Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The effect of elevated CO2, soil and atmospheric water deficit and seasonal phenology on leaf and ecosystem isoprene emission

Emiliano Pegoraro A , Mark J. Potosnak B , Russell K. Monson C , Ana Rey A F , Greg Barron-Gafford D and C. Barry Osmond E
+ Author Affiliations
- Author Affiliations

A Department of Desertification and Geoecology, Estación Experimental de Zonas Áridas, CSIC, 04001 Almería, Spain.

B Division of Earth and Ecosystem Sciences, Desert Research Institute, Reno, NV 89512, USA.

C Department of Ecology and Evolutionary Biology, and Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO 80309, USA.

D Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA.

E School of Biochemistry and Molecular Biology, Australian National University, Canberra, ACT 0200, Australia.

F Corresponding author. Email: arey@eeza.csic.es

Functional Plant Biology 34(9) 774-784 https://doi.org/10.1071/FP07021
Submitted: 29 January 2007  Accepted: 18 June 2007   Published: 30 August 2007

Abstract

Two cottonwood plantations were grown at different CO2 concentrations at the Biosphere 2 Laboratory in Arizona to investigate the response of isoprene emission to elevated [CO2] and its interaction with water deficits. We focused on responses due to seasonal variation and variation in the mean climate from one year to the next. In fall and in spring, isoprene emission rate showed a similar inhibition by elevated [CO2], despite an 8–10°C seasonal difference in mean air temperature. The overall response of isoprene emission to drought was also similar for observations conducted during the spring or fall, and during the fall of two different years with an approximate 5°C difference in mean air temperature. In general, leaf-level isoprene emission rates, measured at constant temperature and photon-flux density, decreased slightly, or remained constant during drought, whereas ecosystem-level isoprene emission rates increased. The uncoupling of ecosystem- and leaf-scale responses is not due to differential dependence on leaf area index (LAI) as LAI increased only slightly, or decreased, during the drought treatments at the same time that ecosystem isoprene emission rate increased greatly. Nor does the difference in isoprene emission rate between leaves and ecosystems appear to be due solely to increases in canopy surface temperature during the drought, though some increase in temperature was observed. It is possible that still further factors, such as increased penetration of PPFD into the canopy as a result of changes in leaf angle, reduced sink strength of the soil for atmospheric isoprene, and decreases in the mean Ci of leaves, combined with the small increases in canopy surface temperature, increased the ecosystem isoprene emission rate. Whatever the causes of the differences in the leaf and ecosystem responses, we conclude that the overall shape of the leaf and ecosystem responses to drought was constant irrespective of season or year.

Additional keywords: Biosphere 2, climate, drought, interannual, leaf area index, NEE, photosynthesis, Populus deltoides, soil, temperature.


References


Barron-Gafford G, Martens D, Grieve K, Biel K, Kudeyarov V, McLain JET, Lipson D, Murthy R (2005) Growth of eastern cottonwoods (Populus deltoides) in elevated [CO2] stimulates stand-level respiration and rhizodeposition of carbohydrates, accelerates soil nutrient depletion, yet stimulates above- and belowground biomass production. Global Change Biology 11, 1220–1233.
Crossref | GoogleScholarGoogle Scholar | open url image1

Boissard C, Cao XL, Juan CY, Hewitt CN, Gallagher M (2001) Seasonal variations in VOC emission rates from gorse (Ulex europaeus). Atmospheric Environment 35, 917–927.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brilli F, Barta C, Fortunati A, Lerdau M, Loreto F, Centritto M (2007) Response of isoprene emission and carbon metabolism to drought in white poplar (Populus alba) seedlings. New Phytologist 175, 244–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Centritto M, Nascetti P, Petrilli L, Raschi A, Loreto F (2004) Profiles of isoprene emission and photosynthetic parameters in hybrid poplars exposed to free-air CO2 enrichment. Plant, Cell & Environment 27, 403–412.
Crossref | GoogleScholarGoogle Scholar | open url image1

Crutzen PJ, Zimmermann PH (1991) The changing photochemistry of the troposphere. Tellus 43, 136–151. open url image1

Delwiche CF, Sharkey TD (1993) Rapid appearance of C-13 in biogenic isoprene when (CO2)-C-13 is fed to intact leaves. Plant, Cell & Environment 16, 587–591.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fall RR, Monson RK (1992) Isoprene emission rate and intercellular isoprene concentration as influenced by stomatal distribution and conductance. Plant Physiology 100, 987–992.
PubMed |
open url image1

Fang CW, Monson RK, Cowling EB (1996) Isoprene emission, photosynthesis, and growth in sweetgum (Liquidambar styraciflua) seedlings exposed to short- and long- term drying cycles. Tree Physiology 16, 441–446.
PubMed |
open url image1

Fehsenfeld F, Calvert J, Fall RR, Goldan P, Guenther AB , et al. (1992) Emission of volatile organic compounds from vegetation and the implications for atmospheric chemistry. Global Biogeochemical Cycles 6, 389–430. open url image1

Fuentes JD, Wang D (1999) On the seasonality of isoprene emissions from a mixed temperate forest. Ecological Applications 9, 1118–1131.
Crossref |
open url image1

Fuentes JD, Lerdau M, Atkinson R, Baldocchi D, Bottenheim JW , et al. (2000) Biogenic hydrocarbons in the atmospheric boundary layer: a review. Bulletin of the American Meteorological Society 81, 1537–1575.
Crossref | GoogleScholarGoogle Scholar | open url image1

Funk JL, Jones CG, Gray DW, Throop HL, Hyatt LA, Lerdau MT (2005) Variation in isoprene emission from Quercus rubra: Sources, causes, and consequences for estimating fluxes. Journal of Geophysical Research 110, D04301.
Crossref | GoogleScholarGoogle Scholar | open url image1

Funk JL, Mak JE, Lerdau MT (2004) Stress-induced changes in carbon sources for isoprene production in Populus deltoides. Plant, Cell & Environment 27, 747–755.
Crossref | GoogleScholarGoogle Scholar | open url image1

Guenther AB, Hills AJ (1998) Eddy covariance measurement of isoprene fluxes. Journal of Geophysical Research 103, 13 145–13 152.
Crossref | GoogleScholarGoogle Scholar | open url image1

Guenther AB, Monson RK, Fall RR (1991) Isoprene and monoterpene emission rate variability – observations with Eucalyptus and emission rate algorithm development. Journal of Geophysical Research 96, 10 799–10 808. open url image1

Guenther AB, Zimmerman PR, Harley PC, Monson RK, Fall R (1993) Isoprene and monoterpene emission rate variability – model evaluations and sensitivity analyses. Journal of Geophysical Research 98, 12 609–12 617. open url image1

Guenther AB, Archer S, Greenberg JP, Harley PC, Helmig D, Klinger L, Vierling L, Wildermuth M, Zimmerman P, Zitzer S (1999) Biogenic hydrocarbon emissions and landcover/climate change in a subtropical savanna. Physics and Chemistry of the Earth. Part B: Hydrology Oceans and Atmosphere 24, 659–667.
Crossref | GoogleScholarGoogle Scholar | open url image1

Harley PC, Guenther AB, Zimmerman P (1996) Effects of light, temperature and canopy position on net photosynthesis and isoprene emission from sweetgum (Liquidambar styraciflua) leaves. Tree Physiology 16, 25–32.
PubMed |
open url image1

Harley PC, Monson RK, Lerdau MT (1999) Ecological and evolutionary aspects of isoprene emission from plants. Oecologia 118, 109–123.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hayward S, Hewitt CN, Sartin JH, Owen SM (2002) Performance characteristics and applications of a proton transfer reaction-mass spectrometer for measuring volatile organic compounds in ambient air. Environmental Science & Technology 36, 1554–1560.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Karl T, Fall R, Rosenstiel TN, Prazeller P, Larsen B, Seufert G, Lindinger W (2002) On-line analysis of the (CO2)-C-13 labeling of leaf isoprene suggests multiple subcellular origins of isoprene precursors. Planta 215, 894–905.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kreuzwieser J, Graus M, Wisthaler A, Hanse A, Rennenberg H, Schnitzler JP (2002) Xylem-transported glucose as an additional carbon source for leaf isoprene formation in Quercus robur. New Phytologist 156, 171–178.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kuhn U, Rottenberger S, Biesenthal T, Wolf A, Schebeske G, Ciccioli P, Brancaleoni E, Frattoni M, Tavares TM, Kesselmeier J (2004) Seasonal differences in isoprene and light-dependent monoterpene emission by Amazonian tree species. Global Change Biology 10, 663–682.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lerdau M, Gray D (2003) Ecology and evolution of light-dependent and light-independent phytogenic volatile organic carbon. New Phytologist 157, 199–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lichtenthaler HK (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annual Review of Plant Physiology and Plant Molecular Biology 50, 47–65.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lindinger W, Hansel A, Jordan A (1998) Proton-transfer-reaction mass spectrometry (PTR–MS): on-line monitoring of volatile organic compounds at pptv levels. Chemical Society Reviews 27, 347–354.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loreto F, Sharkey TD (1990) A gas exchange study of photosynthesis and isoprene emission in Quercus rubra L. Planta 182, 523–531.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Monson RK (2002) Volatile organic compound emissions from terrestrial ecosystems: a primary biological control over atmospheric chemistry. Israel Journal of Chemistry 42, 29–42.
Crossref | GoogleScholarGoogle Scholar | open url image1

Monson RK, Fall RR (1989) Isoprene emission from aspen leaves – influence of environment and relation to photosynthesis and photorespiration. Plant Physiology 90, 267–274.
PubMed |
open url image1

Monson RK, Holland EA (2001) Biospheric trace gas fluxes and their control over tropospheric chemistry. Annual Review of Ecology and Systematics 32, 547–560.
Crossref | GoogleScholarGoogle Scholar | open url image1

Monson RK, Jaeger CH, Adams WW, Driggers EM, Silver GM, Fall R (1992) Relationships among isoprene emission rate, photosynthesis and isoprene synthase activity as influenced by temperature. Plant Physiology 98, 1175–1180.
PubMed |
open url image1

Monson RK, Harley PC, Litvak ME, Wildermuth M, Guenther AB, Zimmerman PR, Fall RR (1994) Environmental and developmental controls over the seasonal pattern of isoprene emission from aspen leaves. Oecologia 99, 260–270.
Crossref | GoogleScholarGoogle Scholar | open url image1

Monson RK, Lerdau MT, Sharkey TD, Schimel DS, Fall R (1995) Biological aspects of constructing volatile organic compound emission inventories. Atmospheric Environment 29, 2989–3002.
Crossref | GoogleScholarGoogle Scholar | open url image1

Monson RK, Trahan N, Rosenstiel TN, Veres P, Moore D , et al. (2007) Isoprene emission from terrestrial ecosystems in response to global change: minding the gap between models and observations. Philosophical Transactions Series A: Mathematical, Physical and Engineering Sciences (In press). , open url image1

Murthy R, Barron-Gafford G, Dougherty PM, Engel VC, Grieve K, Handley L, Klimas C, Potosnak MJ, Zarnoch SJ, Zhang RY (2005) Leaf area index dominates carbon flux response to elevated CO2 in stands Populus deltoides (Bartr.). Global Change Biology 11, 716–731.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets U, Reichstein M (2003) Controls on the emission of plant volatiles through stomata: eifferential sensitivity of emission rates to stomatal closure explained. Journal of Geophysical Research 108, 4208.
Crossref | GoogleScholarGoogle Scholar | open url image1

Osmond B, Ananyev G, Berry JA, Langdon C, Kolber Z , et al. (2004) Changing the way we think about global change research: scaling up in experimental ecosystem science. Global Change Biology 10, 393–407.
Crossref | GoogleScholarGoogle Scholar | open url image1

Owen SM, Peñuelas J (2005) Opportunistic emissions of volatile isoprenoids. Trends in Plant Science 10, 420–426.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pegoraro E, Rey A, Bobich EG, Barron-Gafford G, Grieve KA, Malhi Y, Murthy R (2004a) Effect of elevated CO2 concentration and vapour pressure deficit on isoprene emission from leaves of Populus deltoides during drought. Functional Plant Biology 31, 1137–1147.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pegoraro E, Rey A, Greenberg J, Harley P, Grace J, Malhi Y, Guenther A (2004b) Effect of drought on isoprene emission rates from leaves of Quercus virginiana Mill. Atmospheric Environment 38, 6149–6156.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pegoraro E, Abrell L, Van Haren J, Barron-Gafford G, Grieve KA, Malhi Y, Murthy R, Lin GH (2005a) The effect of elevated atmospheric CO2 and drought on sources and sinks of isoprene in a temperate and tropical rainforest mesocosm. Global Change Biology 11, 1234–1246.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pegoraro E, Rey A, Barron-Gafford G, Monson R, Malhi Y, Murthy R (2005b) The interacting effects of elevated atmospheric CO2 concentration, drought and leaf-to-air vapour pressure deficit on ecosystem isoprene fluxes. Oecologia 146, 120–129.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pegoraro E, Rey A, Abrell L, Van Haren J, Lin GH (2006) Drought effect on isoprene production and consumption in Biosphere 2 tropical rainforest. Global Change Biology 12, 456–469.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rapparini F, Baraldi R, Miglietta F, Loreto F (2004) Isoprenoid emission in trees of Quercus pubescens and Quercus ilex with lifetime exposure to naturally high CO2 environment. Plant, Cell & Environment 27, 381–391.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rey A, Jarvis PG (1998) Long-term photosynthetic acclimation to increased atmospheric CO2 concentration in young birch (Betula pendula) trees. Tree Physiology 18, 441–450.
PubMed |
open url image1

Rosenstiel TN, Potosnak MJ, Griffin KL, Fall R, Monson RK (2003) Increased CO2 uncouples growth from isoprene emission in an agriforest ecosystem. Nature 421, 256–259.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rosenstiel TN, Ebbets AL, Khatri WC, Fall R, Monson RK (2004) Induction of poplar leaf nitrate reductase: a test of extrachloroplastic control of isoprene emission rate. Plant Biology 6, 12–21.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schnitzler JP, Lehning A, Steinbrecher R (1997) Seasonal pattern of isoprene synthase activity in Quercus robur leaves and its significance for modeling isoprene emission rates. Botanica Acta 110, 240–243. open url image1

Schnitzler JP, Graus M, Kreuzwieser J, Heizmann U, Rennenberg H, Wisthaler A, Hansel A (2004) Contribution of different carbon sources to isoprene biosynthesis in poplar leaves. Plant Physiology 135, 152–160.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Scholefield PA, Doick KJ, Herbert BMJ, Hewitt CNS, Schnitzler JP, Pinelli P, Loreto F (2004) Impact of rising CO2 on emissions of volatile organic compounds: isoprene emission from Phragmites australis growing at elevated CO2 in a natural carbon dioxide spring. Plant, Cell & Environment 27, 393–401.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sharkey TD, Loreto F (1993) Water-stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves. Oecologia 95, 328–333.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sharkey TD, Yeh SS (2001) Isoprene emission from plants. Annual Review of Plant Physiology and Plant Molecular Biology 52, 407–436.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sharkey TD, Loreto F, Delwiche CF (1991) High-carbon dioxide and sun shade effects on isoprene emission from oak and aspen tree leaves. Plant, Cell & Environment 14, 333–338.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sharkey TD, Singsaas EL, Lerdau MT, Geron CD (1999) Weather effects on isoprene emission capacity and applications in emissions algorithms. Ecological Applications 9, 1132–1137.
Crossref |
open url image1

Sharkey TD, Chen XY, Yeh S (2001) Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiology 125, 2001–2006.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Silver GM, Fall RR (1991) Enzymatic-synthesis of isoprene from dimethylallyl diphosphate in aspen leaf extracts. Plant Physiology 97, 1588–1591.
PubMed |
open url image1

Singsaas EL, Sharkey TD (2000) The effects of high temperature on isoprene synthesis in oak leaves. Plant, Cell & Environment 23, 751–757.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tingey DT, Evans RC, Gumpertz ML (1981) Effects of environmental conditions on isoprene emission from live oak. Planta 152, 565–570.
Crossref | GoogleScholarGoogle Scholar | open url image1

Torbert HA, Johnson HB (2001) Soil of the intensive agriculture biome of Biosphere 2. Journal of Soil and Water Conservation 56, 4–11. open url image1

Walter A, Lambrecht SC (2004) Biosphere 2 center as a unique tool for environmental studies. Journal of Environmental Monitoring 6, 267–277.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Warneke C, Holzinger R, Hansel A, Jordan A, Lindinger W , et al. (2001) Isoprene and its oxidation products methyl vinyl ketone, methacrolein, and isoprene related peroxides measured online over the tropical rain forest of Surinam in March 1998. Journal of Atmospheric Chemistry 38, 167–185.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wiberley AE, Linskey AR, Falbel TG, Sharkey TD (2005) Development of the capacity for isoprene emission in kudzu. Plant, Cell & Environment 28, 898–905.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wildermuth MC, Fall RR (1996) Light-dependent isoprene emission – characterization of a thylakoid-bound isoprene synthase in Salix discolor chloroplasts. Plant Physiology 112, 171–182.
PubMed |
open url image1









* *Emiliano Pegoraro passed away on 22 April 2007, marking the premature end to a productive and influential scientific career. Emiliano was a friend to many in the isoprene emission research community. His seminal studies on the patterns and mechanisms underlying the responses of leaf and canopy isoprene emissions to drought, temperature and atmospheric CO2 concentration should stand for a long time as exemplars for how to experimentally dissect the mechanisms underlying complex physiological processes. Emiliano’s infectious love for life and science will be remembered and missed by his wife Ana, his family and many friends.