Petunia pp 301-324 | Cite as

Petunia Flower Senescence

  • Michelle L. Jones
  • Anthony D. Stead
  • David G. Clark


Senescence represents the last stage of floral development and is an active process that requires gene transcription and protein translation. A genetically controlled senescence program allows for the ordered degradation of organelles and macromolecules and the remobilization of essential nutrients from the petals. Petunia provides an excellent model system for studies of flower senescence because the plants flower profusely and have large floral organs amenable to molecular and biochemical analysis. While Petunia flowers have a finite lifespan that is under tight developmental control, petal senescence can be accelerated and synchronized by means of exogenous ethylene or by pollination. Petal senescence in Petunia is accompanied by decreased nucleic acid and protein content, DNA and nuclear fragmentation, and structural and compositional changes in the plasma membrane. These changes are correlated with increased mRNA abundance and enzyme activity of proteases, nucleases, and phospholipases. Major macronutrient levels in Petunia petals (collectively called the corolla) also decrease during senescence. These studies support cellular degradation and remobilization as the central functions of petal senescence. Ethylene is clearly involved in modulating the process, but the transcription factors and other components of the senescence signal transduction pathway(s) remain to be elucidated. Further studies focusing on early transcriptome changes during petal senescence will help to identify these early regulators, and subsequent studies of protein changes and the post-translational modification of senescence-related proteins will further our understanding of the pathways executing the senescence program.


Ethylene Production Flower Opening Senescence Program Flower Senescence Petal Senescence 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Arora, A. and Singh, V.P. (2004) Cysteine protease gene expression and proteolytic activity during floral development and senescence in ethylene-insensitive Gladiolus grandiflora. J. Plant Biochem. Biotech. 13, 123–126.Google Scholar
  2. Borochov, A. and Woodson, W.R. (1989) Physiology and biochemistry of flower petal senescence. Hortic. Rev. 11, 15–43.Google Scholar
  3. Borochov, A., Drori, A., Tirosh, T., Borochovneori, H. and Mayak, S. (1990) Quantitative and qualitative changes in membrane proteins during petal senescence. J. Plant Physiol. 136, 203–207.Google Scholar
  4. Borochov, A., Cho, M.H. and Boss, W.F. (1994) Plasma-membrane lipid metabolism of petunia petals during senescence. Physiol. Plant. 90, 279–284.CrossRefGoogle Scholar
  5. Borochov, A., Spiegelstein, H. and PhilosophHadas, S. (1997) Ethylene and flower petal senescence: Interrelationship with membrane lipid catabolism. Physiol. Plant. 100, 606–612.CrossRefGoogle Scholar
  6. Bovy, A.G., Angenent, G.C., Dons, H.J.M. and van Altvorst, A.C. (1999) Heterologous expression of the Arabidopsis etr1-1 allele inhibits the senescence of carnation flowers. Mol. Breed. 5, 301–308.CrossRefGoogle Scholar
  7. Breeze, E., Wagstaff, C., Harrison, E., Bramke, I., Rogers, H. and Stead, A. (2004) Gene expression patterns to define stages of post-harvest senescence in Alstroemeria petals. Plant Biotech. J. 2, 155–168.CrossRefGoogle Scholar
  8. Canetti, L., Lomaniec, E., Elkind, Y. and Lers, A. (2002) Nuclease activities associated with dark-induced and natural leaf senescence in parsley. Plant Sci. 163, 873–880.CrossRefGoogle Scholar
  9. Chang, C., Kwok, S.F., Bleecker, A.B. and Meyerowitz, E.M. (1993) Arabidopsis ethylene-response gene Etr1 - similarity of product to 2-component regulators. Science 262, 539–544.CrossRefPubMedGoogle Scholar
  10. Chang, H., Jones, M.L., Banowetz, G.M. and Clark, D.G. (2003) Overproduction of cytokinins in petunia flowers transformed with P-SAG12-IPT delays corolla senescence and decreases sensitivity to ethylene. Plant Physiol. 132, 2174–2183.CrossRefPubMedGoogle Scholar
  11. Chen, J.C., Jiang, C.Z., Gookin, T.E., Hunter, D.A., Clark, D.G. and Reid, M.S. (2004) Chalcone synthase as a reporter in virus-induced gene silencing studies of flower senescence. Plant Mol. Biol. 55, 521–530.CrossRefPubMedGoogle Scholar
  12. Chen, J.C., Jiang, C.Z. and Reid, M.S. (2005) Silencing a prohibitin alters plant development and senescence. Plant J. 44, 16–24.CrossRefPubMedGoogle Scholar
  13. Clark, D.G., Dervinis, C., Barrett, J.E., Klee, H.J. and Jones, M.L. (2004) Drought-induced leaf senescence and horticultural performance of transgenic P-SAG12-IPT petunias. J. Am. Soc. Hort. Sci. 129, 93–99.Google Scholar
  14. Clevenger, D.J., Barrett, J.E., Klee, H.J. and Clark, D.G. (2004) Factors affecting seed production in transgenic ethylene-insensitive petunias. J. Am. Soc. Hort. Sci. 129, 401–406.Google Scholar
  15. Eason, J.R., Ryan, D.J., Pinkney, T.T. and O'Donoghue, E.M. (2002) Programmed cell death during flower senescence: Isolation and characterization of cysteine proteinases from Sandersonia aurantiaca. Func. Plant Biol. 29, 1055–1064.CrossRefGoogle Scholar
  16. Ferrante, A., Vernieri, P., Tognoni, F. and Serra, G. (2006) Changes in abscisic acid and flower pigments during floral senescence of petunia. Biol. Plant. 50, 581–585.CrossRefGoogle Scholar
  17. Gan, S. and Amasino, R.M. (1995) Inhibition of leaf senescence by autoregulated production of cytokinins. Science 270, 1986–1988.CrossRefPubMedGoogle Scholar
  18. Gerats, T. and Vandenbussche, M. (2005) A model system for comparative research: Petunia. Trends Plant Sci. 10, 251–256.CrossRefPubMedGoogle Scholar
  19. Gilissen, L.J.W. and Hoekstra, F.A. (1984) Pollination-induced corolla wilting in Petunia-hybrida: Rapid transfer through the style of a wilting-inducing substance. Plant Physiol. 75, 496–498.CrossRefPubMedGoogle Scholar
  20. Gubrium, E.K., Clevenger, D.J., Clark, D.G., Barrett, J.E. and Nell, T.A. (2000) Reproduction and horticultural performance of transgenic ethylene-insensitive petunias. J. Am. Soc. Hort. Sci. 125, 277–281.Google Scholar
  21. 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, 565–571.CrossRefPubMedGoogle Scholar
  22. Himelblau, E. and Amasino, R.M. (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J. Plant Physiol. 158, 1317–1323.CrossRefGoogle Scholar
  23. Hoekstra, F.A. and Weges, R. (1986) Lack of control by early pistillate ethylene of the accelerated wilting of Petunia-hybrida flowers. Plant Physiol. 80, 403–408.CrossRefPubMedGoogle Scholar
  24. Hunter, D.A., Steele, B. and Reid, M.S. (2002) Identification of genes associated with perianth senescence in daffodil (Narcissus pseudonarcissus L. “Dutch Master”). Plant Sci. 163, 13–21.CrossRefGoogle Scholar
  25. Itai, A., Ishihara, K. and Bewley, J.D. (2003) Characterization of expression, and cloning, of β-D-xylosidase and α-L-arabinofuranosidase in developing and ripening tomato (Lycopersicon esculentum Mill.) fruit. J. Exp. Bot. 54, 2615–2622.CrossRefPubMedGoogle Scholar
  26. Itzhaki, H., Borochov, A. and Mayak, S. (1990) Age-related-changes in petal membranes from attached and detached rose flowers. Plant Physiol. 94, 1233–1236.CrossRefPubMedGoogle Scholar
  27. Jones, M.L., Larsen, P.B. and Woodson, W.R. (1995) Ethylene-regulated expression of a carnation cysteine proteinase during flower petal senescence. Plant Mol. Biol. 28, 505–512.CrossRefPubMedGoogle Scholar
  28. Jones, M.L. and Woodson, W.R. (1997) Pollination-induced ethylene in carnation: Role of stylar ethylene in corolla senescence. Plant Physiol. 115, 205–212.PubMedGoogle Scholar
  29. Jones, M.L. and Woodson, W.R. (1999a) Interorgan signaling following pollination in carnations. J. Am. Soc. Hort. Sci. 124, 598–604.Google Scholar
  30. Jones, M.L. and Woodson, W.R. (1999b) Differential expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in carnation. Plant Physiol. 119, 755–764.Google Scholar
  31. Jones, M.L. (2004) Changes in gene expression during senescence. In: L. Nooden (Ed.), Plant Cell Death Processes. Elsevier Science, San Diego, pp. 51–72.CrossRefGoogle Scholar
  32. Jones, M.L., Chaffin, G., Eason, J.R. and Clark, D.G. (2005) Ethylene-sensitivity regulates proteolytic activity and cysteine protease gene expression in Petunia corollas. J. Exp. Bot. 56, 2733–2744.CrossRefPubMedGoogle Scholar
  33. Jorgensen, R.A., Cluster, P.D., English, J., Que, Q.D. and Napoli, C.A. (1996) Chalcone synthase cosuppression phenotypes in petunia flowers: Comparison of sense vs antisense constructs and single-copy vs complex T-DNA sequences. Plant Mol. Biol. 31, 957–973.CrossRefPubMedGoogle Scholar
  34. Langston, B.L., Bai, S. and Jones, M.L. (2005) Increases in DNA fragmentation and induction of a senescence-specific nuclease are delayed during corolla senescence in ethylene-insensitive (etr1-1) transgenic petunias. J. Exp. Bot. 56, 15–23.CrossRefPubMedGoogle Scholar
  35. Lay Yee, M., Stead, A.D. and Reid, M.S. (1992) Flower senescence in daylily (Hemerocallis). Physiol. Plant. 86, 308–314.CrossRefGoogle Scholar
  36. Lei, C.H., Lindstrom, J.T. and Woodson, W.R. (1996) Reduction of 1-aminocyclopropane-1-carboxylic acid (ACC) in pollen by expression of ACC deaminase in transgenic petunias. Plant Physiol. 111, 675.Google Scholar
  37. Lers, A., Lomaniec, E., Burd, S. and Khalchitski, A. (2001) The characterization of LeNUC1, a nuclease associated with leaf senescence of tomato. Physiol. Plant. 112, 176–182.CrossRefPubMedGoogle Scholar
  38. Lovell, P.H., Lovell, P.J. and Nichols, R. (1987a) The importance of the stigma in flower senescence in petunia (Petunia-hybrida). Ann. Bot. 60, 41–47.Google Scholar
  39. Lovell, P.J., Lovell, P.H. and Nichols, R. (1987b) The control of flower senescence in Petunia (Petunia-hybrida). Ann. Bot. 60, 49–59.Google Scholar
  40. Mayak, S., Halevy A.H. and Katz, M. (1972) Correlative changes in phytohormones in relation to senescence processes in rose petals. Physiol. Plant. 27, 1–4.Google Scholar
  41. McClung, J., Jupe, E., Liu, X. and Dellorco, R. (1995) Prohibitin: Potential role in senescence, development, and tumor suppression. Exp. Gerontol. 30, 99–124.CrossRefPubMedGoogle Scholar
  42. Pak, C. and van Doorn, W.G. (2005) Delay of iris flower senescence by protease inhibitors. New Phytol. 165, 473–480.CrossRefPubMedGoogle Scholar
  43. Panavas, T., Walker, E.L. and Rubinstein, B. (1998) Possible involvement of abscisic acid in senescence of daylily petals. J. Exp. Bot. 49, 1987–1997.CrossRefGoogle Scholar
  44. Panavas, T., LeVangie, R., Mistler, J., Reid, P.D. and Rubinstein, B. (2000) Activities of nucleases in senescing daylily petals. Plant Physiol. Biochem. 38, 837–843.CrossRefGoogle Scholar
  45. Porat, R., Reuveny, Y., Borochov, A. and Halevy, A.P.H. (1993) Petunia flower longevity – The role of sensitivity to ethylene. Physiol. Plant. 89, 291–294.CrossRefGoogle Scholar
  46. Rogers, H.J. (2006) Programmed cell death in floral organs: How and why do flowers die? Ann. Bot. 97, 309–315.CrossRefPubMedGoogle Scholar
  47. Ronen, M. and Mayak, S. (1981) Interrelationship between abscisic-acid and ethylene in the control of senescence processes in carnation flowers. J. Exp. Bot. 32, 759–765.CrossRefGoogle Scholar
  48. Saha, S., Nagar, P.K. and Sircar, P.K. (1985) Changes in cytokinin activity during flower development in Cosmos-sulphureus Cav. Plant Growth Reg. 3, 27–35.CrossRefGoogle Scholar
  49. Sanmartin, M., Jaroszewski, L., Raikhel, N.P.V. and Rojo, E. (2005) Caspases: Regulating death since the origin of life. Plant Physiol. 137, 841–847.CrossRefPubMedGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. Shibuya, K., Barry, K.G., Ciardi, J.A., Loucas, H.M., Underwood, B.A., Nourizadeh, S., Ecker, J.R., Klee, H.J. and Clark, D.G. (2004) The central role of PhEIN2 in ethylene responses throughout plant development in petunia. Plant Physiol. 136, 2900–2912.CrossRefPubMedGoogle Scholar
  52. Shvarts, M., Weiss, D. and Borochov, A. (1997) Temperature effects on growth, pigmentation and post-harvest longevity of petunia flowers. Scientia Hortic. 69, 217–227.CrossRefGoogle Scholar
  53. 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.CrossRefPubMedGoogle Scholar
  54. Stead, A.D., van Doorn, W.G., Jones, M.L. and Wagstaff, C. (2006) Flower senescence: Fundamental and applied aspects. In: C. Ainsworth (Ed.), Flowering and Its Manipulation. Annual Plant Reviews. Vol. 20. Blackwell Publishing, Oxford, UK, pp. 261–296.Google Scholar
  55. Sugiyama, M., Ito, J., Aoyagi, S. and Fukuda, H. (2000) Endonucleases. Plant Mol. Biol. 44, 387–397.CrossRefPubMedGoogle Scholar
  56. Tang, X.Y., 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.CrossRefPubMedGoogle Scholar
  57. Taverner, E., Letham, D.S., Wang, J., Cornish, E. and Willcocks, D.A. (1999) Influence of ethylene on cytokinin metabolism in relation to Petunia corolla senescence. Phytochem. 51, 341–347.CrossRefGoogle Scholar
  58. Thomas, H., Ougham, H.J., Wagstaff, C. and Stead, A.D. (2003) Defining senescence and death. J. Exp. Bot. 54, 1127–1132.CrossRefPubMedGoogle Scholar
  59. Valpuesta, V., Lange, N.E., Guerrero, C. and Reid, M.S. (1995) Upregulation of a cysteine protease accompanies the ethylene-insensitive senescence of daylily (Hemerocallis) flowers. Plant Mol. Biol. 28, 575–582.CrossRefPubMedGoogle Scholar
  60. van Doorn, W.G., Harkema, H. and Song, J.S. (1995) Water relations and senescence of cut Iris flowers- effects of cycloheximide. Postharv. Biol. Technol. 5, 345–351.CrossRefGoogle Scholar
  61. van Doorn, W.G. (2001) Categories of petal senescence and abscission: A re-evaluation. Ann. Bot. 87, 447–456.CrossRefGoogle Scholar
  62. van Doorn, W.G., Balk, P.A., van Houwelingen, A.M., Hoeberichts, F.A., Hall, R.D. and Vorst, O. (2003) Gene expression during anthesis and senescence in iris flowers. Plant Mol. Biol. 53, 845–863.CrossRefPubMedGoogle Scholar
  63. van Doorn, W.G. and Woltering, E.J. (2005) Many ways to exit? Cell death categories in plants. Trends Plant Sci. 10, 117–122.PubMedGoogle Scholar
  64. Van Staden, J. and Dimalla, G.G. (1980) The effect of silver thiosulfate preservative on the physiology of cut carnations. 2. Influence on endogenous cytokinins. Zeitschrift Fur Pflanzenphysiol. 99, 19–26.Google Scholar
  65. Verlinden, S. (2003) Changes in mineral nutrient concentrations in petunia corollas during development and senescence. HortScience 38, 71–74.Google Scholar
  66. Wagstaff, C., Leverentz, M.K., Griffiths, G., Thomas, B., Chanasut, U. and Stead, A.D. (2002) Cysteine protease gene expression and proteolytic activity during senescence of Alstroemeria petals. J. Exp. Bot. 53, 233–240.CrossRefPubMedGoogle Scholar
  67. Wagstaff, C., Malcolm, P., Rafiq, A., Leverentz, M., Griffiths, G., Thomas, B., Stead, A. and Rogers, H. (2003) Programmed cell death (PCD) processes begin extremely early in Alstroemeria petal senescence. New Phytol. 160, 49–59.CrossRefGoogle Scholar
  68. Watada, A.E., Herner, R.C., Kader, A.A., Romani, R.J. and Staby, G.L. (1984) Terminology for the description of developmental stages of horticultural crops. HortScience 19, 20–21.Google Scholar
  69. Weaver, L.M., Gan, S.S., Quirino, B. and Amasino, R.M. (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol. Biol. 37, 455–469.CrossRefPubMedGoogle Scholar
  70. Wilkinson, J.Q., Lanahan, M.B., Clark, D.G., Bleecker, A.B., Chang, C., Meyerowitz, E.M. and Klee, H.J. (1997) A dominant mutant receptor from Arabidopsis confers ethylene insensitivity in heterologous plants. Nat. Biotech. 15, 444–447.CrossRefGoogle Scholar
  71. Wulster, G., Sacalis, J. and Janes, H. (1982) The effect of inhibitors of protein-synthesis on ethylene induced senescence in isolated carnation petals. J. Amer. Soc. Hortic. Sci. 107, 112–115.Google Scholar
  72. Xu, Y. and Hanson, M.R. (2000) Programmed cell death during pollination-induced petal senescence in petunia. Plant Physiol. 122, 1323–1333.CrossRefPubMedGoogle Scholar
  73. Yamada, T., Takatsu, Y., Kasumi, M., Ichimura, K. and van Doorn, W.G. (2006) Nuclear fragmentation and DNA degradation during programmed cell death in petals of morning glory (Ipomoea nil). Planta 224, 1279–1290.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Michelle L. Jones
    • 1
  • Anthony D. Stead
  • David G. Clark
  1. 1.Department of Horticulture and Crop ScienceThe Ohio State UniversityWoosterUSA

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