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Plant Molecular Biology

, Volume 44, Issue 3, pp 303–318 | Cite as

Regulation of cell death in flower petals

  • Bernard Rubinstein
Article

Abstract

The often rapid and synchronous programmed death of petal cells provides a model system to study molecular aspects of organ senescence. The death of petal cells is preceded by a loss of membrane permeability, due in part to increases in reactive oxygen species that are in turn related to up-regulation of oxidative enzymes and to a decrease in activity of certain protective enzymes. The senescence process also consists of a loss of proteins caused by activation of various proteinases, a loss of nucleic acids as nucleases are activated, and enzyme-mediated alterations of carbohydrate polymers. Many of the genes for these senescence-associated enzymes have been cloned. In some flowers, the degradative changes of petal cells are initiated by ethylene; in others, abscisic acid may play a role. External factors such as pollination, drought and temperature stress also affect senescence, perhaps by interacting with hormones normally produced by the flowers. Signal transduction may involve G-proteins, calcium activity changes and the regulation of protein phosphorylation and dephosphorylation. The efficacy of the floral system as well as the research tools now available make it likely that important information will soon be added to our knowledge of the molecular mechanisms involved in petal cell death.

flower petals hormones membrane permeability pollination programmed cell death senescence senescence-associated genes 

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References

  1. Aida, R., Yoshida, T., Ichimura, K., Goto, R. and Shibata, M. 1998. Extension of flower longevity in transgenic torenia plants incorporating ACC oxidase transgene. Plant Sci. 138: 91–101.Google Scholar
  2. Asada, K. 1992. Ascorbate peroxidase - a hydrogen peroxidescavenging enzyme in plants. Physiol. Plant. 85: 235–241.Google Scholar
  3. Ashman, T.-L. and Schoen, D.J. 1994. How long should flowers live? Nature 371: 788–791.Google Scholar
  4. Ashman, T.-L. and Schoen, D.J. 1997. The cost of floral longevity in Clarkia tembloriensis: an experimental investigation. Evol. Ecol. 11: 289–300.Google Scholar
  5. Bachmair, A., Becker, F., Masterson, R.V. and Schell J. 1990. Perturbation of the ubiquitin system causes leaf curling, vascular tissue alterations and necrotic lesions in a higher plant. EMBO J. 9: 4543–4549.Google Scholar
  6. Bartoli, C.G., Simontacchi, M., Guiamet, J., Montaldi, E. and Puntarulo, S. 1995. Antioxidant enzymes and lipid peroxidation during aging of Chrysanthemum morifolium RAM petals. Plant Sci. 104: 161–168.Google Scholar
  7. Bartoli, C.G., Simontacchi, M., Montaldi, E. and Puntarulo, S. 1996. Oxidative stress, antioxidant capacity and ethylene production during ageing of cut carnation (Dianthus caryophyllus) petals. J. Exp. Bot. 47: 595–601.Google Scholar
  8. Bartoli, C.G., Simontacchi, M., Montaldi, E. and Puntarulo, S. 1997. Oxidants and antioxidants during ageing of chrysanthemum petals. Plant Sci. 129: 157–165.Google Scholar
  9. Baumgartner, B., Kende, H. and Matile, P. 1975. Ribonuclease in senescing morning glory. Purification and demonstration of de novo synthesis. Plant Physiol. 55: 734–737.Google Scholar
  10. Beja-Tal, S. and Borochov, A. 1994. Age-related changes in biochemical and physical properties of carnation petal plasma membranes. J. Plant Physiol. 143: 195–199.Google Scholar
  11. Beja-Tal, S., Borochov, A., Gindin, E. and Mayak, S. 1995. Transient water stress in cut carnation flowers: effects of cycloheximide. Scient. Hort. 64: 167–175.Google Scholar
  12. Bieleski, R.L. 1993. Fructan hydrolysis drives petal expansion in the ephemeral daylily flower. Plant Physiol. 103: 213–219.Google Scholar
  13. Bieleski, R.L. 1995. Onset of phloem export from senescent petals of daylily. Plant Physiol. 109: 557–565.Google Scholar
  14. Bieleski, R.L. and Reid, M.S. 1992. Physiological changes accompanying senescence in the ephemeral daylily flower. Plant Physiol. 98: 1042–1049.Google Scholar
  15. Blank, A. and McKeon, T.A. 1991. Expression of three RNase activities during natural and dark-induced senescence of wheat leaves. Plant Physiol. 97: 1409–1413.Google Scholar
  16. Borochov, A. and Woodson, W.R. 1989. Physiology and biochemistry of flower petal senescence. Hort. Rev. 11: 15–43.Google Scholar
  17. Borochov, A., Cho, M.H. and Boss, W.F. 1994. Plasma membrane lipid metabolism of petunia petals during senescence. Physiol. Plant 90: 279–284.Google Scholar
  18. Borochov, A., Spiegelstein, H. and Philosoph-Hadas, S. 1997. Ethylene and flower petal senescence: interrelationship with membrane lipid catabolism. Physiol. Plant. 100: 606–612.Google Scholar
  19. Buchanan-Wollaston, V. 1997. The molecular biology of leaf senescence. J. Exp. Bot. 48: 181–199.Google Scholar
  20. Buchanan-Wollaston, V. and Ainsworth, C.A. 1997. Leaf senescence in Brassica napus: cloning of senescence related genes by subtractive hybridisation. Plant Mol. Biol. 33: 821–834.Google Scholar
  21. Bui, A.Q. and O'Neill, S.D. 1998. Three 1-aminocyclopropane-1-carboxylate-synthase genes regulated by primary and secondary pollination signals in orchid flowers. Plant Physiol. 116: 419–428.Google Scholar
  22. Cabello-Hurtado, F., Batard, Y., Salaun, J.P., Durst, F., Pinot, F. and Werck-Reichart, D. 1998. Cloning, expression in yeast and functional characterization of CYP81B1, a plant cytochrome P450 that catalyzes in-chain hydroxylation of fatty acids. J. Biol. Chem. 273: 7260–7267.Google Scholar
  23. Callis, J. 1995. Regulation of protein degradation. Plant Cell 7: 845–857.Google Scholar
  24. Celikel, F.G. and van Doorn, W.G. 1995. Solute leakage, lipid peroxidation and protein degradation during senescence of iris tepals. Physiol. Plant. 94: 515–521.Google Scholar
  25. hortorum LH Bailey). Plant Mol. Biol. 34: 855–865.Google Scholar
  26. Courtney, S.E., Rider, C.C. and Stead, A.D. 1994. Changes in protein ubiquitination and the expression of ubiquitin-encoding transcripts in daylily petals during floral development and senescence. Physiol. Plant. 91: 196–204.Google Scholar
  27. Cryns, V. and Yuan, J. 1998. Proteases to die for. Genes Dev. 12: 1551–1570.Google Scholar
  28. 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
  29. del Rio, L.A., Palma, J.M., Sandalio, L.M., Corpas, F.J., Pastori, G.M., Bueno, P. and Lopez-Huertas, E. 1996. Peroxisomes as a source of superoxide and hydrogen peroxide in stressed plants. Biochem. Soc. Trans. 24: 434–438.Google Scholar
  30. del Rio, L.A., Pastori, G.M., Palma, J.M., Sandalio, L.M., Sandalio, F., Sevilla, F., Corpas, F.J., Jimenez, A., Lopez-Huertas, E. and Hernandez, J.A. 1998. The activated oxygen role of peroxisomes in senescence. Plant Physiol. 116: 1195–1200.Google Scholar
  31. de Vetten, N. and Huber, D.J. 1990. Cell wall changes during the expansion and senescence of carnation (Dianthus caryophyllus) petals. Physiol. Plant. 78: 447–454.Google Scholar
  32. Do, Y.-Y. and Huang, P.L. 1997. Gene structure of PAC01, a petal senescence-related gene from Phalaenopsis encoding peroxisomal acyl-CoA oxidase homolog. Biochem. Mol. Biol. Int. 41: 609–617.Google Scholar
  33. Evans, P.T. and Malmberg, R.L. 1989. Do polyamines have roles in plant development? Annu. Rev. Plant Physiol. Plant Mol. Biol. 40: 235–269.Google Scholar
  34. Faragher, J.D., Wachtel, E. and Mayak, S. 1987. Changes in the physical state of membrane lipids during senescence of rose petals. Plant Physiol. 83: 1037–1042.Google Scholar
  35. Garbarino, J.E., Oosumi, T. and Belknap, W.R. 1995. Isolation of a polyubiquitin promoter and its expression in transgenic potato plants. Plant Physiol. 109: 1371–1378.Google Scholar
  36. Garello, G., Menard, C., Dansereau, B. and LePage-Degivry, M.T. 1995. The influence of light quality on rose flower senescence: involvement of abscisic acid. Plant Growth Regul. 16: 135–139.Google Scholar
  37. Green, P.J. 1994. The ribonucleases of higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 421–445.Google Scholar
  38. Griffiths, C.M., Hosken, S.E., Oliver, D., Chojecki, J. and Thomas, H. 1997. Sequencing, expression pattern and RFLP mapping of a senescence-enhanced cDNA from Zea mays with high homology to oryzain and aleurain. Plant Mol. Biol. 34: 815–821.Google Scholar
  39. Guerrero, C., de la Calle, M., Reid, M.S. and Valpuesta, V. 1998. Analysis of the expression of two thiolprotease genes from daylily (Hemerocallis spp.) during flower senescence. Plant Mol. Biol. 36: 656–571.Google Scholar
  40. Halevy, A.H. 1998. Recent advances in postharvest physiology of flowers. J. Korean Soc. Hort. Soc. 39: 652–655.Google Scholar
  41. Halevy, A.H., Porat, R., Spiegelstein, H., Borochov, A., Botha, L. and Whitehead, C.S. 1996. Short-chain fatty acids in the regulation of pollination induced ethylene sensitivity of Phalaenopsis flowers. Physiol. Plant. 97: 469–474.Google Scholar
  42. Halliwell, B. and Gutteridge, J.M.C. 1989. Free Radicals in Biology and Medicine. Clarendon Press, Oxford, UK, pp. 450–499.Google Scholar
  43. He, C.-J., Morgan, P.W. and Drew, M.C. 1996. Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiol. 112: 463–472.Google Scholar
  44. Huang, F.-Y., Philosoph-Hadas, S., Meir, S., Callahan, D.A., Sabato, R., Zelcer, A. and Hepler, P.K. 1997. Increases in cytosolic Ca2C in parsley mesophyll cells correlated with leaf senescence. Plant Physiol. 115: 51–60.Google Scholar
  45. Ichimura, K. and Suto, K. 1998. Role of ethylene in acceleration of flower senescence by filament wounding in Portulaca hybrid. Physiol. Plant. 104: 603–607.Google Scholar
  46. Itzhaki, H., Davis, J.H., Borochov, A., Mayak, S. and Pauls, K.P. 1995. Deuterium magnetic resonance studies of senescencerelated changes in the physical properties of rose petal membrane lipids. Plant Physiol. 108: 1029–1033.Google Scholar
  47. Itzhaki, H., Mayak, S. and Borochov, A. 1998. Phosphatidylcholine turnover during senescence of rose petals. Plant Physiol. Biochem. 36: 457–462.Google Scholar
  48. Jacobson, M., Weil, M. and Raff, M.C. 1997. Programmed cell death in animal development. Cell 88: 347–354.Google Scholar
  49. Jones, M.L. and Woodson, W.R. 1999. Differential expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in carnation. Plant Physiol. 119: 755–764.Google Scholar
  50. Jones, M.L., Larsen, P.B. and Woodson, W.R. 1995. Ethyleneregulated expression of a carnation cysteine proteinase during flower petal senescence. Plant Mol. Biol. 28: 505–512.Google Scholar
  51. Lanahan, M.B., Yen, H.-C., Giovannoni, J.J. and Klee, H.J. 1994. The Never Ripe mutation blocks ethylene perception in tomato. Plant Cell 6: 521–530.Google Scholar
  52. Larsen, P.B., Ashworth, E.N., Jones, M.L. and Woodson, W.R. 1995. Pollination-induced ethylene in carnation. Plant Physiol. 108: 1405–1412.Google Scholar
  53. Laughton, K., Raghothama, K.G., Goldsbrough, P.B. and Woodson, W.R. 1990. Regulation of senescence-r elated gene expression in carnation flower petals by ethylene. Plant Physiol. 93: 1370–1375.Google Scholar
  54. Lay-Yee, M., Stead, A.D. and Reid, M.S. 1992. Flower senescence in daylily (Hemerocallis). Physiol. Plant. 86: 308–314.Google Scholar
  55. Lee, M., Lee, S.H.and Park, K.Y. 1997. Effects of spermine on ethylene biosynthesis in cut carnation (Dianthus caryophyllus L.) flowers during senescence. J. Plant Physiol. 151: 68–73.Google Scholar
  56. LePage-Degivry, M.T., Orlandini, M., Carello, G., Barthe, P. and Gudia, 1991. Regulation of ABA levels in senescing petals of rose flowers. Plant Growth Regul. 10: 67–72.Google Scholar
  57. Lers, A., Khalchitski, A., Lomaniec, E., Burd, S. and Green, P.J. 1998. Senescence-induced RNases in tomato. Plant Mol. Biol. 36: 439–449.Google Scholar
  58. Leshem, Y., Halevy, A.H. and Frenkel, C. 1986. Process and control of plant senescence. Dev. Crop Sci. 8: 142–161.Google Scholar
  59. Matile, P. and Winkenbach, F. 1971. Function of lysosomes and lysosomal enzymes in the senescing corolla of the morning glory. J. Exp. Bot. 22: 759–771.Google Scholar
  60. Mayak, S., Tirosh, T., Thompson, J.E. and Ghosh, S. 1998. The fate of ribulose-1,5-bisphosphate carboxylase subunits during development of carnation petals. Plant Physiol. Biochem. 36: 835–841.Google Scholar
  61. Meyer, R.C., Goldsbrough, P.B. and Woodson, W.R. 1991. An ethylene-responsive flower senescence-related gene from carnation encodes a protein homologous to glutathione S-transferases. Plant Mol. Biol. 17: 277–281.Google Scholar
  62. Michael, M.Z., Savin, K.W., Baudinette, S.C., Graham, M.W., Chandler, S.F., Lu, C.-Y., Caesar, C., Gautrais, I., Young, R., Nugent, C.D., Stevenson, K.R., O'Connor, E.L.-J., Cobbett, C.S., Cornish, E.C. 1993. Cloning of ethylene biosynthetic genes involved in petal senescence of carnation and petunia, and their antisense expression in transgenic plants. In: J.C. Pech, A. Latche and C. Balague (Eds.) Cellular and Molecular Aspects of the Plant Hormone Ethylene, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 298–303.Google Scholar
  63. Midoh, N., Saijou, Y., Matsumoto, K. and Iwata, M. 1996. Effects of 1,1-dimethyl-4-(phenylsulfonyl) semicarbazide (DPSS) on carnation flower longevity. Plant Growth Regul. 20: 195–199.Google Scholar
  64. Mittler, R. and Lam, E. 1995a. Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death. Plant Cell 7: 1951–1962.Google Scholar
  65. Mittler, R. and Lam, E. 1995b. In situ detection of nDNA fragmentation during the differentation of tracheary elements in higher plants. Plant Physiol. 108: 489–493.Google Scholar
  66. Mittler, R., Shulaev, V., Seskar, M. and Lam, E. 1996. Inhibition of programmed cell death in tobacco plants during pathogeninduced hypersensitive response at low oxygen pressure. Plant Cell 8: 1991–2001.Google Scholar
  67. Mutlu, A. and Gal, S. 1999. Plant aspartic proteinases: enzymes on the way to a function. Physiol. Plant. 105: 569–576.Google Scholar
  68. O'Brien, I.E.W., Baguley, B.C., Murray, B.G., Morris, B.A.M. and Ferguson, I.B. 1998. Early stages of the apoptotic pathway in plant cells are reversible. Plant J. 13: 803–814.Google Scholar
  69. O'Neill, S.D. 1997. Pollination regulation of flower development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 547–574.Google Scholar
  70. O'Neill, S.D., Nadeau, J.A., Zhang, X.S., Bui, A.Q. and Halevy, A.H. 1993. Interorgan regulation of ethylene biosynthetic genes by pollination. Plant Cell 5: 419–432.Google Scholar
  71. Orlandini, M., Arene, L. and LePage-Degivry, M.T. 1991. The relationship between petal water potential and levels of abscisic acid in rose flower. Acta. Hort. 298: 161–163.Google Scholar
  72. Orzaez, D. and Granell, A. 1997a. DNA fragmentation is regulated by ethylene during carpel senescence in Pisum sativum. Plant J. 11: 137–144.Google Scholar
  73. Orzaez, D. and Granell, A. 1997b. The plant homologue of the defender against apoptotic death gene is down-regulated during senescence of flower petals. FEBS Lett. 404: 275–278.Google Scholar
  74. Orzaez, D., Blay, R. and Granell, A. 1999. Programme of senescence in petals and carpels of Pisum sativum L. flowers and its control by ethylene. Planta 208: 220–226.Google Scholar
  75. Paliyath, G. and Droillard, M.J. 1992. The mechanisms of membrane deterioration and disassembly during senescence. Plant Physiol. Biochem. 30: 789–812.Google Scholar
  76. Panavas, T. and Rubinstein, B. 1998. Oxidative events during programmed cell death of daylily (Hemerocallis hybrid) petals. Plant Sci. 133: 125–138.Google Scholar
  77. Panavas, T., Reid, P.D. and Rubinstein, B. 1998. Programmed cell death of daylily petals: activities of wall-based enzymes and effects of heat shock. Plant Physiol. Biochem. 36: 379–388.Google Scholar
  78. Panavas, T., Pikula, A., Reid, P.D., Rubinstein, B. and Walker, E.L. 1999. Identification of senescence-associated genes from daylily petals. Plant Mol. Biol. 40: 237–248.Google Scholar
  79. Park, K.Y., Drory, A. and Woodson, W.R. 1992. Molecular cloning of a 1-aminocyclopropane-1-carboxylase synthase from senescing carnation flower petals. Plant Mol. Biol. 18: 377–386.Google Scholar
  80. Payton, S., Fray, R.G., Brown, S. and Grierson, D. 1996. Ethylene receptor expression is regulated during fruit ripening, flower senescence and abscission. Plant Mol. Biol. 31: 1227–1231.Google Scholar
  81. Phillips, H.L. Jr. and Kende, H. 1980. Structural changes in flowers of Ipomea tricolor during flower opening and closing. Protoplasma 102: 199–215.Google Scholar
  82. Pinedo, M.L., Goicoechea, S.M., Lamattina, L. and Conde, R.D. 1996. Estimation of ubiquitin and ubiquitin mRNA content in dark senescing wheat leaves. Biol. Plant. 38: 321–328.Google Scholar
  83. Podd, L.A. and van Staden, J. 1999. Is acetaldehyde the causal agent in the retardation of carnation flower senescence by ethanol? J. Plant Physiol. 154: 351–354.Google Scholar
  84. Porat, R., Borochov, A. and Halevy, A.H. 1993. Enhancement of petunia and Dendrobium flower senescence by jasmonic acid methyl ester is via the promotion of ethylene production. Plant Growth Regul. 13: 297–301.Google Scholar
  85. Porat, R., Borochov, A. and Halevy, A.H. 1994. Pollinationinduced senescence in Phalaenopsis petals. Relationship of ethylene sensitivity to activity of GTP-binding proteins and protein phosphorylation. Physiol. Plant. 90: 679–684.Google Scholar
  86. Porat, R., Reuveny, Y., Borochov, A. and Halevy, A.H. 1993b. Petunia flower longevity: the role of sensitivity to ethylene. Physiol. Plant. 89: 291–294.Google Scholar
  87. Porat, R., Reiss, N., Atzorn, R., Halevy, A.H. and Borochov, A. 1995. Examination of the possible involvement of lipoxygenase and jasmonates in pollination-induced senescence of Phalaenopsis and Dendrobium orchid flowers. Physiol. Plant. 94: 205–210.Google Scholar
  88. Porat, R., Nadeau, J.A., Kirby, J.A., Sutter, E.G. and O'Neill, S.D. 1998. Characterization of the primary pollen signal in the post pollination syndrome of Phalaenopsis flowers. Plant Growth Regul. 24: 109–117.Google Scholar
  89. Reid, M.S. and Wu, M.-J. 1992. Ethylene and flower senescence. Plant Growth Regul. 11: 37–43.Google Scholar
  90. Rottman, W.H., Peter, G.F., Oeller, P.W., Keller, J.A., Shen, N.F., Nagy, B.P., Taylor, L.P., Campbell, A.D. and Theologis, A. 1991. 1-aminocyclopropane-1-carboxylate synthase in tomato is encoded by a multigene family whose transcription is induced during fruit and floral senescence. J. Mol. Biol. 222: 937–961.Google Scholar
  91. Scandalios, J.G. 1993. Oxygen stress and superoxide dismutases. Plant Physiol. 101: 7–12.Google Scholar
  92. Serek, M., Tamari, G., Sisler, E.C. and Borochov, A. 1995. Inhibition of ethylene-induced cellular senescence symptoms by 1-methylcyclopropene, a new inhibitor of ethylene action. Physiol. Plant. 94: 229–232.Google Scholar
  93. Shykoff, J.A., Bucheli, E. and Kaltz, O. 1996. Flower lifespan and disease risk. Nature 379: 779–780.Google Scholar
  94. Siedow, J.N. 1991. Plant lipoxygenase: structure and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 145–188.Google Scholar
  95. Singh, A., Evenson, K.B. and Kao, T.-H. 1992. Ethylene synthesis and floral senescence following compatible and incompatible pollinations in Petunia inflata. Plant Physiol. 99: 38–45.Google Scholar
  96. Smart, C. 1994. Gene expression during leaf senescence. New Phytol. 126: 419–448.Google Scholar
  97. Smith, M.T., Saks, Y. and van Staden, J. 1992. Ultrastructural changes in the petals of senescing flowers of Dianthus caryophyllus L. Ann. Bot. 69: 277–285.Google Scholar
  98. Solomon, M., Belenghi, B., Delledonne, M., Menachem, M. 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
  99. Song, W.C. and Brash, A.R. 1991. Purification of an allene oxide synthase and identification of the enzyme as a cytochrome P-450. Science 253: 781–784.Google Scholar
  100. Sopory, S. and Munshi, M. 1998. Protein kinases and phosphatases and their role in cellular signalling in plants. Crit. Rev. Plant Sci. 17: 245–318.Google Scholar
  101. Stead, A.D. 1992. Pollination-induced flower senescence: a review. Plant Growth Regul 11: 13–20.Google Scholar
  102. Stead, A.D. and van Doorn 1994. Strategies of flower senescence - a review. In: R.J. Scott and A.D. Stead (Eds.) Molecular and Cellular Aspects of Plant Reproduction, Cambridge University Press, Cambridge, UK, pp. 215–238.Google Scholar
  103. Stephenson, P., Collins, B.A., Reid, P.D. and Rubinstein, B. 1996. Localization of ubiquitin to differentiating vascular tissues. Am. J. Bot. 83: 140–147.Google Scholar
  104. Stephenson, P. and Rubinstein, B. 1998. Characterization of proteolytic activity during senescence in daylilies. Physiol. Plant. 104: 463–473.Google Scholar
  105. Sylvestre, I., Droillard, M.-J., Bureau, J.-M. and Paulin, A. 1989. Effects of the ethylene rise on the peroxidation of membrane lipids during the senescence of cut carnations. Plant Physiol. Biochem. 27: 407–413.Google Scholar
  106. Takahashi, T., Mu, J.-H., Gasch, A. and Chua, N.-H. 1998. Identification by PCR of receptor-like kinases from arabidopsis. Plant Mol. Biol. 37: 587–596.Google Scholar
  107. Tang, X., Gomes, A.M.T.R., Bhatia, A. and Woodson, W.R. 1994. Pistil-specific and ethylene-regulated expression of 1-aminocyclopropane-1-carboxylate oxidase genes in petunia flowers. Plant Cell 6: 1227–1239.Google Scholar
  108. Taylor, C.B., Bariola, P.A., DelCardayre, S.B., Raines, R.T. and Green, P.J. 1993. A senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation. Proc. Natl. Acad. Sci. USA 90: 5118–5122.Google Scholar
  109. Thompson, J.E. 1988. The molecular basis for membrane deterioration during senescence. In: L.D. Nooden and A.C. Leopold (Eds.) Senescence and Aging in Plants, Academic Press, New York, pp. 51–83.Google Scholar
  110. Thompson, J.E., Froese, C.D., Hong, Y., Hudak, K.A. and Smith, M.D. 1997. Membrane deterioration during senescence. Can. J. Bot. 75: 867–879.Google Scholar
  111. Valpuesta, V., Lange, N.E., Cuerrero, C. and Reid, M.S. 1995. Upregulation of a cysteine protease accompanies the ethyleneinsensitive senescence of daylily (Hemerocallis) flowers. Plant Mol. Biol. 28: 575–582.Google Scholar
  112. van Altvorst, A.C. and Bovy, A.G. 1995. The role of ethylene in the senescence of carnation flowers: a review. Plant Growth Regul. 16: 43–53.Google Scholar
  113. van Doorn, W.G. 1997. Effects of pollination on floral attraction and longevity. J. Exp. Bot. 48: 1615–1622.Google Scholar
  114. van Doorn, W.G. and Stead, A.D. 1994. The physiology of petal senescence which is not initiated by ethylene. In: R.J. Scott and A.D. Stead (Eds.) Molecular and Cellular Aspects of Plant Reproduction, Cambridge University Press, Cambridge, UK, pp. 239–254.Google Scholar
  115. Vardi, Y. and Mayak, S. 1989. Involvement of abscisic acid during water stress and recovery in petunia flowers. Acta. Hort. 261: 107–112.Google Scholar
  116. Verlinden, S. and Woodson, W.R. 1998. The physiological and molecular responses of carnation flowers to high temperature. Postharvest Biol. Techn. 4: 185–192.Google Scholar
  117. Vierling, E. 1991. The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 579–620.Google Scholar
  118. Vierstra, R.D. 1993. Protein degradation in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 385–410.Google Scholar
  119. Wang, H., Brandt, A.S. and Woodson, W.R. 1993. A flower senescence-related mRNA from carnation encodes a novel protein related to enzymes involved in phosphonate biosynthesis. Plant Mol. Biol. 22: 719–724.Google Scholar
  120. Wang, H., Li, J., Bostock, R.M. and Gilchrist, D.G. 1996. Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8: 375–391.Google Scholar
  121. Whitehead, C.S. 1994. Ethylene sensitivity and flower senescence. In: R.J. Scott and A.D. Stead (Eds.) Molecular and Cellular Aspects of Plant Reproduction, Cambridge University Press, Cambridge, UK, pp. 269–284.Google Scholar
  122. Whitehead, C.S. and Vasiljevic, D. 1993. Role of short-chain saturated fatty acids in the control of ethylene sensitivity in senescing carnation flowers. Physiol. Plant. 88: 243–250.Google Scholar
  123. Wiemken-Gehrig, V., Wiemken, A. and Matile, P. 1974. Cell wall breakdown in wilting flowers of Ipomea tricolor Cav. Planta 115: 297–307.Google Scholar
  124. Willekens, H., Chamnongpol, S., Davey, M., Schrauder, M., Langebartels, C., Van Montagu, M., Inzé, D. and Van Camp, W. 1997. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J. 16: 4806–4816.Google Scholar
  125. Woffenden, B.J., Freeman, T.B. and Beers, E.P. 1998. Proteasome inhibitors prevent tracheary element differentiation in Zinnia mesophyll cell cultures. Plant Physiol. 118: 419–430.Google Scholar
  126. Woltering, E.J. and van Doorn, W.G. 1988. Role of ethylene and senescence of petals: morphological and taxonomical relationships. J. Exp. Bot. 39: 1605–1616.Google Scholar
  127. Woltering, E.J., de Vrije, T., Harren, F. and Hoekstra, F.A. 1997. Pollination and stigma wounding: same response, different signal? J. Exp. Bot. 48: 1027–1033.Google Scholar
  128. Woltering, E.J., Somhorst, D. and van der Veer, P. 1995. The role of ethylene in interorgan signalling during flower senescence. Plant Physiol. 109: 1219–1225.Google Scholar
  129. Woltering, E.J., ten Have, A., Larsen, P.B. and Woodson, W.R. 1994. Ethylene biosynthetic genes and interorgan signalling during flower senescence. In: R.J. Scott and A.D. Stead (Eds.) Molecular and Cellular Aspects of Plant Reproduction, Cambridge University Press, Cambridge, UK, pp. 285–307.Google Scholar
  130. Woodson, W.R. 1994. Molecular biology of flower senescence in carnation. In: R.J. Scott and A.D. Stead (Eds.) Molecular and Cellular Aspects of Plant Reproduction, Cambridge University Press, Cambridge, UK, pp. 255–267.Google Scholar
  131. Woodson, W.R. and Handa, A.K. 1987. Changes in protein patterns and in vivo protein synthesis during presenescence and senescence of Hibiscus petals. J. Plant Physiol. 128: 67–75.Google Scholar
  132. Woodson, W.R., Park, K.Y., Drory, A., Larsen, P.B. and Wang, H. 1992. Expression of ethylene biosynthetic pathway transcripts in senescing carnation flowers. Plant Physiol. 99: 526–532.Google Scholar
  133. Young, T.E., Gallie, D.R., DeMason, D.A. 1997. Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken 2 genotypes. Plant Physiol. 115: 737–751.Google Scholar
  134. Zelitch, I., Havir, E.A., McGonigle, B., McHale, N.A. and Nelson, T. 1991. Leaf catalase mRNA and catalase-protein levels in a high-catalase tobacco mutant with O2-resistant photosynthesis. Plant Physiol. 97: 1592–1595.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Bernard Rubinstein
    • 1
    • 2
  1. 1.Biology Department and Plant Biology Graduate ProgramUniversity of MassachusettsAmherst
  2. 2.USA

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