Adaptation of plant photosynthetic metabolism to extreme CO2 levels in Yellowstone revealed by in vivo fluorescence dynamics

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Original abstract

Introduction While CO 2 enrichment studies have provided valuable insights into how plants respond to elevated CO 2 levels expected under future climate conditions (up to ~700 ppm), if and how photosynthesis can adapt to more extreme CO 2 levels in nature remains yet unknown. Here, we investigate changes in photosynthetic metabolism in a C3 plant growing near high CO 2 emission sources in Yellowstone National Park, at levels up to 6000 ppm CO 2 . Methods We analyze chlorophyll variable fluorescence emission kinetics to identify changes in the photosynthetic electron transport chain (PETC) between plants adapted to high CO 2 versus control plants growing at ambient CO 2 . By applying short flashes using the Fast Repetition Rate Fluorometry (FRRF) technique we separate photochemical from non-photochemical quenching events. This enables monitoring electron transport from water oxidation within PSII into the downstream carrier pools (Plastoquinone (PQ), Ferrodoxin, and NADP + ) of the PETC and into CO 2 carboxylation within the Calvin Benson-Bassham (CBB) cycle. Results We find that plants growing near the extreme CO 2 sources in Yellowstone are much slower to overcome bottlenecks in the PETC and reach lower photochemical Fv/Fm values indicative of lower photosynthetic efficiency. We observe that these plants require higher CO 2 levels to activate the reactions in the CBB cycle. Discussion We conclude that plants growing near high CO 2 sources are metabolically poised in Cyclic Electron Flow (CEF) at ambient CO 2 concentrations and switch to Linear Electron Flow (LEF) only in high CO 2 . Second, after a brief period of dark time (3–4 minutes), the near-source plants more rapidly restore the PETC bottlenecks, slowing LEF and recovering CEF. This outcome retains electrons in the PQH 2 pool slowing flux into the NADP + pool through LEF and blocking utilization of CO 2 by reactions in the CBB cycle. We explain this adaptive response as a coping mechanism against acidification at high CO 2 growth conditions, which compromises enzymatic activity and proton motive force generation. We conclude that plants adapt to extreme atmospheric CO 2 by further compromising the inefficient CBB cycle and by rerouting electron flux through the PETC from LEF into CEF to stimulate more proton pumping and ATP production.

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