Stimulation of isoprene emissions and electron transport rates as key mechanisms of thermal tolerance in the tropical species Vismia guianensis

Tayana B. Rodrigues, Christopher R. Baker, Anthony P. Walker, Nate McDowell, Alistair Rogers, Niro Higuchi, Jeffrey Q. Chambers, Kolby J. Jardine

Research output: Contribution to journalArticlepeer-review

23 Scopus citations

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 this 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 (ƿ = 0.98) and qL (ƿ = 0.99) with leaf isoprene emissions. In contrast, other photoprotective mechanisms, such as non-photochemical quenching, 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.

Original languageEnglish
Pages (from-to)5928-5941
Number of pages14
JournalGlobal Change Biology
Volume26
Issue number10
DOIs
StatePublished - Oct 1 2020

Funding

This material is based upon work supported as part of the Next Generation Ecosystem Experiments‐Tropics (NGEE‐Tropics) funded by the US Department of Energy, Office of Science, Office of Biological and Environmental Research’s Terrestrial Ecosystem Science Program through contract no. DE‐AC02‐05CH11231 to Lawrence Berkeley National Laboratory, DE‐AC05‐00OR22725 to Oak Ridge National Laboratory, and DE‐SC0012704 to Brookhaven National Laboratory. Additional funding for this research was provided by the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). Logistical and scientific support is acknowledged by the Forest Management laboratory (LMF), Climate and Environment (CLIAMB), and Large Scale Biosphere‐Atmosphere (LBA) programs at the National Institute for Amazon Research (INPA). This material is based upon work supported as part of the Next Generation Ecosystem Experiments-Tropics (NGEE-Tropics) funded by the US Department of Energy, Office of Science, Office of Biological and Environmental Research?s Terrestrial Ecosystem Science Program through contract no. DE-AC02-05CH11231 to Lawrence Berkeley National Laboratory, DE-AC05-00OR22725 to Oak Ridge National Laboratory, and DE-SC0012704 to Brookhaven National Laboratory. Additional funding for this research was provided by the Brazilian Conselho Nacional de Desenvolvimento Cient?fico e Tecnol?gico (CNPq). Logistical and scientific support is acknowledged by the Forest Management laboratory (LMF), Climate and Environment (CLIAMB), and Large Scale Biosphere-Atmosphere (LBA) programs at the National Institute for Amazon Research (INPA).

Keywords

  • chlorophyll fluorescence
  • electron transport rates
  • fosmidomycin
  • global warming
  • high temperature stress
  • isoprene energetic requirements
  • leaf gas exchange
  • net photosynthesis

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