Intracellular position of mitochondria in mesophyll cells differs between C3 and C4 grasses
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.
KeywordsC3 plant C3–C4 intermediate plant C4 plant Mesophyll cell Mitochondrion Photorespiration
This study was supported by the Japan Society for the Promotion of Science KAKENHI (Grant Number 15K14638) to O.U. We thank the National Institute of Agrobiological Resources, Tsukuba, Japan, and the Plant Introduction Station, Agricultural Research Service, USDA, for their kind gifts of seeds.
- Bauwe H (2011) Photorespiration: the bridge to C4 photosynthesis. In: Raghavendra AS, Sage RF (eds) C4 photosynthesis and related CO2 concentrating mechanisms. Springer, Heidelberg-Berlin, pp 81–108Google Scholar
- Buchner O, Moser T, Karadar M, Roach T, Kranner I, Holzinger A (2015) Formation of chloroplast protrusions and catalase activity in alpine Ranunculus glacialis under elevated temperature and different CO2/O2 ratios. Protoplasma 252:1613–1619. doi: 10.1007/s00709-015-0778-5 CrossRefPubMedPubMedCentralGoogle Scholar
- Carolin RC, Jacobs SWL, Vesk M (1975) Leaf structure in Chenopodiaceae. Bot Jahrb Syst 95:226–255Google Scholar
- Carolin RC, Jacobs SWL, Vesk M (1977) The ultrastructure of Kranz cells in the family Cyperaceae. Bot Gaz 138:413–419. http://www.jstor.org/stable/2473873
- Duvall MR, Saar DE, Grayburn WS, Holbrook GP (2003) Complex transitions between C3 and C4 photosynthesis during the evolution of Paniceae: a phylogenetic case study emphasizing the position of Steinchisma hians (Poaceae), a C3–C4 intermediate. Int J Plant Sci 164:949–958. doi: 10.1086/378657 CrossRefGoogle Scholar
- Edwards GE, Ku MSB (1987) Biochemistry of C3–C4 intermediates. In: Hatch MD, Boardman NK (eds) The biochemistry of plants, vol 10, Photosynthesis. Academic Press, San Diego, pp 275–325Google Scholar
- Edwards GE, Voznesenskaya EV (2011) C4 photosynthesis: Kranz forms and single-cell C4 in terrestrial plants. In: Raghavendra AS, Sage RF (eds) C4 photosynthesis and related CO2 concentrating mechanisms. Springer, Heidelberg-Berlin, pp 29–61Google Scholar
- Kanai R, Kashiwagi M (1975) Panicum milioides, a Gramineae plant having Kranz leaf anatomy without C4 photosynthesis. Plant Cell Physiol 16:669–679Google Scholar
- Ku SB, Edwards GE, Kanai R (1976) Distribution of enzymes related to C3 and C4 pathway of photosynthesis between mesophyll and bundle sheath cells of Panicum hians and Panicum milioides. Plant Cell Physiol 17:615–620Google Scholar
- Marshall DM, Muhaidat R, Brown NJ, Liu Z, Stanley S, Griffiths, Sage RF, Hibberd JM (2007) Cleome, a genus closely related to Arabidopsis, contains species spanning a developmental progression from C3 to C4 photosynthesis. Plant J 51:886–896. doi: 10.1111/j.1365-313X.2007.03188.x CrossRefPubMedGoogle Scholar