Russian Journal of Plant Physiology

, Volume 59, Issue 4, pp 467–478 | Cite as

Towards an integrated view of monocarpic plant senescence

  • P. J. DaviesEmail author
  • S. Gan


After the flowering of an annual plant, the whole plant will senesce and die. For the process to go to completion, this monocarpic senescence must include three coordinated processes, which have not previously been considered as a total syndrome: (1) the arrest of growth and senescence of the shoot apical meristem; (2) senescence of the leaves; and (3) the suppression of axillary bud growth. Concurrently there is a shift in resource allocation from continued vegetative growth to reproductive growth, combined with a withdrawal of nutrients, especially nitrogen compounds, from the leaves and the transfer of these nutrients to the developing seeds. The start of the senescence process is caused by a shift, almost certainly in gene expression, very early in the reproductive phase. Continuation of the resource transfer and senescence of the vegetative plant involves hormonal regulation and continued changes in gene expression. Each of these processes is examined, especially with reference to the transfer of resources from vegetative to reproductive growth.


Pisum sativum Arabidopsis thaliana Spinacia oleracea senescence monocarpic whole plant resource allocation leaf apical bud axillary buds flowering reproduction sugar nitrogen 



jasmonic acid


long day


short day


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Kelly, M.O. and Davies, P.J., The Control of Whole Plant Senescence, Crit. Rev. Plant Sci., 1988, vol. 7, pp. 139–173.CrossRefGoogle Scholar
  2. 2.
    Sklensky, D.E. and Davies, P.J., Whole Plant Senescence: Reproduction and Nutrient Partitioning, Hort. Rev., 1993, vol. 15, pp. 335–366.Google Scholar
  3. 3.
    Gan, S., Senescence Processes in Plants, Oxford: Blackwell, 2007.CrossRefGoogle Scholar
  4. 4.
    Sklensky, D.E. and Davies, P.J., Resource Partitioning to Male and Female Flowers of Spinacia oleracea L. in Relation to Whole-Plant Monocarpic Senescence, J. Exp. Bot., 2011, vol. 62, pp. 4323–4336.PubMedCrossRefGoogle Scholar
  5. 5.
    Guo, Y. and Gan, S., AtMYB2 Regulates Whole Plant Senescence by Inhibiting Cytokinin-Mediated Branching at Late Stages of Development in Arabidopsis, Plant Physiol., 2011, vol. 156, pp. 1612–1619.PubMedCrossRefGoogle Scholar
  6. 6.
    Proebsting, W.M., Davies, P.J., and Marx, G.A., Photoperiodic Control of Apical Senescence in a Genetic Line of Peas, Plant Physiol., 1976, vol. 58, pp. 800–802.PubMedCrossRefGoogle Scholar
  7. 7.
    Davies, P.J., Proebsting, W.M., and Gianfagna, T.J., Hormonal Relationships in Whole Plant Senescence, Plant Growth Regulation, Pilet, P.E, Ed., Heidelberg: Springer-Verlag, 1977, pp. 273–280.CrossRefGoogle Scholar
  8. 8.
    Murfet, I.C. and Marx, G.A., Flowering in Pisum: Comparison of the Genewa and Hobart Systems of Phenotypic Classification, Pisum Newslett., 1976, vol. 8, pp. 46–48.Google Scholar
  9. 9.
    Proebsting, W.M., Davies, P.J., and Marx, G.A., Photoperiod-Induced Changes in Gibberellin Metabolism in Relation to Apical Growth and Senescence in a Genetic Line of Peas (Pisum sativum L.), Planta, 1978, vol. 141, pp. 231–238.CrossRefGoogle Scholar
  10. 10.
    Murfet, I.C., Flowering in Pisum: Reciprocal Grafts between Known Genotypes, Aust. J. Biol. Sci., 1971, vol. 24, pp. 1089–1101.Google Scholar
  11. 11.
    Murfet, I.C., Flowering in Pisum: Hr, a Gene for High Response to Photoperiod, Heredity, 1973, vol. 31, pp. 157–164.CrossRefGoogle Scholar
  12. 12.
    Murfet, I.C. and Reid, J.B., Flowering in Pisum: Evidence That Gene Sn Controls a Graft-Transmissible Inhibitor, Aust. J. Biol. Sci., 1973, vol. 26, pp. 675–677.Google Scholar
  13. 13.
    Kelly, M.O. and Davies, P.J., Genetic and Photoperiodic Control of the Relative Rates of Reproductive and Vegetative Development in Peas, Ann. Bot., 1986, vol. 58, pp. 13–21.Google Scholar
  14. 14.
    Wang, D.Y., Li, Q., Cui, K.M., and Zhu, Y.X., Gibberellin Is Involved in the Regulation of Cell Death-Mediated Apical Senescence in G2 Pea, J. Int. Plant Biol., 2007, vol. 49, pp. 1627–1633.CrossRefGoogle Scholar
  15. 15.
    Hensel, L.L., Grbic, V., Baumgarten, D.A., and Bleecker, A.B., Developmental and Age-Related Processes That Influence the Longevity and Senescence of Photosynthetic Tissues in Arabidopsis, Plant Cell, 1993, vol. 5, pp. 553–564.PubMedGoogle Scholar
  16. 16.
    Mondal, M.H., Brun, W.A., and Brenner, M.L., Effects of Sink Removal on Photosynthesis and Senescence in Leaves of Soybean (Glycine max L.) Plants, Plant Physiol., 1978, vol. 61, pp. 394–397.PubMedCrossRefGoogle Scholar
  17. 17.
    Wittenbach, V.A., Effects of Pod Removal on Leaf Senescence in Soybeans, Plant Physiol., 1982, vol. 70, pp. 1544–1548.PubMedCrossRefGoogle Scholar
  18. 18.
    Wittenbach, V.A., Effect of Pod Removal on Leaf Senescence and Soluble Protein Composition of Field-Grown Soybeans, Plant Physiol., 1983, vol. 73, pp. 121–124.PubMedCrossRefGoogle Scholar
  19. 19.
    Borrell, A., Hammer, G., and van Oosterom, E., Stay-Green: A Consequence of the Balance between Supply and Demand for Nitrogen during Grain Filling? Ann. Appl. Biol., 2001, vol. 138, pp. 91–95.CrossRefGoogle Scholar
  20. 20.
    Guiboileau, A., Sormani, R., Meyer, C., and Masclaux-Daubresse, C., Senescence and Death of Plant Organs: Nutrient Recycling and Developmental Regulation, C. R. Acad. Sci., Ser. Biol., 2010, vol. 333, pp. 382–391.Google Scholar
  21. 21.
    Kelly, M.O. and Davies, P.J., Photoperiodic and Genetic Control of Carbon Partitioning in Peas and Its Relationship to Apical Senescence, Plant Physiol., 1988, vol. 86, pp. 978–982.PubMedCrossRefGoogle Scholar
  22. 22.
    Zhu, Y.-X. and Davies, P.J., The Control of Apical Bud Growth and Senescence by Auxin and Gibberellin in Genetic Lines of Peas, Plant Physiol., 1997, vol. 113, pp. 631–637.PubMedGoogle Scholar
  23. 23.
    Crafts-Brandner, S.J. and Egli, D.B., Modification of Seed Growth in Soybean by Physical Restraint Effect on Leaf Senescence, J. Exp. Bot., 1987, vol. 38, pp. 2043–2049.CrossRefGoogle Scholar
  24. 24.
    Miceli, F., Crafts-Brandner, S.J., and Egli, D.B., Physical Restriction of Pod Growth Alters Development of Soybean Plants, Crop Sci., 1995, vol. 35, pp. 1080–1085.CrossRefGoogle Scholar
  25. 25.
    Murfet, I.C., The Influence of Genes Ar and Sn on Senescence in Pisum sativum L., Ann. Bot., 1985, vol. 55, pp. 675–684.Google Scholar
  26. 26.
    Borras, L., Maddonni, G.A., and Otegui, M.E., Leaf Senescence in Maize Hybrids: Plant Population, Row Spacing and Kernel Set Effects, Field Crops Res., 2003, vol. 82, pp. 13–26.CrossRefGoogle Scholar
  27. 27.
    Yang, J., Zhang, J., Wang, Z., Zhu, Q., and Liu, L., Water Deficit-Induced Senescence and Its Relationship to the Remobilization of Pre-Stored Carbon in Wheat during Grain Filling, Agron. J., 2001, vol. 93, pp. 196–206.CrossRefGoogle Scholar
  28. 28.
    Yang, J., Zhang, J., Wang, Z., Zhu, Q., and Wang, W., Hormonal Changes in the Grains of Rice Subjected to Water Stress during Grain Filling, Plant Physiol., 2001, vol. 127, pp. 315–323.PubMedCrossRefGoogle Scholar
  29. 29.
    Yang, J., Zhang, J., Wang, Z., Liu, L., and Zhu, Q., Postanthesis Water Deficits Enhance Grain Filling in Two-Line Hybrid Rice, Crop Sci., 2003, vol. 43, pp. 2099–2108.CrossRefGoogle Scholar
  30. 30.
    Leopold, A.C., Niedergang-Kamien, E., and Janick, J., Experimental Modification of Plant Senescence, Plant Physiol., 1959, vol. 34, pp. 570–573.PubMedCrossRefGoogle Scholar
  31. 31.
    Paul, M.J. and Foyer, C.H., Sink Regulation of Photosynthesis, J. Exp. Bot., 2001, vol. 52, pp. 1383–1400.PubMedCrossRefGoogle Scholar
  32. 32.
    Krapp, A. and Stitt, M., An Evaluation of Direct and Indirect Mechanisms for the “Sink-Regulation” of Photosynthesis in Spinach: Changes in Gas Exchange, Carbohydrates, Metabolites, Enzyme Activities and Steady-State Transcript Levels after Cold-Girdling Source Leaves, Planta, 1995, vol. 195, pp. 313–323.CrossRefGoogle Scholar
  33. 33.
    Roitsch, T., Balibrea, M., Hofmann, M., Proels, R., and Sinha, A., Extracellular Invertase: Key Metabolic Enzyme and PR Protein, J. Exp. Bot., 2003, vol. 54, pp. 513–524.PubMedCrossRefGoogle Scholar
  34. 34.
    Engelke, T., Hirsche, J., and Roitsch, T., Anther-Specific Carbohydrate Supply and Restoration of Metabolically Engineered Male Sterility, J. Exp. Bot., 2010, vol. 61, pp. 2693–2706.PubMedCrossRefGoogle Scholar
  35. 35.
    Koch, K.E., Carbohydrate-Modulated Gene Expression in Plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1996, vol. 47, pp. 509–540.PubMedCrossRefGoogle Scholar
  36. 36.
    Huber, S.C. and Huber, J.L., Role and Regulation of Sucrose-Phosphate Synthase in Higher Plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1996, vol. 47, pp. 431–444.PubMedCrossRefGoogle Scholar
  37. 37.
    Wingler, A. and Roitsch, T., Metabolic Regulation of Leaf Senescence: Interactions of Sugar Signalling with Biotic and Abiotic Stress Responses, Plant Biol., 2008, vol. 10, pp. 50–62.PubMedCrossRefGoogle Scholar
  38. 38.
    Lim, P.O., Kim, H.J., and Nam, H.G., Leaf Senescence, Annu. Rev. Plant Biol., 2007, vol. 58, pp. 115–136.PubMedCrossRefGoogle Scholar
  39. 39.
    Levey, S. and Wingler, A., Natural Variation in the Regulation of Leaf Senescence and Relation to Other Traits in Arabidopsis, Plant Cell Environ., 2005, vol. 28, pp. 223–231.CrossRefGoogle Scholar
  40. 40.
    Lim, P.O. and Nam, H.G., The Molecular and Genetic Control of Leaf Senescence and Longevity in Arabidopsis, Curr. Top. Dev. Biol., 2005, vol. 67, pp. 49–83.PubMedCrossRefGoogle Scholar
  41. 41.
    Gan, S., The Hormonal Regulation of Senescence, Plant Hormones: Biosynthesis, Signal Transduction, Action! Davies, P.J, Ed., Dordrecht: Springer-Verlag, 2010, pp. 597–617.Google Scholar
  42. 42.
    Gan, S. and Amasino, R.M., Inhibition of Leaf Senescence by Autoregulated Production of Cytokinin, Science, 1995, vol. 270, pp. 1986–1988.PubMedCrossRefGoogle Scholar
  43. 43.
    Guo, Y., Cai, Z., and Gan, S., Transcriptome of Arabidopsis Leaf Senescence, Plant Cell Environ., 2004, vol. 27, pp. 521–549.CrossRefGoogle Scholar
  44. 44.
    Guo, Y. and Gan, S., AtNAP, a NAC Family Transcription Factor, Has an Important Role in Leaf Senescence, Plant J., 2006, vol. 46, pp. 601–612.PubMedCrossRefGoogle Scholar
  45. 45.
    Pulido, A. and Laufs, P., Co-Ordination of Developmental Processes by Small RNAs during Leaf Development, J. Exp. Bot., 2010, vol. 61, pp. 1277–1291.PubMedCrossRefGoogle Scholar
  46. 46.
    Schommer, C., Palatnik, J.F., Aggarwal, P., Chetelat, A., Cubas, P., Farmer, E.E., Nath, U., and Weigel, D., Control of Jasmonate Biosynthesis and Senescence by MiR319 Targets, PLoS Biol., 2008, vol. 6, pp. 1991–2001.CrossRefGoogle Scholar
  47. 47.
    Van Doorn, W.G., Is the Onset of Senescence in Leaf Cells of Intact Plants Due to Low or High Sugar Levels? J. Exp. Bot., 2008, vol. 59, pp. 1963–1972.PubMedCrossRefGoogle Scholar
  48. 48.
    Pourtau, N., Jennings, R., Pelzer, E., Pallas, J., and Wingler, A., Effect of Sugar-Induced Senescence on Gene Expression and Implications for the Regulation of Senescence in Arabidopsis, Planta, 2006, vol. 224, pp. 556–568.PubMedCrossRefGoogle Scholar
  49. 49.
    Sheehy, J., Mnzava, M., Cassman, K., Mitchell, P., Pablico, P., Robles, R., Samonte, H., Lales, J., and Ferrer, A., Temporal Origin of Nitrogen in the Grain of Irrigated Rice in the Dry Season: The Outcome of Uptake, Cycling, Senescence and Competition Studied Using a 15N-Point Placement Technique, Field Crops Res., 2004, vol. 89, pp. 337–348.CrossRefGoogle Scholar
  50. 50.
    Wingler, A., Purdy, S., MacLean, J.A., and Pourtau, N., The Role of Sugars in Integrating Environmental Signals during the Regulation of Leaf Senescence, J. Exp. Bot., 2006, vol. 57, pp. 391–399.PubMedCrossRefGoogle Scholar
  51. 51.
    Parrott, D., Yang, L., Shama, L., and Fischer, A.M., Senescence Is Accelerated, and Several Proteases Are Induced by Carbon “Feast” Conditions in Barley (Hordeum vulgare L.) Leaves, Planta, 2005, vol. 222, pp. 989–1000.PubMedCrossRefGoogle Scholar
  52. 52.
    Parrott, D.L., McInnerney, K., Feller, U., and Fischer, A.M., Steam-Girdling of Barley (Hordeum vulgare) Leaves Leads to Carbohydrate Accumulation and Accelerated Leaf Senescence, Facilitating Transcriptomic Analysis of Senescence-Associated Genes, New Phytol., 2007, vol. 176, pp. 56–69.PubMedCrossRefGoogle Scholar
  53. 53.
    Agüera, E., Cabello, P., and de la Haba, P., Induction of Leaf Senescence by Low Nitrogen Nutrition in Sunflower (Helianthus annuus) Plants, Physiol. Plant., 2010, vol. 138, pp. 256–267.PubMedCrossRefGoogle Scholar
  54. 54.
    Taylor, L., Nunes-Nesi, A., Parsley, K., Leiss, A., Leach, G., Coates, S., Wingler, A., Fernie, A.R., and Hibberd, J.M., Cytosolic Pyruvate, Orthophosphate Dikinase Functions in Nitrogen Remobilization during Leaf Senescence and Limits Individual Seed Growth and Nitrogen Content, Plant J., 2010, vol. 62, pp. 641–652.PubMedCrossRefGoogle Scholar
  55. 55.
    Srivalli, B. and Khanna-Chopra, R., The Developing Reproductive ’sink’ Induces Oxidative Stress to Mediate Nitrogen Mobilization during Monocarpic Senescence in Wheat, Biochem. Biophys. Res. Commun., 2004, vol. 325, pp. 198–202.PubMedCrossRefGoogle Scholar
  56. 56.
    Jukanti, A.K., Heidlebaugh, N.M., Parrott, D.L., Fischer, I.A., McInnerney, K., and Fischer, A.M., Comparative Transcriptome Profiling of Near-Isogenic Barley (Hordeum vulgare) Lines Differing in the Allelic State of a Major Grain Protein Content Locus Identifies Genes with Possible Roles in Leaf Senescence and Nitrogen Reallocation, New Phytol., 2008, vol. 177, pp. 333–349.PubMedGoogle Scholar
  57. 57.
    Parrott, D.L., Martin, J.M., and Fischer, A.M., Analysis of Barley (Hordeum vulgare) Leaf Senescence and Protease Gene Expression: A Family C1A Cysteine Protease Is Specifically Induced under Conditions Characterized by High Carbohydrate, but Low to Moderate Nitrogen Levels, New Phytol., 2010, vol. 187, pp. 313–331.PubMedCrossRefGoogle Scholar
  58. 58.
    Lammer, D., Cai, X., Arterburn, M., Chatelain, J., Murray, T., and Jones, S., A Single Chromosome Addition from Thinopyrum elongatum Confers a Polycarpic, Perennial Habit to Annual Wheat, J. Exp. Bot., 2004, vol. 55, pp. 1715–1720.PubMedCrossRefGoogle Scholar
  59. 59.
    Wingler, A., Purdy, S.J., Edwards, S.A., Chardon, F., and Masclaux-Daubresse, C., QTL Analysis for Sugar-Regulated Leaf Senescence Supports Flowering-Dependent and -Independent Senescence Pathways, New Phytol., 2010, vol. 185, pp. 420–433.PubMedCrossRefGoogle Scholar
  60. 60.
    Lacerenza, J.A., Parrott, D.L., and Fischer, A.M., A Major Grain Protein Content Locus on Barley (Hordeum vulgare L.) Chromosome 6 Influences Flowering Time and Sequential Leaf Senescence, J. Exp. Bot., 2010, vol. 61, pp. 3137–3149.PubMedCrossRefGoogle Scholar
  61. 61.
    Nooden, L.D. and Penney, J.P., Correlative Controls of Senescence and Plant Death in Arabidopsis thaliana (Brassicaceae), J. Exp. Bot., 2001, vol. 52, pp. 2151–2159.PubMedGoogle Scholar
  62. 62.
    Beveridge, C.A. and Rameau, C., Strigolactones: The New Class of Branching Hormones, Plant Hormones: Biosynthesis, Signal Transduction, Action! Davies, P.J. Ed., Dordrecht: Springer-Verlag, 2010, pp. 507–518.Google Scholar
  63. 63.
    Munne-Bosch, S., Aging in Perennials, Crit. Rev. Plant Sci., 2007, vol. 26, pp. 123–138.CrossRefGoogle Scholar
  64. 64.
    Thomas, H. and Howarth, C.J., Five Ways to Stay Green, J. Exp. Bot., 2000, vol. 51, pp. 329–337.PubMedCrossRefGoogle Scholar
  65. 65.
    Kassahun, B., Bidinger, F., Hash, C., and Kuruvinashetti, M., Stay-Green Expression in Early Generation Sorghum [Sorghum bicolor (L.) Moench] QTL Introgression Lines, Euphytica, 2010, vol. 172, pp. 351–362.CrossRefGoogle Scholar
  66. 66.
    Baninasab, B., Rahemi, M., and Shariatmadari, H., Seasonal Changes in Mineral Content of Different Organs in the Alternate Bearing of Pistachio Trees, Commun. Soil Sci. Plant Anal., 2007, vol. 38, pp. 241–258.CrossRefGoogle Scholar
  67. 67.
    Munoz-Fambuena, N., Mesejo, C., Gonzalez-Mas, C.M., Primo-Millo, E., Agusti, M., and Iglesias, D.J., Fruit Regulates Seasonal Expression of Flowering Genes in Alternate-Bearing’ Moncada’ Mandarin, Ann. Bot., 2011, vol. 108, pp. 511–519.PubMedCrossRefGoogle Scholar
  68. 68.
    Molisch, H., The Longevity of Plants (Der Lebensdauer der Pflanze), New York: E.H. Fulling, 1938.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  1. 1.Departments of Plant Biology and HorticultureCornell UniversityIthacaUSA

Personalised recommendations