Mitochondrial Respiration in Relation to Photosynthetic C4 Acid Decarboxylation in C4 Species

Abstract

Certain respiratory features of bundle sheath cells isolated from the C4 species Urochloa panicoides (phosphoenolpyruvate carboxykinase (PCK)-type)), Panicum miliaceum (NAD malic enzyme (NAD-ME)-type) and Zea mays (NADP malic enzyme (NADP-ME)-type) were examined in relation to the requirements of the C4 acid decarboxylation step of C4 photosynthesis. Cells from both PCK-type and NAD-ME-type species showed high rates of malate-dependent respiration; with ADP or uncoupler the rates were in the range 2-3 μatom O min-1 mg-1 chlorophyll, about 5-10-times the rates with other respiratory substrates. Studies with inhibitors of cytochrome oxidase and the alternative oxidase indicated negligible alternative oxidase-mediated malate respiration in cells from Z. mays, a minor contribution in U. panicoides cells, but possibly a major role for this oxidase in the respiration of P. miliaceum cells. These differences were related to the different roles of respiration in photosynthetic C4 acid decarboxylation. Oxaloacetate strongly suppressed malate-dependent respiration in P. miliaceum bundle sheath cells but not in U. panicoides cells. This difference in the response to oxaloacetate was not due to different kinetic features of the mitochondrial malate dehydrogenase but was apparently largely due to the much lower activity of the enzyme in U. panicoides bundle sheath mitochondria. We propose that insensitivity of respiration to oxaloacetate in bundle sheath cells of PCK-type species may be essential for maintaining the C4 acid decarboxylation process. The reverse may be true for NAD-ME- type species.