Journal of Plant Research

, Volume 130, Issue 5, pp 885–892 | Cite as

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

Regular Paper

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.

Keywords

C3 plant C3–C4 intermediate plant C4 plant Mesophyll cell Mitochondrion Photorespiration 

Supplementary material

10265_2017_947_MOESM1_ESM.pdf (464 kb)
Supplementary material 1 (PDF 463 KB)

References

  1. 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
  2. Bourett TM, Czymmek KJ, Howard RJ (1999) Ultrastructure of chloroplast protuberances in rice leaves preserved by high pressure freezing. Planta 208:472–479. doi:10.1007/s004250050584 CrossRefGoogle Scholar
  3. Brown RH, Brown WV (1975) Photosynthetic characteristics of Panicum milioides, a species with reduced photorespiration. Crop Sci 15:681–685. doi:10.2135/cropsci1975.0011183X001500050020x CrossRefGoogle Scholar
  4. Bruhl JJ, Perry S (1995) Photosynthetic pathway-related ultrastructure of C3, C4 and C3–C4 intermediate sedges (Cyperaceae), with special reference to Eleocharis. Aust J Plant Physiol 22:521–530 doi:10.1071/PP9950521 CrossRefGoogle Scholar
  5. 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
  6. Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ 36:200–212. doi:10.1111/j.1365-3040.2012.02567.x CrossRefPubMedGoogle Scholar
  7. Carolin RC, Jacobs SWL, Vesk M (1973) Structure of cells of mesophyll and parenchymatous bundle sheath of Gramineae. Bot J Linn Soc 66:259–275. doi:10.1111/j.1095-8339.1973.tb02174.x CrossRefGoogle Scholar
  8. Carolin RC, Jacobs SWL, Vesk M (1975) Leaf structure in Chenopodiaceae. Bot Jahrb Syst 95:226–255Google Scholar
  9. 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
  10. Carolin RC, Jacobs SWL, Vesk M (1978) Kranz cells and mesophyll in the Chenopodiales. Aust J Bot 26:683–698 doi:10.1071/BT9780683 CrossRefGoogle Scholar
  11. Dengler NG, Nelson T (1999) Leaf structure and development in C4 plants. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, San Diego, pp 133–172CrossRefGoogle Scholar
  12. 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
  13. 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
  14. 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
  15. Edwards GE, Franceschi VR, Ku MSB, Voznesenskaya EV, Pyankov VI, Andreo CS (2001) Compartmentation of photosynthesis in cells and tissues of C4 plants. J Exp Bot 52:577–590. doi:10.1093/jexbot/52.356.577 PubMedGoogle Scholar
  16. GPWG II (Grass Phylogeny Working Group II) (2012) New grass phylogeny resolve***s deep evolutionary relationships and discovers C4 origins. New Phytol 193:304–312. doi:10.1111/j.1469-8137.2011.03972.x CrossRefGoogle Scholar
  17. Gray JC, Sullivan JA, Hibberd JM, Hanson MR (2001) Stromules: mobile protrusions and interconnections between plastids. Plant Biol 3:223–233. doi:10.1055/s-2001-15204 CrossRefGoogle Scholar
  18. Hanson MR, Sattarzadeh A (2011) Stromules: recent insights into a long neglected feature of plastid morphology and function. Plant Physiol 155:1486–1492. doi:10.1104/pp.110.170852 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hatakeyama Y, Ueno O (2016) Intracellular position of mitochondria and chloroplasts in bundle sheath and mesophyll cells of C3 grasses in relation to photorespiratory CO2 loss. Plant Prod Sci 19:540–551 doi:10.1080/1343943X.2016.1212667 CrossRefGoogle Scholar
  20. Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895:81–106. doi:10.1016/S0304-4173(87)80009-5 CrossRefGoogle Scholar
  21. Hattersley PW, Browning AJ (1981) Occurrence of the suberized lamella in leaves of grasses of different photosynthetic types. I. In parenchymatous bundle sheaths and PCR (“Kranz”) sheaths. Protoplasma 109:371–401. doi:10.1007/BF01287454 CrossRefGoogle Scholar
  22. Hattersley PW, Watson L, Osmond CB (1977) In situ immunofluorescent labelling of ribulose-1,5-bisphosphate carboxylase in leaves of C3 and C4 plants. Aust J Plant Physiol 4:523–539. 10.1071/PP9770523 CrossRefGoogle Scholar
  23. Hylton CH, Rawsthorne S, Smith AM, Jones DA, Woolhouse HW (1988) Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C3-C4 intermediate species. Planta 175:452–459. doi:10.1007/BF00393064 CrossRefPubMedGoogle Scholar
  24. Kanai R, Kashiwagi M (1975) Panicum milioides, a Gramineae plant having Kranz leaf anatomy without C4 photosynthesis. Plant Cell Physiol 16:669–679Google Scholar
  25. Khoshravesh R, Stinson CR, Stata M et al (2016) C3–C4 intermediacy in grasses: organelle enrichment and distribution, glycine decarboxylase expression, and the rise of C2 photosynthesis. J Exp Bot 67:3065–3078. doi:10.1093/jxb/erw150 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kim I, Fisher DG (1990) Structural aspects of the leaves of seven species of Portulaca growing in Hawaii. Can J Bot 68:1803–1811. doi:10.1139/b90-233 CrossRefGoogle Scholar
  27. 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
  28. Lundgren MR, Osborne CP, Christin P-A (2014) Deconstructing Kranz anatomy to understand C4 evolution. J Exp Bot 65:3357–3369. doi:10.1093/jxb/eru186 CrossRefPubMedGoogle Scholar
  29. 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
  30. McKown AD, Dengler NG (2007) Key innovations in the evolution of Kranz anatomy and C4 vein pattern in Flaveria (Asteraceae). Amer J Bot 94:382–399. doi:10.3732/ajb.94.3.382 CrossRefGoogle Scholar
  31. Moser T, Holzinger A, Buchner O (2015) Chloroplast protrusions in leaves of Ranunculus glacialis L. respond significantly to different ambient conditions, but are not related to temperature stress. Plant Cell Environ 38:1347–1356. doi:10.1111/pce.12483 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ohnishi J, Kanai R (1983) Differentiation of photorespiratory activity between mesophyll and bundle sheath cells of C4 plants. I. Glycine oxidation by mitochondria. Plant Cell Physiol 24:1411–1420CrossRefGoogle Scholar
  33. Prendergast HDV, Hattersley PW, Stone NE, Lazarides M (1986) C4 acid decarboxylation type in Eragrostis (Poaceae): patterns of variation in chloroplast position, ultrastructure and geographical distribution. Plant Cell Environ 9:333–344. doi:10.1111/1365-3040.ep11611719 Google Scholar
  34. Prendergast HDV, Hattersley PW, Stone NE (1987) New structural/biochemical associations in leaf blades of C4 grasses (Poaceae). Aust J Plant Physiol 14:403–420. doi:10.1071/PP9870403 CrossRefGoogle Scholar
  35. Rawsthorne S (1992) C3–C4 intermediate photosynthesis: linking physiology to gene expression. Plant J 2:267–274. doi:10.1111/j.1365-313X.1992.00267.x CrossRefGoogle Scholar
  36. Sage RF, Khoshravesh R (2016) Passive CO2 concentration in higher plants. Curr Opin Plant Biol 31:58–65. doi:10.1016/j.pbi.2016.03.016 CrossRefPubMedGoogle Scholar
  37. Sage TL, Sage RF (2009) The functional anatomy of rice leaves: implications for refixation of photorespiratory CO2 and efforts to engineer C4 photosynthesis into rice. Plant Cell Physiol 50:756–772. doi:10.1093/pcp/pcp033 CrossRefPubMedGoogle Scholar
  38. Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol 63:19–47. doi:10.1146/annurev-arplant-042811-105511 CrossRefPubMedGoogle Scholar
  39. Schlüter U, Weber APM (2016) The road to C4 photosynthesis: evolution of a complex trait via intermediary states. Plant Cell Physiol 57:881–889. doi:10.1093/pcp/pcw009 CrossRefPubMedGoogle Scholar
  40. Schulze S, Westhoff P, Gowik U (2016) Glycine decarboxylase in C3, C4 and C3–C4 intermediate species. Curr Opin Plant Biol 31:29–35. doi:10.1016/j.pbi.2016.03.011 CrossRefPubMedGoogle Scholar
  41. Stata M, Sage TL, Rennie TD et al (2014) Mesophyll cells of C4 plants have fewer chloroplasts than those of closely related C3 plants. Plant Cell Environ 37:2587–2600. doi:10.1111/pce.12331 CrossRefPubMedGoogle Scholar
  42. Stata M, Sage TL, Hoffmann N et al (2016) Mesophyll chloroplast investment in C3, C4 and C2 species of the genus Flaveria. Plant Cell Physiol 57:904–918. doi:10.1093/pcp/pcw015 CrossRefPubMedGoogle Scholar
  43. Terashima I, Hanba YT, Tholen D, Niinemets Ü (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiol 155:108–116. doi:10.1104/pp.110.165472 CrossRefPubMedGoogle Scholar
  44. Ueno O (1998) Immunogold localization of photosynthetic enzymes in leaves of various C4 plants, with particular reference to pyruvate, orthophosphate dikinase. J Exp Bot 49:1637–1646. doi:10.1093/jxb/49.327.1637 CrossRefGoogle Scholar
  45. Ueno O (2011) Structural and biochemical characterization of the C3-C4 intermediate Brassica gravinae and relatives, with particular reference to cellular distribution of Rubisco. J Exp Bot 62:5347–5355. doi:10.1093/jxb/err187 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Ueno O, Takeda T, Maeda E (1988) Leaf ultrastructure of C4 species possessing different Kranz anatomical types in the Cyperaceae. Bot Mag Tokyo 101:141–152. doi:10.1007/BF02488891 CrossRefGoogle Scholar
  47. Ueno O, Bang SW, Wada Y et al (2003) Structural and biochemical dissection of photorespiration in hybrids differing in genome constitution between Diplotaxis tenuifolia (C3–C4) and radish (C3). Plant Physiol 132:1550–1559 doi:10.1104/pp.103.021329 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Voznesenskaya EV, Koteyeva NK, Chuong SDX, Ivanova AN, Barroca J, Craven LA, Edwards GE (2007) Physiological, anatomical and biochemical characterization of photosynthetic types in genus Cleome (Cleomaceae). Funct Plant Biol 34:247–267. 10.1071/FP06287 CrossRefGoogle Scholar
  49. Voznesenskaya EV, Koteyeva NK, Edwards GE, Ocampo G (2010) Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3–C4 intermediate in genus Portulaca L. (Portulacaceae). J Exp Bot 61:3647–3662. doi:10.1093/jxb/erq178 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Voznesenskaya EV, Koteyeva NK, Edwards GE, Ocampo G (2016) Unique photosynthetic phenotypes in Portulaca (Portulacaceae): C3–C4 intermediates and NAD-ME C4 species with Pilosoid-type Kranz anatomy. J Exp Bot 67. doi:10.1093/jxb/erw393 PubMedCentralGoogle Scholar
  51. Yoshimura Y, Kubota F, Ueno O (2004) Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase. Planta 220:307–317. doi:10.1007/s00425-004-1335-1 CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  1. 1.Graduate School of Bioresources and Bioenvironmental SciencesKyushu UniversityFukuokaJapan
  2. 2.NARO Kyushu Okinawa Agricultural Research CenterFukuokaJapan
  3. 3.Faculty of AgricultureKyushu UniversityFukuokaJapan

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