Reassimilation of Leaf Internal CO2 Contributes to Isoprene Emission in the Neotropical Species Inga edulis Mart.

Garcia, Sabrina; Jardine, Kolby; Souza, Vinicius; Souza, Rodrigo; Duvoisin Junior, Sergio; Gonçalves, José

doi:10.3390/f10060472

Title: Reassimilation of Leaf Internal CO₂ Contributes to Isoprene Emission in the Neotropical Species Inga edulis Mart.

Journal Article · Thu May 30 00:00:00 EDT 2019 · Forests

DOI:https://doi.org/10.3390/f10060472· OSTI ID:1560599

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^[3]; Souza, Rodrigo ^[4]; Duvoisin Junior, Sergio ^[3];

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National Inst. for Amazonian Research (INPA), Avenida André Araújo, Amazonas (Brazil)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystem Science Division
State Univ. of Amazonas, Avenida Darcy Vargas, Amazonas (Brazil). Faculty of Chemical Engineering
State Univ. of Amazonas, Amazonas (Brazil). Meteorology Dept.

Isoprene (C₅H₈) is a hydrocarbon gas emitted by many tree species and has been shown to protect photosynthesis under abiotic stress. Under optimal conditions for photosynthesis, ~70%–90% of carbon used for isoprene biosynthesis is produced from recently assimilated atmospheric CO₂. While the contribution of alternative carbon sources that increase with leaf temperature and other stresses have been demonstrated, uncertainties remain regarding the biochemical source(s) of isoprene carbon. In this study, we investigated leaf isoprene emissions ($Is$) from neotropical species Inga edulis Mart. as a function of light and temperature under ambient (450 µmol m^-2 s^-1) and CO₂-free (0 µmol m^-2 s^-1) atmosphere. Is under CO₂-free atmosphere showed light-dependent emission patterns similar to those observed under ambient CO₂, but with lower light saturation point. Leaves treated with the photosynthesis inhibitor DCMU (3-(3,4-dichlorophenyl)-1,1-dimethylurea) failed to produce detectable Is in normal light under a CO₂-free atmosphere. While strong temperature-dependent Is were observed under CO₂-free atmosphere in the light, dark conditions failed to produce detectable Is even at the highest temperatures studied (40 °C). Treatment of leaves with ¹³C-labeled sodium bicarbonate under CO₂-free atmosphere resulted in Is with over 50% containing at least one ¹³C atom. Is under CO₂-free atmosphere and standard conditions of light and leaf temperature represented 19% ± 7% of emissions under ambient CO₂. The results show that the reassimilation of leaf internal CO₂ contributes to Is in the neotropical species I. edulis. Through the consumption of excess photosynthetic energy, our results support a role of isoprene biosynthesis, together with photorespiration, as a key tolerance mechanism against high temperature and high light in the tropics.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1560599

Journal Information:: Forests, Vol. 10, Issue 6; ISSN 1999-4907

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 10 works

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References (65)

Characterization of an Isoprene Synthase from Leaves of Quercus petraea (Mattuschka) Liebl. Schnitzler, J. -P.; Arenz, R.; Steinbrecher, R. Botanica Acta, Vol. 109, Issue 3 https://doi.org/10.1111/j.1438-8677.1996.tb00566.x	journal	June 1996
¹³ C Labeling Reveals Chloroplastic and Extrachloroplastic Pools of Dimethylallyl Pyrophosphate and Their Contribution to Isoprene Formation Loreto, Francesco; Pinelli, Paola; Brancaleoni, Enzo Plant Physiology, Vol. 135, Issue 4 https://doi.org/10.1104/pp.104.039537	journal	July 2004
Isoprene Emission from Aspen Leaves: Influence of Environment and Relation to Photosynthesis and Photorespiration Monson, Russell K.; Fall, Ray Plant Physiology, Vol. 90, Issue 1 https://doi.org/10.1104/pp.90.1.267	journal	May 1989
The Influence of Light and Temperature on Isoprene Emission Rates from Live Oak Tingey, David T.; Manning, Marybeth; Grothaus, Louis C. Physiologia Plantarum, Vol. 47, Issue 2 https://doi.org/10.1111/j.1399-3054.1979.tb03200.x	journal	October 1979
An imperative need for global change research in tropical forests Zhou, X.; Fu, Y.; Zhou, L. Tree Physiology, Vol. 33, Issue 9 https://doi.org/10.1093/treephys/tpt064	journal	September 2013
How light, temperature, and measurement and growth [CO2] interactively control isoprene emission in hybrid aspen Niinemets, Ülo; Sun, Zhihong Journal of Experimental Botany, Vol. 66, Issue 3 https://doi.org/10.1093/jxb/eru443	journal	November 2014
Contribution of Various Carbon Sources Toward Isoprene Biosynthesis in Poplar Leaves Mediated by Altered Atmospheric CO2 Concentrations Trowbridge, Amy M.; Asensio, Dolores; Eller, Allyson S. D. PLoS ONE, Vol. 7, Issue 2 https://doi.org/10.1371/journal.pone.0032387	journal	February 2012
A New Approach to Measure Gross CO ₂ Fluxes in Leaves. Gross CO ₂ Assimilation, Photorespiration, and Mitochondrial Respiration in the Light in Tomato under Drought Stress Haupt-Herting, Silke; Klug, Klaus; Fock, Heinrich P. Plant Physiology, Vol. 126, Issue 1 https://doi.org/10.1104/pp.126.1.388	journal	May 2001
Response of isoprene emission and carbon metabolism to drought in white poplar ( Populus alba ) saplings Brilli, Federico; Barta, Csengele; Fortunati, Alessio New Phytologist, Vol. 175, Issue 2 https://doi.org/10.1111/j.1469-8137.2007.02094.x	journal	July 2007
Concentration of isoprene in artificial and thylakoid membranes Harvey, Christopher M.; Li, Ziru; Tjellström, Henrik Journal of Bioenergetics and Biomembranes, Vol. 47, Issue 5 https://doi.org/10.1007/s10863-015-9625-9	journal	September 2015
Biogenic Volatile Organic Compound and Respiratory CO2 Emissions after 13C-Labeling: Online Tracing of C Translocation Dynamics in Poplar Plants Ghirardo, Andrea; Gutknecht, Jessica; Zimmer, Ina PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0017393	journal	February 2011
On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from a heat stress Velikova, V.; Loreto, F. Plant, Cell and Environment, Vol. 28, Issue 3 https://doi.org/10.1111/j.1365-3040.2004.01314.x	journal	March 2005
Enhanced isoprene emission capacity and altered light responsiveness in aspen grown under elevated atmospheric CO ₂ concentration Sun, Zhihong; Niinemets, Ülo; Hüve, Katja Global Change Biology, Vol. 18, Issue 11 https://doi.org/10.1111/j.1365-2486.2012.02789.x	journal	August 2012
Modelling metabolic CO ₂ evolution - a fresh perspective on respiration : Modelling metabolic CO Sweetlove, Lee J.; Williams, Thomas C. R.; Cheung, C. Y. Maurice Plant, Cell & Environment, Vol. 36, Issue 9 https://doi.org/10.1111/pce.12105	journal	May 2013
Abiotic stresses and induced BVOCs Loreto, Francesco; Schnitzler, Jörg-Peter Trends in Plant Science, Vol. 15, Issue 3 https://doi.org/10.1016/j.tplants.2009.12.006	journal	March 2010
Ecological and evolutionary aspects of isoprene emission from plants Harley, Peter C.; Monson, Russell K.; Lerdau, Manuel T. Oecologia, Vol. 118, Issue 2 https://doi.org/10.1007/s004420050709	journal	February 1999
Gas Phase Measurements of Pyruvic Acid and Its Volatile Metabolites Jardine, Kolby J.; Sommer, Evan D.; Saleska, Scott R. Environmental Science & Technology, Vol. 44, Issue 7 https://doi.org/10.1021/es903544p	journal	April 2010
Alternative Carbon Sources for Isoprene Emission de Souza, Vinícius Fernandes; Niinemets, Ülo; Rasulov, Bahtijor Trends in Plant Science, Vol. 23, Issue 12 https://doi.org/10.1016/j.tplants.2018.09.012	journal	December 2018
Protection by Isoprene against Singlet Oxygen in Leaves Affek, Hagit P.; Yakir, Dan Plant Physiology, Vol. 129, Issue 1 https://doi.org/10.1104/pp.010909	journal	April 2002
On-line analysis of the 13 CO 2 labeling of leaf isoprene suggests multiple subcellular origins of isoprene precursors T., Karl; R., Fall; T., Rosenstiel Planta, Vol. 215, Issue 6 https://doi.org/10.1007/s00425-002-0825-2	journal	October 2002
Isoprene Increases Thermotolerance of Fosmidomycin-Fed Leaves Sharkey, Thomas D.; Chen, Xiuyin; Yeh, Sansun Plant Physiology, Vol. 125, Issue 4 https://doi.org/10.1104/pp.125.4.2001	journal	April 2001
The 1-Deoxy-D-Xylulose-5-Phosphate Pathway of Isoprenoid Biosynthesis in Plants Lichtenthaler, Hartmut K. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.arplant.50.1.47	journal	June 1999
Photorespiratory and respiratory decarboxylations in leaves of C ₃ plants under different CO ₂ concentrations and irradiances PÄRnik, T.; Ivanova, H.; Keerberg, O. Plant, Cell & Environment, Vol. 30, Issue 12 https://doi.org/10.1111/j.1365-3040.2007.01725.x	journal	December 2007
Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves Sharkey, Thomas D.; Loreto, Francesco Oecologia, Vol. 95, Issue 3 https://doi.org/10.1007/BF00320984	journal	September 1993
Characterization of Aspen Isoprene Synthase, an Enzyme Responsible for Leaf Isoprene Emission to the Atmosphere Silver, Gary M.; Fall, Ray Journal of Biological Chemistry, Vol. 270, Issue 22 https://doi.org/10.1074/jbc.270.22.13010	journal	June 1995
Is it useful to ask why plants emit isoprene?: Isoprene synthase evolution Sharkey, Thomas D. Plant, Cell & Environment, Vol. 36, Issue 3 https://doi.org/10.1111/pce.12038	journal	December 2012
Internal recycling of respired CO ₂ may be important for plant functioning under changing climate regimes Bloemen, Jasper; Anne McGuire, Mary; Aubrey, Doug P. Plant Signaling & Behavior, Vol. 8, Issue 12 https://doi.org/10.4161/psb.27530	journal	December 2013
How will Earth's surface temperature change in future decades?: SURFACE TEMPERATURE FORECASTS Lean, Judith L.; Rind, David H. Geophysical Research Letters, Vol. 36, Issue 15 https://doi.org/10.1029/2009GL038932	journal	August 2009
Relationships among Isoprene Emission Rate, Photosynthesis, and Isoprene Synthase Activity as Influenced by Temperature Monson, Russell K.; Jaeger, Charles H.; Adams, William W. Plant Physiology, Vol. 98, Issue 3 https://doi.org/10.1104/pp.98.3.1175	journal	March 1992
Temperature Response of Isoprene Emission in Vivo Reflects a Combined Effect of Substrate Limitations and Isoprene Synthase Activity: A Kinetic Analysis Rasulov, Bahtijor; Hüve, Katja; Bichele, Irina Plant Physiology, Vol. 154, Issue 3 https://doi.org/10.1104/pp.110.162081	journal	September 2010
Network Analysis of the MVA and MEP Pathways for Isoprenoid Synthesis Vranová, Eva; Coman, Diana; Gruissem, Wilhelm Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120116	journal	April 2013
Dynamic Balancing of Isoprene Carbon Sources Reflects Photosynthetic and Photorespiratory Responses to Temperature Stress Jardine, Kolby; Chambers, Jeffrey; Alves, Eliane G. Plant Physiology, Vol. 166, Issue 4 https://doi.org/10.1104/pp.114.247494	journal	October 2014
Contribution of Different Carbon Sources to Isoprene Biosynthesis in Poplar Leaves Schnitzler, Jörg-Peter; Graus, Martin; Kreuzwieser, Jürgen Plant Physiology, Vol. 135, Issue 1 https://doi.org/10.1104/pp.103.037374	journal	April 2004
The emission factor of volatile isoprenoids: stress, acclimation, and developmental responses Niinemets, Ü.; Arneth, A.; Kuhn, U. Biogeosciences Discussions, Vol. 7, Issue 2 https://doi.org/10.5194/bgd-7-1529-2010	journal	January 2010
The contribution of reactive carbon emissions from vegetation to the carbon balance of terrestrial ecosystems Guenther, Alex Chemosphere, Vol. 49, Issue 8 https://doi.org/10.1016/S0045-6535(02)00384-3	journal	December 2002
Urgent need for warming experiments in tropical forests Cavaleri, Molly A.; Reed, Sasha C.; Smith, W. Kolby Global Change Biology, Vol. 21, Issue 6 https://doi.org/10.1111/gcb.12860	journal	March 2015
Emerging concept for the role of photorespiration as an important part of abiotic stress response Voss, I.; Sunil, B.; Scheibe, R. Plant Biology, Vol. 15, Issue 4 https://doi.org/10.1111/j.1438-8677.2012.00710.x	journal	March 2013
Global Climate Forcing by Criteria Air Pollutants Unger, Nadine Annual Review of Environment and Resources, Vol. 37, Issue 1 https://doi.org/10.1146/annurev-environ-082310-100824	journal	November 2012
Secondary Organic Aerosol Formation from Isoprene Photooxidation Kroll, Jesse H.; Ng, Nga L.; Murphy, Shane M. Environmental Science & Technology, Vol. 40, Issue 6 https://doi.org/10.1021/es0524301	journal	March 2006
Formation of Secondary Organic Aerosols Through Photooxidation of Isoprene Claeys, M. Science, Vol. 303, Issue 5661 https://doi.org/10.1126/science.1092805	journal	February 2004
Methanol and isoprene emissions from the fast growing tropical pioneer species Vismia guianensis (Aubl.) Pers. (Hypericaceae) in the central Amazon forest Jardine, Kolby J.; Jardine, Angela B.; Souza, Vinicius F. Atmospheric Chemistry and Physics, Vol. 16, Issue 10 https://doi.org/10.5194/acp-16-6441-2016	journal	January 2016
An Evaluation of the Recycling in Measurements of Photorespiration Gerbaud, Alain; Andre, Marcel Plant Physiology, Vol. 83, Issue 4 https://doi.org/10.1104/pp.83.4.933	journal	April 1987
Estimation of photorespiratory carbon dioxide recycling during photosynthesis Delfine, Sebastiano; Di Marco, Giorgio; Loreto, Francesco Functional Plant Biology, Vol. 26, Issue 8 https://doi.org/10.1071/PP99096	journal	January 1999
Photorespiration: metabolic pathways and their role in stress protection Wingler, Astrid; Lea, Peter J.; Quick, W. Paul Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402 https://doi.org/10.1098/rstb.2000.0712	journal	October 2000
A unified mechanism of action for volatile isoprenoids in plant abiotic stress Vickers, Claudia E.; Gershenzon, Jonathan; Lerdau, Manuel T. Nature Chemical Biology, Vol. 5, Issue 5 https://doi.org/10.1038/nchembio.158	journal	April 2009
Stress-induced changes in carbon sources for isoprene production in Populus deltoides Funk, J. L.; Mak, J. E.; Lerdau, M. T. Plant, Cell and Environment, Vol. 27, Issue 6 https://doi.org/10.1111/j.1365-3040.2004.01177.x	journal	June 2004
Estimates of global terrestrial isoprene emissions using MEGAN (Model of Emissions of Gases and Aerosols from Nature) Guenther, A.; Karl, T.; Harley, P. Atmospheric Chemistry and Physics Discussions, Vol. 6, Issue 1 https://doi.org/10.5194/acpd-6-107-2006	journal	January 2006
El Niño drought increased canopy turnover in Amazon forests Leitold, Veronika; Morton, Douglas C.; Longo, Marcos New Phytologist, Vol. 219, Issue 3 https://doi.org/10.1111/nph.15110	journal	March 2018
Xylem-transported glucose as an additional carbon source for leaf isoprene formation in Quercus robur Kreuzwieser, Jurgen; Graus, Martin; Wisthaler, Armin New Phytologist, Vol. 156, Issue 2 https://doi.org/10.1046/j.1469-8137.2002.00516.x	journal	November 2002
Increased Thermostability of Thylakoid Membranes in Isoprene-Emitting Leaves Probed with Three Biophysical Techniques Velikova, Violeta; Várkonyi, Zsuzsanna; Szabó, Milán Plant Physiology, Vol. 157, Issue 2 https://doi.org/10.1104/pp.111.182519	journal	August 2011
Atmospheric Degradation of Volatile Organic Compounds Atkinson, Roger; Arey, Janet Chemical Reviews, Vol. 103, Issue 12 https://doi.org/10.1021/cr0206420	journal	December 2003
Emission of Isoprene from Salt-Stressed Eucalyptus globulus Leaves Loreto, Francesco; Delfine, Sebastiano Plant Physiology, Vol. 123, Issue 4 https://doi.org/10.1104/pp.123.4.1605	journal	August 2000
C ₃ plants enhance rates of photosynthesis by reassimilating photorespired and respired CO ₂ : Intracellular CO Busch, Florian A.; Sage, Tammy L.; Cousins, Asaph B. Plant, Cell & Environment, Vol. 36, Issue 1 https://doi.org/10.1111/j.1365-3040.2012.02567.x	journal	July 2012
Isoprene research - 60 years later, the biology is still enigmatic: Isoprene research Sharkey, Thomas D.; Monson, Russell K. Plant, Cell & Environment, Vol. 40, Issue 9 https://doi.org/10.1111/pce.12930	journal	March 2017
The oxidative pentose phosphate pathway: structure and organisation Kruger, Nicholas J.; von Schaewen, Antje Current Opinion in Plant Biology, Vol. 6, Issue 3 https://doi.org/10.1016/S1369-5266(03)00039-6	journal	June 2003
Natural Abundance Carbon Isotope Composition of Isoprene Reflects Incomplete Coupling between Isoprene Synthesis and Photosynthetic Carbon Flow Affek, Hagit P.; Yakir, Dan Plant Physiology, Vol. 131, Issue 4 https://doi.org/10.1104/pp.102.012294	journal	March 2003
Rapid appearance of 13C in biogenic isoprene when 13CO2 is fed to intact leaves Delwiche, C. F.; Sharkey, T. D. Plant, Cell and Environment, Vol. 16, Issue 5 https://doi.org/10.1111/j.1365-3040.1993.tb00907.x	journal	June 1993
Photosynthetic Electron Transport Controls Expression of the High Light Inducible Gene in the Cyanobacterium Synechococcus elongatus Strain PCC 7942 Salem, Kavitha; van Waasbergen, Lorraine G. Plant and Cell Physiology, Vol. 45, Issue 5 https://doi.org/10.1093/pcp/pch072	journal	May 2004
The Functional Anatomy of Rice Leaves: Implications for Refixation of Photorespiratory CO2 and Efforts to Engineer C4 Photosynthesis into Rice Sage, T. L.; Sage, R. F. Plant and Cell Physiology, Vol. 50, Issue 4 https://doi.org/10.1093/pcp/pcp033	journal	February 2009
Why only some plants emit isoprene: Phylogeny of isoprene Monson, Russell K.; Jones, Ryan T.; Rosenstiel, Todd N. Plant, Cell & Environment, Vol. 36, Issue 3 https://doi.org/10.1111/pce.12015	journal	October 2012
Atmospheric Degradation of Volatile Organic Compounds Atkinson, Roger; Arey, Janet ChemInform, Vol. 35, Issue 10 https://doi.org/10.1002/chin.200410285	journal	March 2004
Biogenic volatile organic compound and respiratory CO₂ emissions after ¹³C-labeling: online tracing of C translocation dynamics in poplar plants Ghirado, A.; Gutknecht, J.; Zimmer, I. Karlsruhe https://doi.org/10.5445/ir/110087648	text	January 2011
The emission factor of volatile isoprenoids: stress, acclimation, and developmental responses Niinemets, Ü.; Arneth, A.; Kuhn, U. Biogeosciences, Vol. 7, Issue 7 https://doi.org/10.5194/bg-7-2203-2010	journal	January 2010
Estimates of global terrestrial isoprene emissions using MEGAN (Model of Emissions of Gases and Aerosols from Nature) Guenther, A.; Karl, T.; Harley, P. Atmospheric Chemistry and Physics, Vol. 6, Issue 11 https://doi.org/10.5194/acp-6-3181-2006	journal	January 2006
Methanol and isoprene emissions from the fast growing tropical pioneer species Vismia guianensis (Aubl.) Pers. (Hypericaceae) in the central Amazon forest Jardine, Kolby J.; Jardine, Angela B.; Souza, Vinicius F. Karlsruhe https://doi.org/10.5445/ir/1000121828	text	January 2016

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Title: Reassimilation of Leaf Internal CO2 Contributes to Isoprene Emission in the Neotropical Species Inga edulis Mart.

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Title: Reassimilation of Leaf Internal CO₂ Contributes to Isoprene Emission in the Neotropical Species Inga edulis Mart.