. Nature and regulation of pistil-expressed genes in tomato. Plant Mol. Biol. 28: 691–711.Google Scholar
  102. Minami, A. and Fukuda, H. 1995. Transient and specific expression of a cysteine endopeptidase associated with autolysis during differentiation of Zinnia mesophyll cells into tracheary elements. Plant Cell Physiol. 36: 1599–1606.Google Scholar
  103. Mittler, R. and Lam, E. 1996. Sacrifice in the face of foes: pathogeninduced programmed cell death in plants. Trends Microbiol. 4: 10–15.Google Scholar
  104. Mogensen, H.L. 1984. Quantitative observations on the pattern of synergid degeneration in barley. Am. J. Bot. 71: 1448–1451.Google Scholar
  105. Murgia, M., Huang, B-Q., Tucker, S.C. and Musgrave, M.E. 1993. Embryo sac lacking antipodal cells in Arabidopsis thaliana (Brassicaceae). Am. J. Bot. 80: 824–838.Google Scholar
  106. Murphy, D.J. and Ross, J.H.E. 1998. Biosynthesis, targeting and processing of oleosin-like proteins, which are major pollen coat components in Brassica napus. Plant J. 13: 1–16.Google Scholar
  107. Mutu, A. and Gal, S. 1999. Plant aspartic proteinases: enzymes on the way to a function. Physiol. Plant. 105: 569–576.Google Scholar
  108. Nasrallah, J.B. 1997. Signal perception and response in the interactions of self-incompatiblity in Brassica. Essays Biochem. 32: 143–160.Google Scholar
  109. Nettancourt, D., Devreux, M., Bozzini, A., Cresti, M. and Sarfatti, G. 1973. Ultrastructural aspects of the self-incompatibility mechanism in Lycopersicum peruvianum Mill. J. Cell Sci. 12: 403–419.Google Scholar
  110. Neuffer, M.G., Coe, E.H. and Wessler, S.R. 1997. The Mutants of Maize, Cold Spring Harbor Laboratory Press, Plainview, NY.Google Scholar
  111. Nothnagel, E.A. 1997. Proteoglycan and related components in plant cells. Int. Rev. Cytol. 174: 195–291.Google Scholar
  112. Orzaez, D. and Granell, A. 1997. DNA fragmentation is regulated by ethylene during carpel senescence in Pisum sativum. Plant J. 11: 137–144.Google Scholar
  113. Pai, J.-T., Brown, M.S. and Goldstein, J.L. 1996. Purification and cDNA cloning of a second apoptosis-related cysteine protease that cleaves and activates sterol regulatory element binding proteins. Proc. Natl. Acad. Sci. USA 93: 5437–5442.Google Scholar
  114. Pennell, R.I. and Lamb, C. 1997. Programmed cell death in plants. Plant Cell 9: 1157–1168.Google Scholar
  115. Piffanelli, P. and Murphy, D.J. 1998. Novel organelles and targeting mechanisms in the anther tapetum. Trends Plant Sci. 3: 250–253.Google Scholar
  116. Preuss, D., Lemieux, B., Yen, G. and Davis, R.W. 1993. A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupt cell signaling during fertilization. Genes Dev. 7: 974–985.Google Scholar
  117. Ray, S., Park, S.-S. and Ray, A. 1997. Pollen tube guidance by female gametophyte. Development 124: 2489–2494.Google Scholar
  118. Reiser, L. and Fischer, R.L. 1993. The ovule and the embryo sac. Plant Cell 5: 1291–1301.Google Scholar
  119. Rhee, S.Y. and Somerville, C.R. 1998. Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. Plant J. 15: 79–88.Google Scholar
  120. Rodriguez-Concepcion, M. and Beltrain, J.P. 1995. Repression of the pea lipoxygenase gene loxg is associated with carpel development. Plant Mol. Biol. 27: 887–899.Google Scholar
  121. Russell, S.D. 1979. Fine structure of megagametophyte development in Zea mays. Can. J. Bot. 57: 1093–1110.Google Scholar
  122. Russell, S.D. 1993. The egg cell: developmental role in fertilization and early embryogenesis. Plant Cell 5: 1349–1359.Google Scholar
  123. Russell S.D. 1996. Attraction and transpot of male gametes for fertilization. Sex. Plant Reprod. 9: 337–342.Google Scholar
  124. Sassen, M.M.A. 1974. The stylar transmitting tissue. Acta Bot. Neerl. 23: 99–108.Google Scholar
  125. Schnable, P.S. and Wise, R.P. 1998. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci. 3: 175–180.Google Scholar
  126. Schindler, T., Bergfeld, R. and Schopfer, P. 1995. Arabinogalactan proteins in maize coleoptiles: developmental relationship to cell death during xylem differentiation but not to extension growth. Plant J. 7: 25–36.Google Scholar
  127. Seigel, B.A. and Verbeke, J.A. 1989. Diffusible factors essential for epidermal cell redifferentiation in Catharanthus roseus. Science 244: 580–582.Google Scholar
  128. Serpe, M.D. and Nothnagel, E.A. 1994. Effects of Yariv phenylglycosides on Rosa cell suspensions: evidence for the involvement of arabinogalactan proteins in cell proliferation. Planta 193: 542–550.Google Scholar
  129. Solomon, M., Belenghi, B., Delledonne, M., Menachem, E. and Levine, A. 1999. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11: 431–443.Google Scholar
  130. Sumner, M.J. 1992. Embryology of Brassica campestris: the entrance and discharge of the pollen tube in the synergid and the formation of the zygote. Can. J. Bot. 70: 1577–1990.Google Scholar
  131. Susin, S.A., Lorenzo, H.K., Zamzami, N., Marzo, I., Snow, B.E., Brothers, G.M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., Larochette, N., Goodlett, D.R., Aebersold, R., Siderovski, D.P., Penninger, J.M. and Kroemer, G. 1999. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397: 441–446.Google Scholar
  132. Susin, S.A., Zamazmi, H.K. and Kroemer, G. 1998. Mitochondria as regulator of apoptosis: doubt no more. Biochim. Biophys. Acta. 1366: 151–161.Google Scholar
  133. Thornberry, N.A. and Lazebnik, Y. 1998. Caspases: enemies within. Science 281: 1312–1316.Google Scholar
  134. Tian, H.Q. and Russell, S.D. 1997. Developmental changes in calcium distribution and accumulation in fertilized and unfertilized ovules and embryo sacs of Nicotiana tabacum. Planta 202: 93–105.Google Scholar
  135. Tran Thanh Van, K., Toubart, P., Cousson, A., Darvill, A.G., Gollin, D.J., Chelf, P. and Albersheim, P. 1985. Manipulation of the morphogenetic pathway of tobacco explants by oligosaccharins. Nature 314: 615–617.Google Scholar
  136. Vaux, D.L. and Korsmeyer, S.J. 1999. Cell death in development. Cell 96: 245–254.Google Scholar
  137. van Hengel, A.J. 1998. Ph.D. thesis, Department of Molecular Biology, Wageningen Agricultural University.Google Scholar
  138. Vieira, M., Pissarra, J., Verissimo, P., Castanheira, P, Costa, Y., Pereira, S., Pires, E. and Faro, C. 1999. Cardosin B is an aspartic proteinase expressed at the extracellular matrix of the transmitting tissue of Cynara cardunculus L. Submitted.Google Scholar
  139. Vierstra, R.D. 1996. Proteolysis in plants: mechanisms and functions. Plant Mol. Biol. 32: 275–302.Google Scholar
  140. Walker, D.B. 1975a. Postgenital carpel fusion in Catharanthus roseus (Apocynaceae). I. Light and scanning electron microscopic study of gynoecial onogeny. Am. J. Bot. 62: 457–467.Google Scholar
  141. Walker, D.B. 1975b. Postgenital carpel fusion in Catharanthus roseus. II. Fine structure of the epidermis before fusion. Protoplasma 86: 29–41.Google Scholar
  142. Walker, D.B. 1975c. Postgenital carpel fusioin in Catharanthus roseus. III. Fine structure of the epidermis during and after fusion. Protoplasma 86: 43–63.Google Scholar
  143. Wang, H., Wu, H.-M. and Cheung, A.Y. 1996. Pollination induces mRNA poly(A) tail-shortening and cell deterioration in flower transmitting tissue. Plant J. 9: 715–727.Google Scholar
  144. Webb, M.C. and Gunning, B.E.S. 1990. Embryo sac development in Arabidopsis thaliana I. Megasporogenesis, including the microtubular cytoskeleton. Sex. Plant Reprod. 3: 244–256.Google Scholar
  145. Wemmer, T., Kaufmann, H., Kirch, H-H., Schneider, K., Lottspeich, F. and Thompson, R.D. 1994. The most abundant soluble basic protein of the stylar transmitting tissue in potato (Solanum tuberosum L.) is an endochitinase. Planta 194: 264–273.Google Scholar
  146. Winkler, R.G. and Helentjaris, T. 1995. The maize dwarf3 gene encodes a cytochrome p450-mediated early step in gibberellin biosynthesis. Plant Cell 7: 1307–1317.Google Scholar
  147. Wolter-Arts, M., Derksen, J., Kooijman, J.W. and Mariani, C. 1996. Stigma development in Nicotiana tabacum. Cell death in transgenic plants as a marker to follow cell fate at high resolution. Sex. Plant Reprod. 9: 243–254.Google Scholar
  148. Wolter-Arts, M., Lush, W.M. and Mariani, C. 1998. Lipids are required for directional pollen tube growth. Nature 392: 818–820.Google Scholar
  149. Worrall, D., Hird, D.L., Hodge, R., Paul, W., Draper, J. and Scott, R. 1992. Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell 4: 759–771.Google Scholar
  150. Wu, H.-M., and Cheung, A.Y. 1998. Sexual reproduction: from sexual differentiation to fertilization. Annu. Plant Rev. 1: 181–222.Google Scholar
  151. Wu, H.-M., Wang, H. and Cheung, A.Y. 1995. A pollentube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell 82: 393–403.Google Scholar
  152. Wu, S.S.H., Platt, K.A., Ratnayake, C., Wang, T-W., Ting, J.T.L. and Huang, A.H.C. 1997. Isolation and characterization of neutral-lipid-containing organelles and globuli-filled plastids from Brassica napus tapetum. Proc. Natl. Acad. Sci. USA. 94: 12711–12716.Google Scholar
  153. Wu, H.-M., Wong, E., Ogdahl, J. and Cheung, A.Y. 2000. A pollen tube growth-promoting arabinogalactan protein from Nicotiana alata is similar to the tobacco TTS protein. Plant J. 22: 165–176.Google Scholar
  154. Wyllie, A.H. 1980. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activity. Nature 284: 555–556.Google Scholar
  155. Xu, F.-X. and Chye, M.-L. 1999. Expression of cysteine proteinase during developmental events associated with programmed cell death in brinjal. Plant J. 17: 321–327.Google Scholar
  156. Xu, W., Purugganan, M.M., Polisensky, D.H., Antosiewicz, D.M., Fry, S.C. and Braam, J. 1995. Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 7: 1555–1567.Google Scholar
  157. Yamamoto, R., Demura, T. and Fukuda, H. 1997. Brassinosteroids induce entry into the final stage of tracheary element differentiation in cultured Zinnia cells. Plant Cell Physiol. 38: 980–983.Google Scholar
  158. Yan, H., Yang, H.Y. and Jensen, W.A. 1991. Ultrastructure of the developing embryo sac of sunflower (Helianthus annuus) before and after fertilization. Can. J. Bot. 69: 191–202.Google Scholar
  159. Yao, M.-C. 1996. Programmed DNA deletions in Tetrahymena: mechanisms and implications. Trends Genet. 12: 26–30.Google Scholar
  160. Youl, J.J., Bacic, A. and Oxley, D. 1998. Arabinogalactan-proteins from Nicotiana alata and Pyrus communis contain glycosylphosphatidylinositol membrane anchors. Proc. Natl. Acad. Sci. USA 95: 7921–7926.Google Scholar
  161. Zhang, X.S. and O'Neill, S.D. 1993. Ovary and gametophyte development are coordinately regulated by auxin and ethylene following pollination. Plant Cell 5: 403–418.Google Scholar
  162. Zurek, D.M. and Clouse, S.D. 1994. Molecular cloning and characterization of a brassinosteroid-regulated gene from elongating soybean (Glycine max L.) epicotyls. Plant Physiol. 104: 161–170.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Hen-ming Wu
    • 1
  • Alice Y. Cheung
    • 1
  1. 1.Department of Biochemistry and Molecular BiologyUSA

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