Photorespiration maintains carbon recycling efficiency at low irradiance despite impaired glycolate/glycerate antiport or hydroxypyruvate reduction

Authors: Walker, Berkley; South, Paul; Ort, Donald

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/12/2016
Publication Date: 6/1/2016
Citation: Walker, B.J., South, P.F., Ort, D.R. 2016. Photorespiration maintains carbon recycling efficiency at low irradiance despite impaired glycolate/glycerate antiport or hydroxypyruvate reduction. Plant Physiology. 129(1):93-103.

Interpretive Summary: Plants use carbon dioxide from the atmosphere to grow and produce our food, fuel, and fiber through the process of photosynthesis. The first reaction of photosynthesis is supposed to involve carbon dioxide, but occasional this reaction takes place with atmospheric oxygen, which produces a compound that the plant can not readily use. Plants recycle this compound to something they can use through a process called photorespiration. Photorespiration is not perfect at this recycling and some plants lose carbon dioxide from photorespiration at 30% of the rates of net carbon dioxide uptake. While the biochemistry of photorespiration is thought to be well-understood, it is unclear how it impacts net photosynthesis. This research uses mutant plants with impaired photorespiration to determine how photorespiration interacts with photosynthesis. We determined that despite major disruption to photorespiration, plants are able to fix carbon dioxide at similar rates as long as the rate of photorespiration is small. When rates of photorespiration are higher, photorespiration appears to impact photosynthesis via feedback mechanisms. This research is important for understanding a significant limitation to the growth of many crop plants. Additionally, this research may aid future efforts to increase the efficiency of crop plants by re-engineering photorespiratory metabolism.

Technical Abstract: Photorespiration partially recycles fixed carbon that would otherwise be lost following the oxygenation reaction of Ribulose, 1-5, carboxylase oxygenase (Rubisco) and significantly reduces net photosynthesis in C3 plants. The recycling of photorespiratory C2 to C3 intermediates is not perfectly efficient, and can further decrease in efficiency when photorespiration is genetically disrupted as in plants lacking peroxisomal hydroxypyruvate activity (hprpmdh1pmdh2). It is not clear if photorespiratory efficiency decreases in other photorespiratory mutants in all situations or if it is the primary cause of decreases in net photosynthesis found in photorespiratory mutants. To determine under what conditions decreases in photorespiratory efficiency impact net photosynthesis, we probed the quantum efficiency and biochemistry of CO2 fixation in hprpmdh1pmdh2 and plants missing PLGG1, the recently identified plastidic glycolate/glycerate antiporter. Surprisingly, we found that the quantum efficiency of CO2 fixation as measured under low irradiances was the same between wild type, plgg1-1, and hprpmdh1pmdh2, despite a modeled predicted decrease of 40% under low CO2. At moderate irradiances, hprpmdh1pmdh2 had decreased rates of net photosynthesis and a higher photocompensation point, but plgg1-1 was similar to wild type. At high irradiances plgg1-1 had decreased net photosynthesis, which was explained by decreases in Rubisco activity and photoinhibition. We conclude that photorespiration can proceed at full efficiencies at low irradiances when rates of Rubisco oxygenation are minimal despite major genetic disruption through alternative pathways. As rates of Rubisco oxygenation increase, photorespiration may then impact net CO2 fixation through decreases in efficiency and downregulation or damage to Rubisco activity and light energy conversion.