Vertical canopy gradient in photosynthesis and monoterpenoid emissions: An insight into the chemistry and physiology behind

Atmospheric Environment

Volumn 80, Issue , 2013, Pages 85-95

  Simpraga M ^a   Verbeeck, H ^a   Bloemen, J ^a   Vanhaecke, L ^a   Demarcke, M ^b   Joo E ^a   Pokorska, O ^a   Amelynck, C ^b   Schoon, N ^b   Dewulf, J ^a   Van Langenhove, H ^a   Heinesch, B ^c   Aubinet, M ^c   Steppe, K ^a  

^a GHENT UNIVERSITY   (Belgium)

^b BELGIAN INSTITUTE FOR SPACE AERONOMY   (Belgium)

^c UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Beech; Carotenoids; Monoterpenoids; Photosynthesis; Sun and shade leaves; Vertical canopy gradient; Volatiles

Indexed keywords

BEECH; BIOGENIC VOLATILE ORGANIC COMPOUNDS; CAROTENOIDS; DYNAMIC BRANCH ENCLOSURE SYSTEMS; MONOTERPENOIDS; PHYSIOLOGICAL STATUS; SPECIFIC LEAF AREA; VOLATILES;

FORESTRY; PHYSIOLOGY; PIGMENTS; UNSATURATED COMPOUNDS;

PHOTOSYNTHESIS;

CAROTENOID; CHLOROPHYLL A; ISOPRENOID; NITROGEN; PIGMENT; TERPENOID;

ADULT; ALGORITHM; CARBON EMISSION; FOREST ECOSYSTEM; LEAF; PHOTOSYNTHESIS; TERPENE; TREE; VOLATILE ORGANIC COMPOUND;

AIR TEMPERATURE; ARTICLE; BEECH; CANOPY; CHLOROPHYLL CONTENT; CIRCADIAN RHYTHM; CLIMATE; EXHAUST GAS; GAS EXCHANGE; GROWING SEASON; HUMIDITY; LEAF AREA; MICROCLIMATE; NONHUMAN; PHOTOSYNTHESIS; PLANT HEIGHT; PLANT LEAF; PRIORITY JOURNAL; SUN EXPOSURE; TEMPERATE DECIDUOUS FOREST;

CAROTENOIDS; FAGUS; FORESTRY; PHOTOSYNTHESIS; PHYSIOLOGY; PIGMENT;

EUROPE;

EID: 84883040518     PISSN: 13522310     EISSN: 18732844     Source Type: Journal    
DOI: 10.1016/j.atmosenv.2013.07.047     Document Type: Article

References (81)

1. Adriaenssens S., Hansen K., Staelens J., Wuyts K., De Schrijver A., Lander Baeten L., Boeckx P., Samson R., Verheyen K. Throughfall deposition and canopy exchange processes along a vertical gradient within the canopy of beech (Fagus sylvatica L.) and Norway spruce (Picea abies (L.) Karst). Science of the Total Environment 2012, 420:168-182.
2. Aranda I., Pardo F., Gil L., Pardos J.A. Anatomical basis of the change in leaf mass per area and nitrogen investment with relative irradiance within the canopy of eight temperate tree species. Acta Oecologica 2004, 25:187-195.
3. Boardmann N.K. Comparative photosynthesis of sun and shade plants. Annual Reviews Plant Physiology 1977, 28:355-377.
4. Bruce T.J.A., Pickett J.A. Perception of plant volatile blends by herbivorous insects-finding the right mix. Phytochemistry 2011, 72:1605-1611.
5. Bussotti F., Borghini F., Celesti C., Leonzio C., Bruschi P. Leaf morphology and macronutrients in broadleaved trees in central Italy. Trees 2000, 14:361-368.
6. Casella E., Ceulemans R. Spatial distribution of leaf morphological and physiological characteristics in relation to local radiation regime within the canopies of 3-year-old Populus clones in coppice culture. Tree Physiology 2002, 22:1277-1288.
7. Čater M., Simončič P. Photosynthetic response of young beech (Fagus sylvaticaL.) on research plots in different light conditions. Sumarski List 2009, 11:569-576.
8. Closa I., Irigoyen J.J., Goicoechea N. Microclimatic conditions determined by stem density influence leaf anatomy and leaf physiology of beech (Fagus sylvatica L.) growing within stands that naturally regenerate from clear-cuttings. Trees Structure and Function 2010, 24:1029-1043.
9. Copolovici L., Kännaste A., Remmel T., Vislap V., Niinemets Ü. Volatile emissions from Alnus glutionosa induced by herbivory are quantitatively related to the extent of damage. Journal of Chemical Ecology 2011, 37:18-28.
10. Croteau R. Biosynthesis and catabolism of monoterpenoids. Chemical Reviews 1987, 87:929-954.
11. Dindorf T., Kuhn U., Ganzeveld L., Schebeske G., Ciccioli P., Holzke C., Koeble R., Seufert G., Kesselmeier J. Significant light and temperature dependent monoterpene emissions from European beech (Fagus sylvatica L.) and their potential impact on the European volatile organic compound budget. Journal of Geophysical Research-Atmosphere 2006, 111. 10.1029/2005JD006751.
12. Dudareva N., Negre F., Nagegowda D.A., Orlova I. Plant volatiles: recent advances and future perspectives. Critical Reviews Plant Science 2006, 25:417-440.
13. Eisenreich W., Bacher A., Arugoni D., Rohdich F. Biosynthesis of isoprenoids via the non-mevalonate pathway. Cellullar Molecular Life Science 2004, 61:1401-1426.
14. Ellsworth D.S., Reich P.B. Canopy structure and vertical patterns of photosynthesis and related leaf traits in a deciduous forest. Oecologia 1993, 96:169-178.
15. Eriksson H., Eklundh L., Hall K., Lindroth A. Estimating LAI in deciduous forest stands. Agricultural and Forest Meteorology 2005, 129:27-37.
16. Frak E., Le Roux X., Millard P., Adam B., Dreyer E., Escuit C., Sinoquet H., Vandame M., Varlet-Grancher C. Spatial distribution of leaf nitrogen and photosynthetic capacity within the foliage of individual trees: disentangling the effects of local light quality, leaf irradiance, and transpiration. Journal of Experimental Botany 2002, 53:2207-2216.
17. Franklin A.N. Shade avoidance. New Phytologist 2008, 179:930-944.
18. Fuentes J.D., Wang D., Neumann H.H., Gillespie T.J., Hartog G., Dann T.F. Ambient biogenic hydrocarbons and isoprene emissions from a mixed deciduous forest. Journal of Atmospheric Chemistry 1996, 25:67-95.
19. 2 labelling and PTR-MS analysis. Plant, Cell & Environment 2010, 33:781-792.
20. Gielen B., Low M., Deckmyn G., Metzger U., Franck F., Heerdt C., Matyssek R., Valcke R., Cuelemans R. Chronic ozone exposure affects leaf senescence of adult beech trees: a chlorophyll fluorescence approach. Journal of Experimental Botany 2007, 58:785-792.
21. Goldstein I., Andrade J.L., Meinzer F.C., Holbrook N.M., Cavelier J., Jackson P., Celis A. Stem water storage and diurnal patterns of water use in forest canopy trees. Plant, Cell & Environment 1998, 21:193-200.
22. 2 partial pressures for 5 years. Functional Ecology 2001, 15:497-505.
23. Grossoni P., Bussotti F., Tani E., Gravano S., Santarelli S., Bottacci A. Morpho-anatomical alterations in leaves of Fagus sylvatica L. and Quercus ilex L. in different environmental stress conditions. Chemosphere 1998, 36:919-924.
24. Hansen U., Fiedler B., Rank B. Variation of pigment composition and antioxidative systems along the canopy light gradient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance. Trees 2002, 16:354-364.
25. Harley P., Guenther A., Zimmerman P. Effects of light, temperature and canopy position on net photosynthesis and isoprene emission from sweetgum (Liquidambar styraciflua) leaves. Tree Physiology 1996, 16:25-32.
26. Holopainen J.K., Gershenzon J. Multiple stress factors and the emission of plant VOCs. Trends in Plant Science 2010, 15:176-184.
27. Holzke C., Dindorf T., Kesselmeier J., Kuhn U., Koppmann R. Terpene emissions from European beech (Fagus sylvatica L.): pattern and emission behaviour over two vegetation periods. Journal of Atmospheric Chemistry 2006, 55:81-102.
28. Hothorn T., Bretz F., Westfall P. Simultaneous inference in general parametric models. Biometrical Journal 2008, 50:346-363.
29. IPCC Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change 2007, 996. Cambridge University Press, Cambridge, UK. S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, H.L. Miller (Eds.).
30. Johne A., Weissbecker B., Schütz S. Volatile emissions from Aesculus hippocastanum induced by mining of larval stages of Cameraria ohridella influence oviposition by conspecific females. Journal of Chemical Ecology 2006, 32:2303-2319.
31. Joó E., Van Langenhove H., Šimpraga M., Steppe K., Amelynck C., Schoon N., Müller J.-F., Dewulf J. Variation in biogenic volatile organic compound emission pattern of Fagus sylvatica L. due to aphid infection. Atmospheric Environment 2010, 44:227-234.
32. Joó E., Dewulf J., Demarcke M., Amelynck C., Schoon N., Müller J.-F., Šimpraga M., Steppe K., Van Langenhove H. Quantification of interferences in PTR-MS measurements of monoterpene emissions from Fagus sylvatica L. using simultaneous TD-GC-MS measurements. Journal of Mass Spectrometry 2010, 291:90-95.
33. Kesselmeier J., Staudt M. Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. Journal of Atmospheric Chemistry 1999, 33:23-88.
34. Kim G.T., Yano S., Kozuka T., Tsukaya H. Photomorphogenesis of leaves: shade avoidance and differentiation of sun and shade leaves. Photochemical Photobiology Science 2005, 4:770-774.
35. Kozlowski T.T., Pallardy S.G. Physiology of Woody Plants 1997, 411. Academic Press, London.
36. Lamb B., Thomas P., Baldocchi D., Allwine E., Dilts S., Westberg H., Geron C., Guenther A., Lee K., Harley P., Zimmerman P. Evaluation of forest canopy models for estimating isoprene emissions. Journal of Geophysical Research 1996, 101:22787-22798.
37. Lambers H., Chapin F.S., Pons T.L. Plant Physiological Ecology 1998, 540. Springer, USA.
38. Larcher W. Physiological Plant Ecology 2003, 513. Springer. fourth ed.
39. Le Goff N., Granier A., Ottorinni J.M., Peiffer M. Biomass increment and carbon balance of ash (Fraxinus excelsior) trees in an experimental stand in northeastern France. Annals of Forest Science 2004, 61:577-588.
40. Lenk S., Buschmann C. Distribution of UV-shielding oft he epidermis of sun and shade leaves of the beech (Fagus sylvatica L.) as monitored by multi-color flourescence imaging. Journal of Plant Physiology 1997, 163:1273-1283.
41. Lenz R., Selige T., Seufert G. Scaling up the biogenic emissions from test sites at Castelporziano. Atmospheric Environment 1997, 31:239-250.
42. Lichtenthaler H.K. Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. Photosynthetic Research 2007, 92:163-179.
43. Lichtenthaler H.K. Biosynthesis and accumulation of isoprenoid carotenoids and chlorophylls and emission of isoprene by leaf chloroplasts. Bulletin of the Georgian National Academy of Science 2009, 3:81-94.
44. Lichtenthaler H.K., Rohmer M., Schwender J. Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plant. Physiologia Plantarum 1997, 101:643-652.
45. Lin C.H., Chen B.H. Determination of carotenoids in tomato juice by liquid chromatography. Journal of Chromatography 2003, 1012:103-109.
46. Lindinger W., Hansel A., Jordan A. Proton-transfer-reaction mass spectrometry (PTR-MS): on-line monitoring of volatile organic compounds at pptv levels. Chemical Society Reviews 1998, 27:347-354.
47. Lombardini L., Restrepo-Diaz H., Volder A. Photosynthetic light response and epidermal characteristics of sun and shade pecan leaves. Journal of American Society of Horticulture 2009, 134:372-378.
48. Mann R.S., Ali J.G., Hermann L.S., Tiwari S., Pelz-Stelinski K.S., Alborn H.T., Stelinski L.L. Induced release of a plant-defense volatile 'deceptively' attracts insect vectors to plants infected with a bacterial pathogen. PLoS Pathogens 2012, 8:e1002610.
49. Marshall J.D., Monserud R.A. Foliage height influences specific leaf area of three conifer species. Canadian Journal of Forest Research 2003, 33:164-170.
50. Medlyn B.E., Dreyer E., Ellsworth D., Forstreuter M., Harley P.C., Kirschbaum M.U.F., Le Roux X., Montpied P., Strassemeyer J., Walcroft A., Wang K., Loustau D. Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment 2002, 25:1167-1179.
51. Meir P., Kruijt B., Broadmeadow M., Barbosa E., Kull O., Carswell F., Nobre A., Jarvis P.G. Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area. Plant, Cell & Environment 2002, 25:343-357.
52. 2 response of leaf isoprene emission: an alternative view of Sanadze's double carboxylation scheme. Bulletin of the Georgian National Academy of Science 2009, 3:95-105.
53. 2 across a beech (Fagus sylvatica L.) canopy. Journal of Experimental Botany 2009, 80:2407-2418.
54. Morecroft M.D., Roberts J.M. Photosynthesis and stomatal conductance of mature canopy oak (Quercus robur) and sycamore (Acer pseudoplatanus) trees throughout the growing season. Functional Ecology 1999, 13:332-342.
55. Niinemets Ü., Hauff K., Bertin N., Tenhunen J.D., Steinbrecher R., Seufert G. Monoterpene emissions in relation to foliar photosynthetic and structural variables in Mediterranean evergreen Quercus species. New Phytologist 2002, 153:243-256.
56. Niinemets Ü., Loreto F., Reichstein M. Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends in Plant Science 2004, 9:180-186.
57. Niinemets Ü., Arneth A., Kuhn U., Monson R.K., Peñuelas J., Staudt M. The emission factor of volatile isoprenoids: stress, acclimation, and developmental responses. Biogeosciences 2010, 7:2203-2223.
58. Niinemets Ü., Copolovici L., Hüve K. High within-canopy variation in isoprene emission potentials in temperate trees: implications for predicting canopy-scale isoprene fluxes. Journal of Geophysical Research 2010, 115:G04029.
59. Noe S.M., Hüe K., Niinemets Ü., Copolovici L. Seasonal variation in vertical volatile compounds air concentrations within a remote hemiboreal mixed forest. Journal of Atmospheric Chemistry and Physics 2012, 12:3909-3926.
60. Owen S.M., Peñuelas J. Opportunistic emissions of volatile isoprenoids. Trends in Plant Science 2005, 10:420-426.
61. Petritan A.M., Von Lupke B., Petritan I.C. Acomparative analysis of foliar composition and leaf construction costs of beech (Fagus sylvatica L.), sycamore maple (Acer pseudoplatanus L.) and ash (Fraxunus excelsior L.) saplings along a light gradient. Annals of Forest Science 2010, 67:610-617.
62. Pinheiro J., Bates D., DebRoy S., Sarkar D., R Core team Nlme: Linear and Nonlinear Mixed Effects Models 2009, 1-96. R Package Version 3.
63. Priestley I. The Discovery of Oxygen: Experiments by Joseph Priestley, 1775 (1912) 1775, Kessinger Publishing, 2007.
64. Rasulov B., Hüve K., Valbe M., Laisk A., Niinemets Ü. Evidence that light, carbon dioxide, and oxygen dependencies of leaf isoprene emission are driven by energy status in hybrid aspen. Plant Physiology 2009, 151:448-460.
65. Rasulov B., Hüve K., Bichele I., Laisk A., Niinemets Ü. Temperature response of isoprene emission invivo reflects a combined effect of substrate limitations and isoprene synthase activity: a kinetic analysis. Plant Physiology 2010, 154:1558-1570.
66. Rosenstiel T.N., Fisher A.J., Fall R., Monson R.K. Differential accumulation of dimethylallyl diphosphate in leaves and needles of isoprene- and methylbutenol-emitting and nonemitting species. Plant Physiology 2002, 129:1276-1284.
67. Sanadze G.A. Biogenic isoprene (a review). Russian Journal of Plant Physiology 2004, 51:729-741.
68. Sarijeva G., Knapp M., Lichtenthaler H.K. Differences in photosynthetic activity, chlorophyll and carotenoid levels, and in chlorophyll fluorescence parameters in green sun and shade leaves of Ginkgo and Fagus. Journal of Plant Physiology 2007, 164:950-955.
69. Schuh G., Heiden A.C., Hoffmann T., Kahl J., Rockel P., Rudolph J., Wildt J. Emissions of volatile organic compounds from sunflower and beech: dependence on temperature and light intensity. Journal of Atmospheric Chemistry 1997, 27:291-318.
70. Shah J. Plants under attack: systemic signals in defense. Current Opinion in Plant Biology 2009, 12:459-464.
71. Sharkey T.D., Wiberley A.E., Donohue A.R. Isoprene emission from plants: why and how. Annals of Botany 2008, 101:5-18.
72. Šimpraga M., Verbeeck H., Demarcke M., Joo E., Amelynck C., Schoon N., Dewulf J., Van Langenhove H., Heinsch B., Aubinet M., Müller J.-F., Steppe K. Comparing monoterpenoid emissions and net photosynthesis of beech (Fagus sylvatica L.) in controlled and natural conditions. Atmospheric Environment 2011, 45:2922-2928.
73. Steppe K., Niinemets Ü., Teskey R.O. Tree size- and age-related changes in leaf physiology and their influence on carbon gain. Size- and Age-related Changes in Tree Structure and Function 2011, 235-253. Springer, Dordrecht. F.C. Meinzer, T. Dawson, B. Lachenbruch (Eds.).
74. Taiz L., Zeiger E. Plant Physiology 2010, 648. Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts, MA, USA. fifth ed.
75. 2 diffusion. Journal of Experimental Botany 2006, 57:343-354.
76. Uemura A., Ishida A., Nakano T., Terashima I., Tanabe H., Matsumoto Y. Acclimation of leaf characteristics of Fagus species to previous-year and current-year solar irradiances. Tree Physiology 2000, 20:945-951.
77. Valladares F., Aranda J.M., Balaguer L., Dizengremel P., Manrique E., Dreyer E. The greater seedling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. Trees 2002, 16:395-403.
78. Van Wittenberghe S., Adriaenssens S., Staelens J., Verheyen K., Samson R. Morphological and physiological leaf characteristics of young and adult European beech along a vertical canopy gradient. Trees Structure and Function 2012, 10.1007/S00468-012-0714-7.
79. Vande Walle I. Carbon Sequestration in Short-rotation Forestry Plantations and in Belgian Forest Ecosystems 2007, 244. (PhD dissertation), Ghent University.
80. Varinderpal-Singh B.S., Yadvinder-Singh Thind H.S., Gupta R.K. Need based nitrogen management using the chlorophyll meter and leaf colour chart in rice and wheat in South Asia: a review. Nutrient Cycling in Agroecosystems 2010, 88:361-380.
81. Vile D., Garnier E., Shipley B., Laurent G., Navas M.L., Roumet C., Lavouret S., Diaz S., Hodgson J.H., Lloret F., Midgley F., Poorter H., Rutherford M.C., Wilson P.J., Wright I.J. Specific leaf area and dry matter content estimate thickness in laminar leaves. Annals of Botany 2005, 10.1093/aob/mci264.