Abstract
Photorespiration, an essential component of plant metabolism, is concerted across four subcellular compartments, namely, chloroplast, peroxisome, mitochondrion, and the cytoplasm. It is unclear how the pathway located in different subcellular compartments respond to stress occurring exclusively in one of those. We attempted to assess the inter-organelle interaction during the photorespiratory pathway. For that purpose, we induced oxidative stress by menadione (MD) in mitochondria and photo-oxidative stress (high light) in chloroplasts. Subsequently, we examined the changes in selected photorespiratory enzymes, known to be located in other subcellular compartments. The presence of MD upregulated the transcript and protein levels of five chosen photorespiratory enzymes in both normal and high light. Peroxisomal glycolate oxidase and catalase activities increased by 50% and 25%, respectively, while chloroplastic glycerate kinase and phosphoglycolate phosphatase increased by ~30%. The effect of MD was maximum in high light, indicating photo-oxidative stress was an influential factor to regulate photorespiration. Oxidative stress created in mitochondria caused a coordinative upregulation of photorespiration in other organelles. We provided evidence that reactive oxygen species are important signals for inter-organelle communication during photorespiration. Thus, MD can be a valuable tool to modulate the redox state in plant cells to study the metabolic consequences across membranes.
Highlights
Photosynthesis in higher plants is affected by abiotic stress such as oxidative conditions and high light (HL) intensities
Our work demonstrated the importance of mitochondrial metabolism in protecting photosynthesis against photoinhibition
reactive oxygen species (ROS) produced in either chloroplasts (HL-stress) or mitochondria could move across the cell, modulating enzymes in other organelles, including peroxisomes and chloroplasts
Summary
Photosynthesis in higher plants is affected by abiotic stress such as oxidative conditions and high light (HL) intensities. Prolonged exposure to such stress can damage the photosynthetic apparatus, PSII, resulting in photoinhibition [1,2,3]. Plants try to protect photosynthesis against photoinhibition by operating different compartments of their cells [4]. In addition to dark mitochondrial respiration, photorespiration is acknowledged to be a protective mechanism against photoinhibition, as indicated by the classic work on photorespiratory mutants [9,10,11]. The coordination of photorespiratory metabolism between mitochondria and peroxisomes was demonstrated in vitro reconstructed systems [17]
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