Intracellular position of mitochondria in mesophyll cells differs between C3 and C4 grasses.

Abstract

In C3 plants, part of the CO2 fixed during photosynthesis in chloroplasts is released from mitochondria during photorespiration by decarboxylation of glycine via glycine decarboxylase (GDC), thereby reducing photosynthetic efficiency. The apparent positioning of most mitochondria in the interior (vacuole side of chloroplasts) of mesophyll cells in C3 grasses would increase the efficiency of refixation of CO2 released from mitochondria by ribulose 1,5-bisphosphate carboxylase/​oxygenase (Rubisco) in chloroplasts. Therefore, in mesophyll cells of C4 grasses, which lack both GDC and Rubisco, the mitochondria ought not to be positioned the same way as in C3 mesophyll cells. To test this hypothesis, we investigated the intracellular position of mitochondria in mesophyll cells of 14 C4 grasses of different C4 subtypes and subfamilies (Chloridoideae, Micrairoideae, and Panicoideae) and a C3-C4 intermediate grass, Steinchisma hians, under an electron microscope. In C4 mesophyll cells, most mitochondria were positioned adjacent to the cell wall, which clearly differs from the positioning in C3 mesophyll cells. In S. hians mesophyll cells, the positioning was similar to that in C3 cells. These results suggest that the mitochondrial positioning in C4 mesophyll cells reflects the absence of both GDC and Rubisco in the mesophyll cells and the high activity of phosphoenolpyruvate carboxylase. In contrast, the relationship between the mitochondrial positioning and enzyme distribution in S. hians is complex, but the positioning may be related to the capture of respiratory CO2 by Rubisco. Our study provides new possible insight into the physiological role of mitochondrial positioning in photosynthetic cells.