A unifying conceptual model for the environmental responses of isoprene emissions from plants

Background and Aims Isoprene is the most important volatile organic compound emitted by land plants in terms of abundance and environmental effects. Controls on isoprene emission rates include light, temperature, water supply and CO2 concentration. A need to quantify these controls has long been recognized. There are already models that give realistic results, but they are complex, highly empirical and require separate responses to different drivers. This study sets out to find a simpler, unifying principle. Methods A simple model is presented based on the idea of balancing demands for reducing power (derived from photosynthetic electron transport) in primary metabolism versus the secondary pathway that leads to the synthesis of isoprene. This model's ability to account for key features in a variety of experimental data sets is assessed. Key results The model simultaneously predicts the fundamental responses observed in short-term experiments, namely: (1) the decoupling between carbon assimilation and isoprene emission; (2) a continued increase in isoprene emission with photosynthetically active radiation (PAR) at high PAR, after carbon assimilation has saturated; (3) a maximum of isoprene emission at low internal CO2 concentration (ci) and an asymptotic decline thereafter with increasing ci; (4) maintenance of high isoprene emissions when carbon assimilation is restricted by drought; and (5) a temperature optimum higher than that of photosynthesis, but lower than that of isoprene synthase activity. Conclusions A simple model was used to test the hypothesis that reducing power available to the synthesis pathway for isoprene varies according to the extent to which the needs of carbon assimilation are satisfied. Despite its simplicity the model explains much in terms of the observed response of isoprene to external drivers as well as the observed decoupling between carbon assimilation and isoprene emission. The concept has the potential to improve global-scale modelling of vegetation isoprene emission.

[1]  T. Sharkey,et al.  Metabolic profiling of the methylerythritol phosphate pathway reveals the source of post-illumination isoprene burst from leaves. , 2013, Plant, cell & environment.

[2]  A. Arneth,et al.  Volatile isoprenoid emissions from plastid to planet. , 2013, The New phytologist.

[3]  C. Jones,et al.  Sensitivity of biogenic isoprene emissions to past, present, and future environmental conditions and implications for atmospheric chemistry , 2012 .

[4]  Ü. Niinemets,et al.  Enhanced isoprene emission capacity and altered light responsiveness in aspen grown under elevated atmospheric CO2 concentration , 2012 .

[5]  P. Shepson,et al.  In-canopy gas-phase chemistry during CABINEX 2009: Sensitivity of a 1-D canopy model to vertical mixing and isoprene chemistry , 2012 .

[6]  M. Saunois,et al.  The formaldehyde budget as seen by a global-scale multi-constraint and multi-species inversion system , 2012 .

[7]  R. Monson,et al.  Modeling the isoprene emission rate from leaves. , 2012, The New phytologist.

[8]  Ü. Niinemets,et al.  Circadian control of global isoprene emissions , 2012 .

[9]  R. B. Jackson,et al.  Contribution of Various Carbon Sources Toward Isoprene Biosynthesis in Poplar Leaves Mediated by Altered Atmospheric CO2 Concentrations , 2012, PloS one.

[10]  T. Sharkey,et al.  Stabilization of thylakoid membranes in isoprene-emitting plants reduces formation of reactive oxygen species , 2012, Plant signaling & behavior.

[11]  C. N. Hewitt,et al.  Ground-level ozone influenced by circadian control of isoprene emissions , 2011 .

[12]  C. N. Hewitt,et al.  Global terrestrial isoprene emission models: Sensitivity to variability in climate and vegetation , 2011 .

[13]  T. Sharkey,et al.  Increased Thermostability of Thylakoid Membranes in Isoprene-Emitting Leaves Probed with Three Biophysical Techniques1[W][OA] , 2011, Plant Physiology.

[14]  A. Borg-Karlson,et al.  Atmospheric chemistry in stereo: A new look at secondary organic aerosols from isoprene , 2011 .

[15]  Ü. Niinemets,et al.  Induction of a Longer Term Component of Isoprene Release in Darkened Aspen Leaves: Origin and Regulation under Different Environmental Conditions1 , 2011, Plant Physiology.

[16]  C. N. Hewitt,et al.  Isoprene emissions from plants are mediated by atmospheric CO2 concentrations , 2011 .

[17]  T. Keenan,et al.  Overlooking the canopy: The importance of canopy structure in scaling isoprenoid emissions from the leaf to the landscape , 2011 .

[18]  P. Friedlingstein,et al.  Late Holocene methane rise caused by orbitally controlled increase in tropical sources , 2011, Nature.

[19]  R. Peterson,et al.  The rate of nitrite reduction in leaves as indicated by O2 and CO2 exchange during photosynthesis , 2011, Journal of experimental botany.

[20]  O. Boucher,et al.  How vegetation impacts affect climate metrics for ozone precursors , 2010 .

[21]  Ü. Niinemets,et al.  High within‐canopy variation in isoprene emission potentials in temperate trees: Implications for predicting canopy‐scale isoprene fluxes , 2010 .

[22]  J. W. Munger,et al.  Emissions of isoprenoids and oxygenated biogenic volatile organic compounds from a New England mixed forest , 2010 .

[23]  A. Arneth,et al.  Evaluation of a photosynthesis-based biogenic isoprene emission scheme in JULES and simulation of isoprene emissions under present-day climate conditions , 2010 .

[24]  Ü. Niinemets,et al.  Temperature Response of Isoprene Emission in Vivo Reflects a Combined Effect of Substrate Limitations and Isoprene Synthase Activity: A Kinetic Analysis1 , 2010, Plant Physiology.

[25]  P. Mullineaux,et al.  Genetic structure and regulation of isoprene synthase in Poplar (Populus spp.) , 2010, Plant Molecular Biology.

[26]  U. Niinemets.  Mild versus severe stress and BVOCs: thresholds, priming and consequences. , 2010, Trends in plant science.

[27]  C. N. Hewitt,et al.  Sensitivity of isoprene emissions from the terrestrial biosphere to 20th century changes in atmospheric CO2 concentration, climate, and land use , 2010 .

[28]  Stephen Sitch,et al.  Isoprene emissions and climate , 2009 .

[29]  R. Pike,et al.  How plants can influence tropospheric chemistry: the role of isoprene emissions from the biosphere , 2009 .

[30]  Christine Wiedinmyer,et al.  A review of Secondary Organic Aerosol (SOA) formation from isoprene , 2009 .

[31]  A. Laisk,et al.  Evidence That Light, Carbon Dioxide, and Oxygen Dependencies of Leaf Isoprene Emission Are Driven by Energy Status in Hybrid Aspen1 , 2009, Plant Physiology.

[32]  C. N. Hewitt,et al.  Biogenic volatile organic compounds in the Earth system. , 2009, The New phytologist.

[33]  J. Peñuelas,et al.  Process based inventory of isoprenoid emissions from European forests: model comparisons, current knowledge and uncertainties , 2009 .

[34]  Claudia E Vickers,et al.  A unified mechanism of action for volatile isoprenoids in plant abiotic stress. , 2009, Nature chemical biology.

[35]  R. Monson,et al.  Response of isoprene emission to ambient CO2 changes and implications for global budgets , 2009 .

[36]  R. B. Jackson,et al.  Leaf isoprene emission rate as a function of atmospheric CO2 concentration , 2009 .

[37]  D. Lawlor,et al.  Causes of Decreased Photosynthetic Rate and Metabolic Capacity in Water-deficient Leaf Cells: a Critical Evaluation of Mechanisms and Integration of Processes , 1996 .

[38]  A. Arneth,et al.  The CO2 inhibition of terrestrial isoprene emission significantly affects future ozone projections , 2008 .

[39]  R. Martin,et al.  Net ecosystem fluxes of isoprene over tropical South America inferred from Global Ozone Monitoring Experiment (GOME) observations of HCHO columns , 2008 .

[40]  I. D. Smedt,et al.  Evaluating the performance of pyrogenic and biogenic emission inventories against one decade of space-based formaldehyde columns , 2008 .

[41]  Jean-Francois Lamarque,et al.  Predicted change in global secondary organic aerosol concentrations in response to future climate, emissions, and land use change , 2008 .

[42]  T. Sharkey,et al.  Isoprene emission from plants: why and how. , 2007, Annals of botany.

[43]  Ü. Niinemets,et al.  Modeling Volatile Isoprenoid Emissions – A Story with Split Ends , 2007, Plant biology.

[44]  Benjamin Smith,et al.  CO2 inhibition of global terrestrial isoprene emissions: Potential implications for atmospheric chemistry , 2007 .

[45]  Jens Kattge,et al.  Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. , 2007, Plant, cell & environment.

[46]  S. Wofsy,et al.  Factors controlling CO2 exchange on timescales from hourly to decadal at Harvard Forest , 2007 .

[47]  Rüdiger Grote,et al.  Sensitivity of volatile monoterpene emission to changes in canopy structure: a model-based exercise with a process-based emission model. , 2007, The New phytologist.

[48]  P. Hari,et al.  Process-based estimates of terrestrial ecosystem isoprene emissions: incorporating the effects of a direct CO 2 -isoprene interaction , 2007 .

[49]  P. Palmer,et al.  Estimates of global terrestrial isoprene emissions using MEGAN (Model of Emissions of Gases and Aerosols from Nature) , 2006 .

[50]  Christine Wiedinmyer,et al.  Quantifying the Seasonal and Interannual Variability of North American Isoprene Emissions using Satellite Observations of Formaldehyde Column , 2005 .

[51]  M. Rohmer,et al.  Isoprenoid biosynthesis in plant chloroplasts via the MEP pathway: Direct thylakoid/ferredoxin‐dependent photoreduction of GcpE/IspG , 2006, FEBS letters.

[52]  T. Sharkey,et al.  A gas-exchange study of photosynthesis and isoprene emission inQuercus rubra L. , 1990, Planta.

[53]  D. Hauglustaine,et al.  Future tropospheric ozone simulated with a climate‐chemistry‐biosphere model , 2005 .

[54]  K. Hikosaka,et al.  The balance between RuBP carboxylation and RuBP regeneration: a mechanism underlying the interspecific variation in acclimation of photosynthesis to seasonal change in temperature. , 2005, Functional plant biology : FPB.

[55]  Y. Cen,et al.  The Regulation of Rubisco Activity in Response to Variation in Temperature and Atmospheric CO2 Partial Pressure in Sweet Potato1[w] , 2005, Plant Physiology.

[56]  Paul J. Valdes,et al.  The ice age methane budget , 2005 .

[57]  Jiwen Fan,et al.  Atmospheric Oxidation Mechanism of Isoprene , 2004 .

[58]  F. Loreto,et al.  13C Labeling Reveals Chloroplastic and Extrachloroplastic Pools of Dimethylallyl Pyrophosphate and Their Contribution to Isoprene Formation1 , 2004, Plant Physiology.

[59]  M. Andreae,et al.  Formation of Secondary Organic Aerosols Through Photooxidation of Isoprene , 2004, Science.

[60]  T. Sharkey,et al.  Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves , 1993, Oecologia.

[61]  T. Sharkey,et al.  On the relationship between isoprene emission and photosynthetic metabolites under different environmental conditions , 1993, Planta.

[62]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[63]  D. T. Canvin,et al.  Nitrate, nitrite and ammonia assimilation by leaves: Effect of light, carbon dioxide and oxygen , 1974, Planta.

[64]  Ü. Niinemets,et al.  Costs of production and physiology of emission of volatile leaf isoprenoids. , 2004 .

[65]  F. Loreto,et al.  13 C Labeling Reveals Chloroplastic and Extrachloroplastic Pools of Dimethylallyl Pyrophosphate and Their Contribution to Isoprene Formation 1 , 2004 .

[66]  T. Rosenstiel,et al.  Induction of poplar leaf nitrate reductase: a test of extrachloroplastic control of isoprene emission rate. , 2004, Plant biology.

[67]  J. Briantais,et al.  Partitioning of photosynthetic electron flow between CO2 and O2 reduction in a C3 leaf (Phaseolus vulgaris L.) at different CO2 concentrations and during drought stress , 2004, Planta.

[68]  C. Jones,et al.  Effect of Climate Change on Isoprene Emissions and Surface Ozone Levels , 2003 .

[69]  T. Sharkey,et al.  Biochemical regulation of isoprene emission , 2003 .

[70]  C. Körner,et al.  The process-based SIM-BIM model: towards more realistic prediction of isoprene emissions from adult Quercus petraea forest trees , 2003 .

[71]  D. Yakir,et al.  Natural Abundance Carbon Isotope Composition of Isoprene Reflects Incomplete Coupling between Isoprene Synthesis and Photosynthetic Carbon Flow , 2003, Plant Physiology.

[72]  Thomas P. Kurosu,et al.  Mapping isoprene emissions over North America using formaldehyde column observations from space , 2003 .

[73]  R. Monson,et al.  Increased CO2 uncouples growth from isoprene emission in an agriforest ecosystem , 2003, Nature.

[74]  A. Wisthaler,et al.  Xylem-transported glucose as an additional carbon source for leaf isoprene formation in Quercus robur. , 2002, The New phytologist.

[75]  Denis Loustau,et al.  Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data , 2002 .

[76]  G. Seufert,et al.  On-line analysis of the 13CO2 labeling of leaf isoprene suggests multiple subcellular origins of isoprene precursors , 2002, Planta.

[77]  Richard G. Derwent,et al.  The Oxidation of Organic Compounds in the Troposphere and their Global Warming Potentials , 2002 .

[78]  T. Sharkey,et al.  ISOPRENE EMISSION FROM PLANTS. , 2003, Annual review of plant physiology and plant molecular biology.

[79]  W. Eisenreich,et al.  Studies on the nonmevalonate pathway to terpenes: The role of the GcpE (IspG) protein , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[80]  G. Pétron,et al.  Seasonal temperature variations influence isoprene emission , 2001 .

[81]  T. Sharkey,et al.  Isoprene increases thermotolerance of fosmidomycin-fed leaves. , 2001, Plant physiology.

[82]  M. Salvucci,et al.  Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[83]  R. Monson,et al.  Biochemistry and physiology of foliar isoprene production. , 2000, Trends in plant science.

[84]  M. J. Martin,et al.  A process-based model to predict the effects of climatic change on leaf isoprene emission rates , 2000 .

[85]  C. Giersch,et al.  Process-based modelling of isoprene emission by oak leaves. , 2000 .

[86]  Paul J. Crutzen,et al.  Impact of Non-Methane Hydrocarbons on Tropospheric Chemistry and the Oxidizing Power of the Global Troposphere: 3-Dimensional Modelling Results , 2000 .

[87]  J. Tenhunen,et al.  A model of isoprene emission based on energetic requirements for isoprene synthesis and leaf photosynthetic properties for Liquidambar and Quercus , 1999 .

[88]  M. Lerdau,et al.  ISOPRENE EMISSION AND PHOTOSYNTHESIS IN A TROPICAL FOREST CANOPY: IMPLICATIONS FOR MODEL DEVELOPMENT , 1999 .

[89]  M. Rohmer,et al.  On the reduction steps in the mevalonate independent 2-C-methyl-d-erythritol 4-phosphate (MEP) pathway for isoprenoid biosynthesis in the bacterium Zymomonas mobilis , 1999 .

[90]  K. Hikosaka,et al.  Balancing carboxylation and regeneration of ribulose‐1,5‐ bisphosphate in leaf photosynthesis: temperature acclimation of an evergreen tree, Quercus myrsinaefolia , 1999 .

[91]  Hartmut K. Lichtenthaler,et al.  THE 1-DEOXY-D-XYLULOSE-5-PHOSPHATE PATHWAY OF ISOPRENOID BIOSYNTHESIS IN PLANTS. , 1999, Annual review of plant physiology and plant molecular biology.

[92]  N. Brüggemann,et al.  Isoprene synthase activity and its relation to isoprene emission in Quercus robur L. leaves , 1999 .

[93]  R. Steinbrecher,et al.  Seasonal Pattern of Isoprene Synthase Activity in Quercus robur Leaves and its Significance for Modeling Isoprene Emission Rates , 1997 .

[94]  M. Keller,et al.  Controls on isoprene emission from trees in a subtropical dry forest , 1997 .

[95]  Jörg Schwender,et al.  Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate‐independent pathway , 1997, FEBS letters.

[96]  T. Sharkey,et al.  Field measurements of isoprene emission from trees in response to temperature and light. , 1996, Tree physiology.

[97]  P. Harley,et al.  Effects of light, temperature and canopy position on net photosynthesis and isoprene emission from sweetgum (Liquidambar styraciflua) leaves. , 1996, Tree physiology.

[98]  R. Fall,et al.  Characterization of Aspen Isoprene Synthase, an Enzyme Responsible for Leaf Isoprene Emission to the Atmosphere (*) , 1995, The Journal of Biological Chemistry.

[99]  C. N. Hewitt,et al.  A global model of natural volatile organic compound emissions , 1995 .

[100]  R. Monson,et al.  Isoprene and monoterpene emission rate variability: Model evaluations and sensitivity analyses , 1993 .

[101]  T. Sharkey,et al.  Rapid appearance of 13C in biogenic isoprene when 13CO2 is fed to intact leaves , 1993 .

[102]  R. Monson,et al.  Relationships among Isoprene Emission Rate, Photosynthesis, and Isoprene Synthase Activity as Influenced by Temperature. , 1992, Plant physiology.

[103]  Russell K. Monson,et al.  Isoprene and monoterpene emission rate variability: Observations with Eucalyptus and emission rate algorithm development , 1991 .

[104]  R. Monson,et al.  Isoprene emission from aspen leaves : influence of environment and relation to photosynthesis and photorespiration. , 1989, Plant physiology.

[105]  W. Campbell.  Nitrate reductase and its role in nitrate assimilation in plants , 1988 .