No signs of meristem senescence in old scots pine

Journal of Ecology

Volumn 102, Issue 3, 2014, Pages 555-565

  Mencuccini, Maurizio ^a,b   Oñate, Marta ^c   Peñuelas, Josep ^b,d   Rico, Laura ^b,d   Munné Bosch, Sergi ^c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b CREAF   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

^d CSIC   (Spain)

Author keywords

Ageing; DNA methylation; Growth; Reproduction; Scotland; Scots pine; Senescence; Size related processes

Indexed keywords

AGING; CONIFEROUS TREE; DNA; GRAFTING; GROWTH RATE; HISTOLOGY; HORMONE; METHYLATION; PHOTOSYNTHESIS; PHYSIOLOGY; PHYTOCHEMISTRY; PIGMENT; ROOTSTOCK; SENESCENCE;

PINUS SYLVESTRIS;

EID: 84898799089     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12219     Document Type: Article

References (84)

1. Abdul-Hamid, H. & Mencuccini, M. (2009) Age- and size-related changes in physiological characteristics and chemical composition of Acer pseudoplatanus and Fraxinus excelsior trees. Tree Physiology, 29, 27-38.
2. Ally, D., Ritland, K. & Otto, S.P. (2010) Aging in a long-lived clonal tree. PLOS Biology, 8, e1000454.
3. Amaral, J.S., Casal, S., Torres, D., Seabra, R.M. & Oliveira, B.P. (2005) Simultaneous determination of tocopherols and tocotrienols in hazelnuts by a normal phase liquid chromatographic method. Analytical Sciences, 21, 1545-1548.
4. Angelier, F., Weimerskirch, H., Dano, S. & Chastel, O. (2007) Age, experience and reproductive performance in a long-liver bird: a hormonal perspective. Behavioural Ecology and Sociobiology, 61, 611-621.
5. Bartholomew, A., Malcolm, D.C. & Nixon, C.J. (2001) The Scots pine population at Glen Loyne, Inverness-shire: present condition and regenerative capacity. Scottish Forestry, 55, 141-148.
6. Baudisch, A. (2005) Hamilton's indicators of the force of selection. Proceedings of the National Academy of Sciences of the United States of America, 102, 8263-8268.
7. Baudisch, A., Salguero-Gomez, R., Jones, O.R., Wrycza, T., Mbeau-Ache, C., Franco, M. & Colchero, F. (2013) The pace and shape of senescence in angiosperms. Journal of Ecology, 101, 596-606.
8. Beaumont, D., Dugan, D., Evans, G. & Taylor, S. (1995) Deer management and tree regeneration in the RSPB reserve at Abernethy forest. Our Pinewood Heritage (ed. J.R. Aldhous), pp. 186-195. Forestry Commission, Royal Society for the Protection of Birds and Scottish Natural Heritage, Edinburgh, UK.
9. Boege, K. & Marquis, R.J. (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology and Evolution, 20, 441-448.
10. Bond, B.J. (2000) Age-related changes in photosynthesis of woody plants. Trends in Plant Science, 5, 349-353.
11. Bond, B.J., Czarnomski, N.M., Cooper, C., Day, M.E. & Greenwood, M.S. (2007) Developmental decline in height growth in Douglas fir. Tree Physiology, 27, 441-453.
12. Bossdorf, O., Richards, C.L. & Pigliucci, M. (2008) Epigenetics for ecologists. Ecological Letters, 11, 106-115.
13. Carranza, J., Alarcos, S., Sanchez-Prieto, C.B., Valencia, J. & Mateos, C. (2004) Disposable-soma senescence mediated by sexual selection in an ungulate. Nature, 432, 2215-2218.
14. Caswell, H. (2012) Matrix models and sensitivity analysis of populations classified by age and stage: a vec-permutation matrix approach. Theoretical Ecology, 5, 403-417.
15. Caswell, H. & Salguero-Gómez, R. (2013) Age, stage, and senescence in plants. Journal of Ecology, 101, 585-595.
16. Chen, G.H., Wang, Y.J., Wang, X.M., Zhou, J.N. & Liu, R.Y. (2005) Effect of aging on species-typical behaviors in senescence-accelerated mouse. Physiology & Behaviour, 85, 536-545.
17. Chen, Y.-T., Shen, C.H., Lin, W.D., Chu, H.A., Huang, B.L., Kuo, C.I., Yeh, K.W., Huang, L.C. & Chang, I.F. (2012) Small RNAs of Sequoia sempervirens during rejuvenation and phase change. Plant Biology, 15, 27-36.
18. Curtin, F. & Schulz, P. (1998) Multiple correlations and Bonferroni's correction. Biological Psychiatry, 44, 775-777.
19. Day, M.E., Greenwood, M.S. & Díaz-Sala, C. (2002) Age- and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control. Tree Physiology, 22, 507-513.
20. Diaz-Sala, C., Rey, M., Boronat, A., Besford, R. & Rodriguez, R. (1995) Variations in the DNA methylation and polypeptide patterns of adult hazel (Corylus avellana L.) associated with sequential in vitro subcultures. Plant Cell Repords, 15, 218-221.
21. Edwards, C. & Mason, W.L. (2006) Stand structure and dynamics of four native Scots pine (Pinus sylvestris L.) woodlands in northern Scotland. Forestry, 79, 261-277.
22. Finch, C.E. (1990) Longevity, Senescence, and the Genome. University of Chicago Press, Chicago, IL.
23. Finnegan, E.J., Peacock, W.J. & Dennis, E.S. (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proceedings of the National Academy of Sciences of the United States of America, 93, 8449-8454.
24. Finnegan, E.J., Genger, R.K., Peacock, W.J. & Dennis, E.S. (1998) DNA methylation in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 223-247.
25. Fish, T., Wilson, R., Edwards, C., Mills, C., Crone, A., Kirchhefer, A.J., Linderholm, L., Loader, N.J. & Woodley, E. (2010) Exploring for senescence signals in native Scots pine (Pinus sylvestris L.) in the Scottish Highlands. Forest Ecology and Management, 260, 321-330.
26. Fraga, M.F., Cañal, M.J. & Rodríguez, R. (2002) Phase-change related epigenetic and physiological changes in Pinus radiata D. Don. Planta, 4, 672-678.
27. Fraga, M.F., Rodríguez, R. & Cañal, M.J. (2002) Genomic DNA methylation-demethylation during aging and reinvigoration of Pinus radiata. Tree Physiology, 22, 813-816.
28. Goslin, P.G. (2006) Tree seeds. The Encyclopedia of Seeds: Science, Technology and Uses (eds M. Black, J.D. Bewley & P. Halmer), pp. 725-731. CAB International, Wallingford.
29. Greenwood, M.S., Day, M.E. & Schatz, J. (2010) Separating the effects of tree size and meristem maturation on shoot development of grafted scions of red spruce (Picea rubens Sarg.). Tree Physiology, 30, 459-468.
30. Haffner, V., Enjalric, F., Lardet, L. & Carron, M.P. (1991) Maturation of woody plants: a review of metabolic and genomic aspects. Annales des Sciences Forestieres, 48, 615-630.
31. Hamilton, W.D. (1966) Moulding of senescence by natural selection. Journal of Theoretical Biology, 12, 12-45.
32. Harper, J.L. (1977) Population Biology of Plants. Academic Press, London, UK.
33. Holliday, R. & Plug, J.E. (1975) DNA modification mechanism and gene activity during development. Science, 187, 226-232.
34. Hudgins, J.W. & Franceschi, V.R. (2004) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiology, 129, 1003-1018.
35. Kirchhefer, A.J. (2001) Reconstruction of summer temperatures from tree-rings of Scots pine (Pinus sylvestris L.) in coastal northern Norway. Holocene, 11, 41-52.
36. van Kooten, O. & Snel, J.F.H. (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research, 25, 147-150.
37. Lambé, P., Mutambel, H.S.N., Fouche, J.-G., Deltour, R., Foidart, J.-M. & Gaspar, T. (1997) DNA methylation as a key process in regulation of organogenic totipotency and plant neoplastic progression? In Vitro Cellular & Developmental Biology-Plant, 33, 155-162.
38. Lichtenthaler, H.K. & Wellburn, A.R. (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11, 591-592.
39. Loehle, C. (1997) Optimal defensive investment in plants. Oikos, 49, 199-208.
40. Martínez-Vilalta, J., Vanderklein, D. & Mencuccini, M. (2007) Tree height and age-related decline in growth in Scots pine (Pinus sylvestris L.). Oecologia, 150, 529-544.
41. Matsuzaki, J., Norisada, M., Kodaira, J., Suzuki, M. & Tange, T. (2005) Shoots grafted into the upper crowns of tall Japanese cedar (Cryptomeria japonica D. Don) show foliar gas exchange characteristics similar to those of intact shoots. Trees, 19, 198-203.
42. Medawar, P. (1952) An Unsolved Problem of Biology. Lewis, London.
43. Mencuccini, M. & Grace, J. (1996) Hydraulic conductance, light interception and needle nutrient concentration in Scots pine stands (Thetford, UK) and their relations with net aboveground primary production. Tree Physiology, 16, 459-468.
44. Mencuccini, M., Martínez-Vilalta, J., Vanderklein, D., Hamid, H.A., Korakaki, E., Lee, S. & Michiels, B. (2005) Size-mediated ageing reduces vigour in trees. Ecology Letters, 8, 1183-1190.
45. Mencuccini, M., Martínez-Vilalta, J., Hamid, H.A., Korakaki, E. & Vanderklein, D. (2007) Evidence for age- and size-mediated controls of tree growth from grafting studies. Tree Physiology, 27, 463-473.
46. Müller, M. & Munné-Bosch, S. (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods, 7, 1-11.
47. Munné-Bosch, S. (2007) Aging in perennials. Critical Reviews in Plant Sciences, 26, 123-138.
48. Munné-Bosch, S. (2008) Do perennials really senesce? Trends in Plant Science, 13, 216-220.
49. Munné-Bosch, S. & Lalueza, P. (2007) Age-related changes in oxidative stress markers and abscisic acid levels in a drought-tolerant shrub, Cistus clusii grown under Mediterranean field conditions. Planta, 225, 1039-1049.
50. Oñate, M. & Munné-Bosch, S. (2008) Meristem aging is not responsible for the age-related changes in growth and abscisic acid levels in the Mediterranean shrub, Cistus clusii. Plant Biology, 10, 148-155.
51. Oñate, M. & Munné-Bosch, S. (2009) Influence of plant maturity, shoot reproduction and sex on vegetative growth in the dioecious plant, Urtica dioica. Annals of Botany, 104, 945-956.
52. Oñate, M. & Munné-Bosch, S. (2010) Loss of flower bud vigour in the Mediterranean shrub, Cistus albidus L. at advanced developmental stages. Plant Biology, 12, 475-483.
53. Pemeger, T.V. (1998) What is wrong with Bonferroni adjustments. British Medical Journal, 136, 1236-1238.
54. Peñuelas, J. & Munné-Bosch, S. (2010) Potentially immortal? New Phytologist, 187, 564-567.
55. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
56. Reimers, E., Holmengen, N. & Mysterud, A. (2005) Life-history variation of wild reindeer (Rangifer tarandus) in the highly productive North Ottadalen region. Norway Journal of Zoology, 265, 53-62.
57. Reyna-López, G.E., Simpson, J. & Ruiz-Herrera, J. (1997) Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Molecular Genetics and Genomics, 253, 703-710.
58. Ricklefs, R.E. & Finch, C.E. (1995) Aging: A Natural History. Scientific American Library, New York, NY, USA.
59. Roach, D.A. (1993) Evolutionary senescence in plants. Genetica, 91, 53-64.
60. Ronemus, M.J., Galbiati, M., Ticknor, C., Chen, J. & Dellaporta, S.L. (1996) Demethylation-induced developmental pleiotropy in Arabidopsis. Science, 273, 654-657.
61. Ryan, M.G., Binkley, D. & Fownes, J.H. (1997) Age-related decline in forest productivity: patterns and processes. Advances in Ecological Research, 27, 213-262.
62. Ryan, M.G. & Yoder, B.J. (1997) Hydraulic limits to tree height and tree growth. BioScience, 47, 235-242.
63. Salguero-Gómez, R. & Casper, B.B. (2010) Keeping plant shrinkage in the demographic loop. Journal of Ecology, 98, 312-323.
64. Salguero-Gómez, R. & Casper, B.B. (2011) A hydraulic explanation for size-specific plant shrinkage: developmental hydraulic sectoriality. New Phytologist, 189, 229-240.
65. Salguero-Gómez, R., Shefferson, R.P. & Hutchings, M.J. (2013) Plants do not count... or do they? New perspectives on the universality of senescence. Journal of Ecology, 101, 545-554.
66. Salmon, A., Clotault, J., Jenczewski, E., Chable, V. & Manzanares-Dauleux, M.J. (2008) Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Sciences, 174, 61-70.
67. Shefferson, R.P. & Roach, D.A. (2013) Longitudinal analysis in Plantago: strength of selection and reverse-age reveal age-indeterminate senescence. Journal of Ecology, 101, 577-584.
68. Silvertown, J., Franco, M. & Perez-Ishiwara, R. (2001) Evolution of senescence in iteroparous perennial plants. Evolutionary Ecological Research, 3, 393-412.
69. Taiz, L. & Zeiger, E. (2010) Plant Physiology. Sinauer Associates, Sunderland, MA, 782 pp.
70. Tenenhaus, A. & Tenenhaus, M. (2011) Regularized generalized canonical correlation analysis. Psychometrika, 76, 275-284.
71. Theiss, G. & Follmann, H. (1980) Methylcytosine formation in wheat embryo DNA. Biochemical Biophysical Research Communications, 94, 291-297.
72. Thomas, H. (2002) Ageing in plants. Mechanisms of Ageing and Development, 123, 747-753.
73. Thomas, H. (2012) Senescence, ageing and death of the whole plant. New Phytologist, 197, 696-711.
74. Tuomi, Y., Crone, E.E., Gremer, J.R., Jakalaniemi, A., Lesica, P., Pedersen, B. & Ramula, S. (2013) Prolonged dormancy interacts with senescence for two perennial herbs. Journal of Ecology, 101, 566-576.
75. Valdés, A.E., Fernández, B. & Centeno, M.L. (2003) Alterations in endogenous levels of cytokinins following grafting of Pinus radiata support ratio of cytokinins as an index of ageing and vigour. Journal of Plant Physiology, 160, 1407-1410.
76. Valdés, A.E., Fernández, B. & Centeno, M.L. (2004) Hormonal changes throughout maturation and ageing in Pinus pinea. Plant Physiology & Biochemistry, 42, 335-340.
77. Valdés, A.E., Centeno, M.L., Espinel, S. & Fernández, B. (2002) Could plant hormones be the basis of maturation indices in Pinus radiata? Plant Physiology & Biochemistry, 40, 211-216.
78. Vanderklein, D., Martínez-Vilalta, J., Lee, S. & Mencuccini, M. (2007) Plant size, not age, regulates growth and gas exchange in grafted Scots pine trees. Tree Physiology, 27, 71-79.
79. Vaupel, J.W. (1990) Relatives risks: frailty models of life history risks. Theoretical Population Biology, 37, 220-234.
80. Vaupel, J.W., Manton, K.G. & Stallard, E. (1979) The impact of heterogeneity in individual frailty on the dynamics of mortality. Demography, 16, 439-454.
81. Vaupel, J.W., Baudisch, A., Dölling, M., Roach, D.A. & Gampe, J. (2004) The case for negative senescence. Theoretical Population Biology, 65, 339-351.
82. Webber, B.L. & Woodrow, I.E. (2009) Chemical and physical plant defence across multiple ontogenetic stages in a tropical rain forest understorey tree. Journal of Ecology, 97, 761-771.
83. Williams, G.C. (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution, 11, 398-411.
84. Yoda, K., Shinozaki, K., Ogawa, H., Hozumi, K. & Kira, T. (1965) Estimation of the total amount of respiration in woody organs of trees and forest communities. Journal of Biology, Osaka City University, 16, 15-26.