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Title: Isoprene: New insights into the control of emission and mediation of stress tolerance by gene expression

Abstract

Isoprene is a volatile compound produced in large amounts by some, but not all, plants by the enzyme isoprene synthase. Plants emit vast quantities of isoprene, with a net global output of 600 Tg per year, and typical emission rates from individual plants around 2% of net carbon assimilation. There is significant debate about whether global climate change resulting from increasing CO2 in the atmosphere will increase or decrease global isoprene emission in the future. We show evidence supporting predictions of increased isoprene emission in the future, but the effects could vary depending on the environment under consideration. For many years, isoprene was believed to have immediate, physical effects on plants such as changing membrane properties or quenching reactive oxygen species. Although observations sometimes supported these hypotheses, the effects were not always observed, and the reasons for the variability were not apparent. Although there may be some physical effects, recent studies show that isoprene has significant effects on gene expression, the proteome, and the metabolome of both emitting and nonemitting species. Consistent results are seen across species and specific treatment protocols. Finally, this review summarizes recent findings on the role and control of isoprene emission from plants.

Authors:
 [1];  [1];  [1]; ORCiD logo [2]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
  2. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Great Lakes Bioenergy Research Center, Madison, MI (United States)
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)
OSTI Identifier:
1607880
Alternate Identifier(s):
OSTI ID: 1557327
Grant/Contract Number:  
FG02-91ER20021; T32 GM110523-06; SC0018409
Resource Type:
Accepted Manuscript
Journal Name:
Plant, Cell and Environment
Additional Journal Information:
Journal Volume: 42; Journal Issue: 10; Journal ID: ISSN 0140-7791
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; climate change; CO2; growth; high temperature; signaling; stress tolerance; triose phosphate utilization limitation; isoprene

Citation Formats

Lantz, Alexandra T., Allman, Joshua, Weraduwage, Sarathi M., and Sharkey, Thomas D. Isoprene: New insights into the control of emission and mediation of stress tolerance by gene expression. United States: N. p., 2019. Web. doi:10.1111/pce.13629.
Lantz, Alexandra T., Allman, Joshua, Weraduwage, Sarathi M., & Sharkey, Thomas D. Isoprene: New insights into the control of emission and mediation of stress tolerance by gene expression. United States. https://doi.org/10.1111/pce.13629
Lantz, Alexandra T., Allman, Joshua, Weraduwage, Sarathi M., and Sharkey, Thomas D. Sat . "Isoprene: New insights into the control of emission and mediation of stress tolerance by gene expression". United States. https://doi.org/10.1111/pce.13629. https://www.osti.gov/servlets/purl/1607880.
@article{osti_1607880,
title = {Isoprene: New insights into the control of emission and mediation of stress tolerance by gene expression},
author = {Lantz, Alexandra T. and Allman, Joshua and Weraduwage, Sarathi M. and Sharkey, Thomas D.},
abstractNote = {Isoprene is a volatile compound produced in large amounts by some, but not all, plants by the enzyme isoprene synthase. Plants emit vast quantities of isoprene, with a net global output of 600 Tg per year, and typical emission rates from individual plants around 2% of net carbon assimilation. There is significant debate about whether global climate change resulting from increasing CO2 in the atmosphere will increase or decrease global isoprene emission in the future. We show evidence supporting predictions of increased isoprene emission in the future, but the effects could vary depending on the environment under consideration. For many years, isoprene was believed to have immediate, physical effects on plants such as changing membrane properties or quenching reactive oxygen species. Although observations sometimes supported these hypotheses, the effects were not always observed, and the reasons for the variability were not apparent. Although there may be some physical effects, recent studies show that isoprene has significant effects on gene expression, the proteome, and the metabolome of both emitting and nonemitting species. Consistent results are seen across species and specific treatment protocols. Finally, this review summarizes recent findings on the role and control of isoprene emission from plants.},
doi = {10.1111/pce.13629},
journal = {Plant, Cell and Environment},
number = 10,
volume = 42,
place = {United States},
year = {Sat Jul 27 00:00:00 EDT 2019},
month = {Sat Jul 27 00:00:00 EDT 2019}
}

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Figures / Tables:

Table 1 Table 1: Q10 values for isoprene emission and assimilation. Values were calculated at 400 ppm CO2 for a temperature increase from 25 to 35°C. (Reproduced from Lantz et al. 2019)

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journal, July 2005


Conversion of [1-3H2,G-14C]geranyl pyrophosphate to cyclic monoterpenes without loss of tritium
journal, April 1981


Diurnal profiles of isoprene, methacrolein and methyl vinyl ketone at an urban site in Hong Kong
journal, February 2014


Observed and modeled ecosystem isoprene fluxes from an oak-dominated temperate forest and the influence of drought stress
journal, February 2014


Biogenic isoprene emission as expression of dissipativity, a fundamental cell property
journal, March 2017


Role of isoprene in secondary organic aerosol formation on a regional scale
journal, January 2007

  • Zhang, Yang; Huang, Jian-Ping; Henze, Daven K.
  • Journal of Geophysical Research, Vol. 112, Issue D20
  • DOI: 10.1029/2007JD008675

Use of carbon-11 in Populus shows that exogenous jasmonic acid increases biosynthesis of isoprene from recently fixed carbon
journal, May 2005


Transgenic, non-isoprene emitting poplars don’t like it hot: Thermotolerance in isoprene emission knock-down mutants of poplar
journal, June 2007


Kinetics of leaf temperature fluctuation affect isoprene emission from red oak (Quercus rubra) leaves
journal, December 1999


Spectacular Oscillations in Plant Isoprene Emission under Transient Conditions Explain the Enigmatic CO 2 Response
journal, October 2016

  • Rasulov, Bahtijor; Talts, Eero; Niinemets, Ülo
  • Plant Physiology, Vol. 172, Issue 4
  • DOI: 10.1104/pp.16.01002

North American isoprene influence on intercontinental ozone pollution
journal, January 2011

  • Fiore, A. M.; Levy II, H.; Jaffe, D. A.
  • Atmospheric Chemistry and Physics, Vol. 11, Issue 4
  • DOI: 10.5194/acp-11-1697-2011

Modeling the isoprene emission rate from leaves: Tansley review
journal, June 2012


Isoprene Emission from Aspen Leaves: Influence of Environment and Relation to Photosynthesis and Photorespiration
journal, May 1989


The Effect of Isoprene on the Properties of Spinach Thylakoids and Phosphatidyicholine Liposomes
journal, November 1999


Diurnal variation of dimethylallyl diphosphate concentrations in oak (Quercus robur) leaves
journal, June 2002


Isoprenoid emissions, photosynthesis and mesophyll diffusion conductance in response to blue light
journal, November 2013


Monoterpene emission from coniferous trees in response to elevated CO2 concentration and climate warming
journal, March 1999


Elevated [CO2] magnifies isoprene emissions under heat and improves thermal resistance in hybrid aspen
journal, October 2013

  • Sun, Zhihong; Hüve, Katja; Vislap, Vivian
  • Journal of Experimental Botany, Vol. 64, Issue 18
  • DOI: 10.1093/jxb/ert318

Importance of monoterpenes and isoprene in urban air in northern Europe
journal, November 2012


Arabidopsis, a Model to Study Biological Functions of Isoprene Emission?
journal, April 2007

  • Loivamäki, Maaria; Gilmer, Frank; Fischbach, Robert J.
  • Plant Physiology, Vol. 144, Issue 2
  • DOI: 10.1104/pp.107.098509

Biogenic isoprene in subtropical urban settings and implications for air quality
journal, November 2013


Isoprene Emission Rate and Intercellular Isoprene Concentration as Influenced by Stomatal Distribution and Conductance
journal, October 1992


Thermotolerant cyclamen with reduced acrolein and methyl vinyl ketone
journal, April 2012

  • Kai, Hiroomi; Hirashima, Keita; Matsuda, Osamu
  • Journal of Experimental Botany, Vol. 63, Issue 11
  • DOI: 10.1093/jxb/ers110

Ecological and evolutionary aspects of isoprene emission from plants
journal, February 1999

  • Harley, Peter C.; Monson, Russell K.; Lerdau, Manuel T.
  • Oecologia, Vol. 118, Issue 2
  • DOI: 10.1007/s004420050709

Contributions and source identification of biogenic and anthropogenic hydrocarbons to secondary organic aerosols at Mt. Tai in 2014
journal, January 2017


Alternative Carbon Sources for Isoprene Emission
journal, December 2018

  • de Souza, Vinícius Fernandes; Niinemets, Ülo; Rasulov, Bahtijor
  • Trends in Plant Science, Vol. 23, Issue 12
  • DOI: 10.1016/j.tplants.2018.09.012

Isoprene Increases Thermotolerance of Fosmidomycin-Fed Leaves
journal, April 2001

  • Sharkey, Thomas D.; Chen, Xiuyin; Yeh, Sansun
  • Plant Physiology, Vol. 125, Issue 4
  • DOI: 10.1104/pp.125.4.2001

Isoprene Synthase Genes form a Monophyletic Clade of Acyclic Terpene Synthases in the Tps-B Terpene Synthase Family: Isoprene Synthase Evolution
journal, December 2012

  • Sharkey, Thomas D.; Gray, Dennis W.; Pell, Heather K.
  • Evolution, Vol. 67, Issue 4
  • DOI: 10.1111/evo.12013

Isoprene function in two contrasting poplars under salt and sunflecks
journal, March 2013


Terpenoid synthase structures: a so far incomplete view of complex catalysis
journal, January 2012

  • Gao, Yang; Honzatko, Richard B.; Peters, Reuben J.
  • Natural Product Reports, Vol. 29, Issue 10
  • DOI: 10.1039/c2np20059g

Overlooking the canopy: The importance of canopy structure in scaling isoprenoid emissions from the leaf to the landscape
journal, February 2011


Isoprene and nitric oxide reduce damages in leaves exposed to oxidative stress
journal, December 2008


Evolutionary significance of isopreneemission from mosses
journal, May 1999

  • Hanson, David T.; Swanson, Sarah; Graham, Linda E.
  • American Journal of Botany, Vol. 86, Issue 5
  • DOI: 10.2307/2656571

Characterization of Aspen Isoprene Synthase, an Enzyme Responsible for Leaf Isoprene Emission to the Atmosphere
journal, June 1995


Is it useful to ask why plants emit isoprene?: Isoprene synthase evolution
journal, December 2012

  • Sharkey, Thomas D.
  • Plant, Cell & Environment, Vol. 36, Issue 3
  • DOI: 10.1111/pce.12038

Relationships among Isoprene Emission Rate, Photosynthesis, and Isoprene Synthase Activity as Influenced by Temperature
journal, March 1992

  • Monson, Russell K.; Jaeger, Charles H.; Adams, William W.
  • Plant Physiology, Vol. 98, Issue 3
  • DOI: 10.1104/pp.98.3.1175

Endogenous isoprene protects Phragmites australis leaves against singlet oxygen
journal, October 2004


Isoprenoid biosynthesis in plant chloroplasts via the MEP pathway: Direct thylakoid/ferredoxin-dependent photoreduction of GcpE/IspG
journal, February 2006


Formation of Secondary Organic Aerosols Through Photooxidation of Isoprene
journal, February 2004


Uncertainty in biogenic isoprene emissions and its impacts on tropospheric chemistry in East Asia
journal, October 2013


Isoprene emission protects photosynthesis in sunfleck exposed Grey poplar
journal, February 2010


Postillumination Isoprene Emission: In Vivo Measurements of Dimethylallyldiphosphate Pool Size and Isoprene Synthase Kinetics in Aspen Leaves
journal, January 2009

  • Rasulov, Bahtijor; Copolovici, Lucian; Laisk, Agu
  • Plant Physiology, Vol. 149, Issue 3
  • DOI: 10.1104/pp.108.133512

Seasonal Variations in Isoprene Emissions from a Boreal Aspen Forest
journal, July 1999


Isoprene Suppression by CO2 Is Not Due to Triose Phosphate Utilization (TPU) Limitation
journal, April 2019

  • Lantz, Alexandra T.; Solomon, Christine; Gog, Linus
  • Frontiers in Forests and Global Change, Vol. 2
  • DOI: 10.3389/ffgc.2019.00008

Retrograde Signaling by the Plastidial Metabolite MEcPP Regulates Expression of Nuclear Stress-Response Genes
journal, June 2012


Rapid appearance of 13C in biogenic isoprene when 13CO2 is fed to intact leaves
journal, June 1993


Effect of Temperature on Postillumination Isoprene Emission in Oak and Poplar
journal, December 2010

  • Li, Ziru; Ratliff, Ellen A.; Sharkey, Thomas D.
  • Plant Physiology, Vol. 155, Issue 2
  • DOI: 10.1104/pp.110.167551

Estimates of global terrestrial isoprene emissions using MEGAN (Model of Emissions of Gases and Aerosols from Nature)
journal, January 2006

  • Guenther, A.; Karl, T.; Harley, P.
  • Atmospheric Chemistry and Physics, Vol. 6, Issue 11
  • DOI: 10.5194/acp-6-3181-2006

Warming increases isoprene emissions from an arctic fen
journal, May 2016


Dissecting the role of isoprene and stress-related hormones (ABA and ethylene) in Populus nigra exposed to unequal root zone water stress
journal, July 2017

  • Marino, Giovanni; Brunetti, Cecilia; Tattini, Massimiliano
  • Tree Physiology, Vol. 37, Issue 12
  • DOI: 10.1093/treephys/tpx083

Why only some plants emit isoprene: Phylogeny of isoprene
journal, October 2012

  • Monson, Russell K.; Jones, Ryan T.; Rosenstiel, Todd N.
  • Plant, Cell & Environment, Vol. 36, Issue 3
  • DOI: 10.1111/pce.12015

Thermotolerant cyclamen with reduced acrolein and methyl vinyl ketone
other, January 2012

  • Kai, Hiroomi; Hirashima, Keita; Matsuda, Osamu
  • Oxford : Oxford Univ. Press
  • DOI: 10.15488/469

Estimates of global terrestrial isoprene emissions using MEGAN (Model of Emissions of Gases and Aerosols from Nature)
journal, January 2006

  • Guenther, A.; Karl, T.; Harley, P.
  • Atmospheric Chemistry and Physics Discussions, Vol. 6, Issue 1
  • DOI: 10.5194/acpd-6-107-2006

Works referencing / citing this record:

Rapid conversion of isoprene photooxidation products in terrestrial plants
journal, November 2020


Overexpression of Isoprene Synthase Affects ABA- and Drought-Related Gene Expression and Enhances Tolerance to Abiotic Stress
journal, June 2020

  • Xu, Jia; Trainotti, Livio; Li, Mingai
  • International Journal of Molecular Sciences, Vol. 21, Issue 12
  • DOI: 10.3390/ijms21124276

Shoot Characterization of Isoprene and Ocimene-Emitting Transgenic Arabidopsis Plants under Contrasting Environmental Conditions
journal, April 2020


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.