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Title: Stimulation of isoprene emissions and electron transport rates are a key mechanism of thermal tolerance in the tropical species Vismia guianensis

Abstract

Tropical forests absorb large amounts of atmospheric CO2 through photosynthesis, but high surface temperatures suppress this absorption while promoting isoprene emissions. While mechanistic isoprene emission models predict a tight coupling to photosynthetic electron transport (ETR) as a function of temperature, direct field observations of these phenomenon are lacking in the tropics and are necessary to assess the impact of a warming climate on global isoprene emissions. Here, we demonstrate that in the early successional species Vismia guianensis in the central Amazon, ETR rates increased with temperature in concert with isoprene emissions, even as stomatal conductance (gs) and net photosynthetic carbon fixation (Pn) declined. We observed the highest temperatures of continually increasing isoprene emissions yet reported (50°C). While Pn showed an optimum value of 32.6 ± 0.4°C, isoprene emissions, ETR, and the oxidation state of PSII reaction centers (qL) increased with leaf temperature with strong linear correlations for ETR (? = 0.98) and qL (? = 0.99) with leaf isoprene emissions. In contrast, other photoprotective mechanisms, such as non-photochemical quenching (NPQ), were not activated at elevated temperatures. Inhibition of isoprenoid biosynthesis repressed Pn at high temperatures through a mechanism that was independent of stomatal closure. While extreme warming will decrease gsmore » and Pn in tropical species, our observations support a thermal tolerance mechanism where the maintenance of high photosynthetic capacity under extreme warming is assisted by the simultaneous stimulation of ETR and metabolic pathways that consume the direct products of ETR including photorespiration and the biosynthesis of thermoprotective isoprenoids. Our results confirm that models which link isoprene emissions to the rate of ETR hold true in tropical species and provide necessary “ground-truthing” for simulations of the large predicted increases in tropical isoprene emissions with climate warming.« less

Authors:
 [1];  [2];  [3]; ORCiD logo [4]; ORCiD logo [5];  [1];  [6];  [6]
  1. National Inst. for Amazon Research (INPA), Manaus, Amazonas (Brazil)
  2. Univ. of California, Berkeley, CA (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  5. Brookhaven National Lab. (BNL), Upton, NY (United States). Biological, Environmental & Climate Sciences Dept.
  6. National Inst. for Amazon Research (INPA), Manaus, Amazonas (Brazil); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Brookhaven National Laboratory (BNL), Upton, NY (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); National Institute for Amazon Research (INPA)
OSTI Identifier:
1632387
Alternate Identifier(s):
OSTI ID: 1635196; OSTI ID: 1641861; OSTI ID: 1671404; OSTI ID: 1843020
Report Number(s):
BNL-215992-2020-JAAM; PNNL-SA-156475
Journal ID: ISSN 1354-1013
Grant/Contract Number:  
AC02-05CH11231; AC05-00OR22725; SC0012704; DE‐AC05‐00OR22725; DE‐SC0012704; DE‐AC02‐05CH11231; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Global Change Biology
Additional Journal Information:
Journal Volume: 26; Journal Issue: 10; Journal ID: ISSN 1354-1013
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; chlorophyll fluorescence; electron transport rates; fosmidomycin; global warming; high temperature stress; isoprene energetic requirements; leaf gas exchange; net photosynthesis

Citation Formats

Rodrigues, Tayana B., Baker, Christopher R., Walker, Anthony P., McDowell, Nate, Rogers, Alistair, Higuchi, Niro, Chambers, Jeffrey Q., and Jardine, Kolby J. Stimulation of isoprene emissions and electron transport rates are a key mechanism of thermal tolerance in the tropical species Vismia guianensis. United States: N. p., 2020. Web. doi:10.1111/gcb.15213.
Rodrigues, Tayana B., Baker, Christopher R., Walker, Anthony P., McDowell, Nate, Rogers, Alistair, Higuchi, Niro, Chambers, Jeffrey Q., & Jardine, Kolby J. Stimulation of isoprene emissions and electron transport rates are a key mechanism of thermal tolerance in the tropical species Vismia guianensis. United States. https://doi.org/10.1111/gcb.15213
Rodrigues, Tayana B., Baker, Christopher R., Walker, Anthony P., McDowell, Nate, Rogers, Alistair, Higuchi, Niro, Chambers, Jeffrey Q., and Jardine, Kolby J. Thu . "Stimulation of isoprene emissions and electron transport rates are a key mechanism of thermal tolerance in the tropical species Vismia guianensis". United States. https://doi.org/10.1111/gcb.15213. https://www.osti.gov/servlets/purl/1632387.
@article{osti_1632387,
title = {Stimulation of isoprene emissions and electron transport rates are a key mechanism of thermal tolerance in the tropical species Vismia guianensis},
author = {Rodrigues, Tayana B. and Baker, Christopher R. and Walker, Anthony P. and McDowell, Nate and Rogers, Alistair and Higuchi, Niro and Chambers, Jeffrey Q. and Jardine, Kolby J.},
abstractNote = {Tropical forests absorb large amounts of atmospheric CO2 through photosynthesis, but high surface temperatures suppress this absorption while promoting isoprene emissions. While mechanistic isoprene emission models predict a tight coupling to photosynthetic electron transport (ETR) as a function of temperature, direct field observations of these phenomenon are lacking in the tropics and are necessary to assess the impact of a warming climate on global isoprene emissions. Here, we demonstrate that in the early successional species Vismia guianensis in the central Amazon, ETR rates increased with temperature in concert with isoprene emissions, even as stomatal conductance (gs) and net photosynthetic carbon fixation (Pn) declined. We observed the highest temperatures of continually increasing isoprene emissions yet reported (50°C). While Pn showed an optimum value of 32.6 ± 0.4°C, isoprene emissions, ETR, and the oxidation state of PSII reaction centers (qL) increased with leaf temperature with strong linear correlations for ETR (? = 0.98) and qL (? = 0.99) with leaf isoprene emissions. In contrast, other photoprotective mechanisms, such as non-photochemical quenching (NPQ), were not activated at elevated temperatures. Inhibition of isoprenoid biosynthesis repressed Pn at high temperatures through a mechanism that was independent of stomatal closure. While extreme warming will decrease gs and Pn in tropical species, our observations support a thermal tolerance mechanism where the maintenance of high photosynthetic capacity under extreme warming is assisted by the simultaneous stimulation of ETR and metabolic pathways that consume the direct products of ETR including photorespiration and the biosynthesis of thermoprotective isoprenoids. Our results confirm that models which link isoprene emissions to the rate of ETR hold true in tropical species and provide necessary “ground-truthing” for simulations of the large predicted increases in tropical isoprene emissions with climate warming.},
doi = {10.1111/gcb.15213},
journal = {Global Change Biology},
number = 10,
volume = 26,
place = {United States},
year = {Thu Jun 11 00:00:00 EDT 2020},
month = {Thu Jun 11 00:00:00 EDT 2020}
}

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