Isoprenoid emission in hygrophyte and xerophyte European woody flora: Ecological and evolutionary implications

Global Ecology and Biogeography

Volumn 23, Issue 3, 2014, Pages 334-345

  Loreto, Francesco ^a   Bagnoli, Francesca ^b   Calfapietra, Carlo ^a,c   Cafasso, Donata ^d   De Lillis, Manuela ^a   Filibeck, Goffredo ^e   Fineschi, Silvia ^b   Guidolotti, Gabriele ^e   Sramkó, Gábor ^f   Tökölyi, Jácint ^g   Ricotta, Carlo ^h  

^a CNR   (Italy)

^b INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

^c CzechGlobe Global Change Research Centre AS CR vvi   (Czech Republic)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e UNIVERSITY OF TUSCIA   (Italy)

^f INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^g UNIVERSITY OF DEBRECEN   (Hungary)

^h SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Adaptation; Chemo taxonomy; Hygrophytes; Isoprene; Monoterpenes; Phylogenies; Salicaceae; Water stress; Xerophytes

Indexed keywords

EID: 84893874222     PISSN: 1466822X     EISSN: 14668238     Source Type: Journal    
DOI: 10.1111/geb.12124     Document Type: Article

References (64)

1. Abouheif, E. (1999) A method for testing the assumption of phylogenetic independence in comparative data. Evolutionary Ecology Research, 1, 895-909.
2. Altschul, S.F., Madden, T.L., Schäffer, A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389-3402.
3. Bennet, K., Tzedakis, P. & Willis, K. (1991) Quaternary refugia of north European trees. Journal of Biogeography, 18, 103-115.
4. Biffin, E., Lucas, E.J., Craven, L.A., Ribeiro da Costa, I., Harrington, M.G. & Crisp, M.D. (2010) Evolution of exceptional species richness among lineages of fleshy-fruited Myrtaceae. Annals of Botany, 106, 79-93.
5. Blondel, J. & Aronson, J. (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, Oxford.
6. Böhling, N., Greuter, W. & Raus, T. (2002) Zeigerwerte der Gefäßpflanzen der Südägäis (Griechenland) [Indicator values of the vascular plants in the southern Aegean (Greece)]. Braun-Blanquetia, 32, 1-106.
7. Comes, H.P. (2004) The Mediterranean region - a hotspot for plant biogeographic research. New Phytologist, 164, 11-14.
8. Conti, F., Abbate, G., Alessandrini, A. & Blasi, C. (2005) An annotated checklist of the Italian vascular flora. Palombi Editore, Roma.
9. Dicke, M. & Baldwin, I.T. (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. Trends in Plant Science, 15, 167-175.
10. Diekmann, M. (2003) Species indicator values as an important tool in applied plant ecology - a review. Basic and Applied Ecology, 4, 493-506.
11. Duprè, C., Stevens, C., Ranke, T., Leeker, A., Peppeler-Lisbach, C., Gowing, D., Dise, N.B., Dorland, E., Bobbink, R. & Diekmann, M. (2010) Changes in species richness and composition in European acidic grasslands over the past 70 years: the contribution of cumulative atmospheric nitrogen deposition. Global Change Biology, 16, 344-357.
12. Eckenwalder, J. (1996) Systematics and evolution of Populus. Biology of Populus and its implication for management and conservation (ed. by H. Stettler, J. Bradshaw and P.H.T. Heilman), pp. 7-32. NRC Research Press, Ottawa.
13. Eiserhardt, W.L., Svenning, J.C., Kissling, W.D. & Balslev, H. (2011) Geographical ecology of the palms (Arecaceae): determinants of diversity and distributions across spatial scales. Annals of Botany, 108, 1391-1416.
14. Ellenberg, H. (1974) Zeigerwerteder Gefäßpflanzen Mitteleuropas. Scripta Geobotanica, 9, 1-94.
15. Ellenberg, H., Weber, H., Düll, R., Wirth, V., Werner, W. & Paulissen, D. (1991) Zeigerwerte der Pflanzen von Mitteleuropa. Scripta Geobotanica, 18, 1-248.
16. Fanelli, G., Pignatti, S. & Testi, A. (2007) An application case of ecological indicator values (Zeigerwerte) calculated with a simple algorithmic approach. Plant Biosystems, 141, 15-21.
17. Felsenstein, J. (1985) Confidence limits on phylogenesis: an approach using the bootstrap. Evolution, 39, 783-791.
18. Fineschi, S. & Loreto, F. (2012) Leaf volatile isoprenoids: an important defensive armament in forest tree species. iForest, 5, 13-17.
19. Fineschi, S., Loreto, F., Staudt, M. & Penuelas, J. (2013) Diversification of volatile isoprenoid emissions from trees: evolutionary and ecological perspectives. Biology, controls and models of tree volatile organic compound emissions (ed. by U. Niinemets and R.K. Monson), pp. 1-20. Springer, Dordrecht, Germany.
20. Fortunati, A., Barta, C., Brilli, F., Centritto, M., Zimmer, I., Schnitzler, J.P. & Loreto, F. (2008) Isoprene emission is not temperature-dependent during and after severe drought-stress: a physiological and biochemical analysis. Plant Journal, 55, 687-697.
21. Godefroid, S. & Dana, E.D. (2007) Can Ellenberg's indicator values for Mediterranean plants be used outside their region of definition? Journal of Biogeography, 34, 62-68.
22. Greenberg, J.P., Guenther, A.B., Madronich, S., Baugh, W., Ginoux, P., Druilhet, A., Delmas, R. & Delon, C. (1999) Biogenic volatile organic compound emissions in central Africa during the experiments for the regional sources and sinks of oxidants (EXPRESSO) biomass burning season. Journal of Geophysical Research, 104, 30659-30671.
23. Hadfield, J.D. (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software, 33, 1-22.
24. Hanson, D.T., Swanson, S., Graham, L.E. & Sharkey, T.D. (1999) Evolutionary significance of isoprene emission from mosses. America Journal of Botany, 86, 634-639.
25. Harley, P.C., Monson, R.K. & Lerdau, M.T. (1999) Ecological and evolutionary aspects of isoprene emission from plants. Oecologia, 118, 109-123.
26. Harrison, S.P., Morfopoulos, C., Srikanta Dani, K.G., Prentice, I.C., Arneth, A., Atwell, B.J., Barkley, M.P., Leishman, M.R., Loreto, F., Medlyn, B.E., Niinemets, Ü., Possell, M., Peñuelas, J. & Wright, I.J. (2013) Volatile isoprenoid emissions from plastid to planet. New Phytologist, 197, 49-57.
27. Hill, M., Mountford, J., Roy, D. & Bunce, R. (1999) Ellenberg's indicator values for British plants. Institute of Terrestrial Ecology, Huntingdon.
28. Jones, M.L., Hayes, F., Mills, G., Sparks, T.H. & Fuhrer, J. (2007) Predicting community sensitivity to ozone, using Ellenberg indicator values. Environmental Pollution, 146, 744-753.
29. Kerstiens, G. & Possell, M. (2001) Is competence for isoprene emission related to the mode of phloem loading? New Phytologist, 152, 368-372.
30. Kesselmeier, J. & Staudt, M. (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. Journal of Atmospheric Chemistry, 33, 23-88.
31. Klaus, V., Kleinebecker, T., Boch, S., Müller, J., Socher, S.A., Prati, D., Fischer, M. & Hölzel, N. (2012) NIRS meets Ellenberg's indicator values: prediction of moisture and nitrogen values of agricultural grassland vegetation by means of near-infrared spectral characteristics. Ecological Indicators, 14, 82-86.
32. Krecek, J., Novakova, J. & Horicka, Z. (2010) Ellenberg's indicator in water resources control: the Jizera Mountains, Czech Republic. Ecological Engineering, 36, 1112-1117.
33. Llusiá, J., Peñuelas, J., Sardans, J., Owen, S.M. & Niinemets, U. (2010) Measurement of volatile terpene emissions in 70 dominant vascular plant species in Hawaii: aliens emit more than natives. Global Ecology and Biogeography, 19, 863-874.
34. Loreto, F. & Schnitzler, J.P. (2010) Abiotic stresses and induced BVOCs. Trends in Plant Science, 15, 154-166.
35. Loreto, F. & Velikova, V. (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology, 127, 1781-1787.
36. Loreto, F., Ciccioli, P., Brancaleoni, E., Valentini, R., De Lillis, M., Csiky, O. & Seufert, G. (1998) A hypothesis on the evolution of isoprenoid emission by oaks based on the correlation between emission type and Quercus taxonomy. Oecologia, 115, 302-305.
37. Loreto, F., Bagnoli, F. & Fineschi, S. (2009) One species, many terpenes: matching chemical and biological diversity. Trends in Plant Science, 14, 416-420.
38. Médail, F. & Diadema, K. (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. Journal of Biogeography, 36, 1333-1345.
39. Médail, F. & Quézel, P. (1999) Biodiversity hotspots in the Mediterranean basin: setting global conservation priorities. Conservation Biology, 13, 1510-1513.
40. Monson, R.K., Jones, R.T., Rosenstiel, T.N. & Schnitzler, J.P. (2013) Why only some plants emit isoprene. Plant, Cell and Environment, 36, 503-516.
41. Nei, M. & Gojobori, T. (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Molecular Biology and Evolution, 5, 418-426.
42. Niinemets, U., Loreto, F. & Reichstein, M. (2004) Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends in Plant Science, 9, 180-186.
43. Owen, S.M. & Peñuelas, J. (2005) Opportunistic emissions of volatile isoprenoids. Trends in Plant Science, 10, 420-426.
44. Pignatti, S. (1982) Flora d'Italia. Edagricole, Bologna.
45. Pignatti, S., Menegoni, P. & Pietrosanti, S. (2005) Bioindicazione attraverso le piante vascolari. Valori di indicazione secondo Ellenberg (Zeigerwerte) per le specie della Flora d'Italia. Braun-Blanquetia, 39, 1-97.
46. Prinzing, A., Durka, W., Klotz, S. & Brandl, R. (2001) The niche of higher plants: evidence for phylogenetic conservatism. Proceedings of the Royal Society B: Biological Sciences, 268, 2383-2389.
47. Qiu, Q., Ma, T., Hu, Q., Liu, B., Wu, Y., Zhou, H., Wang, Q., Wang, J., Liu, J. & Sederoff, R. (2011) Genome-scale transcriptome analysis of the desert poplar, Populus euphratica. Tree Physiology, 31, 452-461.
48. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
49. Ramsay, H., Rieseberg, L.H. & Ritland, K. (2009) The correlation of evolutionary rate with pathway position in plant terpenoid biosynthesis. Molecular Biology and Evolution, 26, 1045-1053.
50. Schaffers, A. & Sýcora, K. (2000) Reliability of Ellenberg indicator values for moisture, nitrogen and soil reaction: a comparison with field measurements. Journal of Vegetation Science, 11, 225-244.
51. Schmidtlein, S. (2005) Imaging spectroscopy as a tool for mapping Ellenberg indicator values. Journal of Applied Ecology, 42, 966-974.
52. Sharkey, T.D., Yeh, S., Wiberley, A.E., Falbel, T.G., Gong, D. & Fernandez, D.E. (2005) Evolution of the isoprene biosynthetic pathway in kudzu. Plant Physiology, 137, 700-712.
53. Sharkey, T.D., Gray, D.W., Pell, H.K., Breneman, S.R. & Toppers, L. (2013) Isoprene synthase genes form a monophyletic clade of acyclic terpene synthases in the TPS-b terpene synthase family. Evolution, 67, 1026-1040.
54. Silver, G.M. & Fall, R. (1995) Characterization of aspen isoprene synthase, an enzyme responsible for leaf isoprene emission to the atmosphere. Journal of Biological Chemistry, 270, 13010-13016.
55. Silvertown, J., Dodd, M., Gowing, D., Lawson, C. & McConway, K. (2006) Phylogeny and the hierarchical organization of plant diversity. Ecology, 87, S39-S49.
56. Singsaas, E.L., Lerdau, M., Winter, K. & Sharkey, T.D. (1997) Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiology, 115, 1413-1420.
57. Smith, R. & Sytsma, K. (1990) Evolution of Populus nigra (sect. Aigeiros): introgressive hybridization and the chloroplast contribution of Populus alba (sect. Populus). American Journal of Botany, 77, 1176-1187.
58. Stevens, P.F. (2001) onwards. Angiosperm phylogeny website. Version 12, July 2012. Available at www.mobot.org/MOBOT/research/APweb
59. Sullivan, C.A., Skeffington, M.S., Gormally, M.J. & Finn, J.A. (2010) The ecological status of grasslands on lowland farmlands in western Ireland and implications for grassland classification and nature value assessment. Biological Conservation, 143, 1529-1539.
60. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739.
61. Thompson, J. (2005) Plant evolution in the Mediterranean. Oxford University Press, Oxford.
62. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876-4882.
63. Velikova, V., Varkonyi, Z., Szabò, M., Maslenkova, L., Nogues, I., Kovacs, L., Peeva, V., Busheva, M., Garab, G., Sharkey, T.D. & Loreto, F. (2011) Increased thermostability of thylakoid membranes in isoprene-emitting leaves probed with three biophysical techniques. Plant Physiology, 157, 905-916.
64. Vickers, C.E., Gershenzon, J., Lerdau, M.T. & Loreto, F. (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nature Chemical Biology, 5, 283-291.