Interdependence of photosynthesis and respiration in plant cells: interactions between chloroplasts and mitochondria

Abstract

Photosynthesis and respiration in an illuminated plant cell are not only interdependent but also mutually beneficial. Respiratory rates increase after hours of illumination due to carbohydrate (substrate) accumulation. Besides such long-term effects, photosynthesis and respiration interact even during short illumination periods of a few minutes. The rate of respiration in isolated leaf protoplasts increases severalfold after 10-15 min of illumination. Such light-enhanced dark respiration (LEDR) has been demonstrated in protoplasts as well as in leaves. The stimulation of LEDR by bicarbonate and its sensitivity to inhibitors of photosynthesis (DCMU) or the Calvin cycle (D,L-glyceraldehyde point out the importance of photosynthetic carbon metabolism for respiration. From metabolite analyses of protoplasts, the majority of LEDR is due to mitochondrial oxidation of malate produced by chloroplasts. Simultaneous measurements of photosynthesis and respiration, using mass spectrometry, demonstrate that mitochondrial TCA cycle-based CO₂ evolution is inhibited by illumination while O₂ uptake is either unaffected or stimulated. The marked sensitivity of photosynthesis in leaves or protoplasts to classic mitochondrial inhibitors such as oligomycin, sodium azide or antimycin A implies that mitochondrial metabolism is essential for photosynthesis. Respiration not only benefits photosynthesis but also protects illuminated leaf protoplasts against photoinhibition. Oxidative electron transport and phosphorylation play a much more important role than the reactions of glycolysis and the TCA cycle in this beneficial interaction. The metabolite shuttles involving PGA-DHAP and/or OAA-malate across the chloroplast and mitochondrial membranes could form the biochemical basis of the interaction between photosynthesis and respiration. Alternatively, cytosolic NAD(P)H, derived from photosynthetic products, can be directly acted upon by the mitochondrial external NAD(P)H dehydrogenase and oxidised through the mitochondrial electron transport system. Mitochondrial oxidation of NAD(P)H (even if indirect) helps to prevent the over-reduction of the cytosol and, consequently, the chloroplast in illuminated leaf cells. Besides the direct interaction with chloroplasts, mitochondria can supply reducing equivalents through malate to peroxisomes during photorespiration and provide citrate as the precursor of oxoglutarate, necessary for glutamine and glutamate formation. These two phenomena further complement the strong interdependence of photosynthesis and mitochondrial metabolism.