Skip to main content
SpringerLink
Log in

Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

In C4 plants, photorespiration is decreased relative to C3 plants. However, it remains unclear how much photorespiratory capacity C4 leaf tissues actually have. We thoroughly investigated the quantitative distribution of photorespiratory organelles and the immunogold localization of the P protein of glycine decarboxylase (GDC) in mesophyll (M) and bundle sheath (BS) cells of various C4 grass species. Specific differences occurred in the proportions of mitochondria and peroxisomes in the BS cells (relative to the M cells) in photosynthetic tissues surrounding a vein: lower in the NADP-malic enzyme (NADP-ME) species having poorly formed grana in the BS chloroplasts, and higher in the NAD-malic enzyme (NAD-ME) and phosphoenolpyruvate carboxykinase (PCK) species having well developed grana. In all C4 species, GDC was localized mainly in the BS mitochondria. When the total amounts of GDC in the BS mitochondria per unit leaf width were estimated from the immunogold labeling density and the quantity of mitochondria, the BSs of NADP-ME species contained less GDC than those of NAD-ME or PCK species. This trend was also verified by immunoblot analysis of leaf soluble protein. There was a high positive correlation between the degree of granal development (granal index) in the BS chloroplasts and the total amount of GDC in the BS mitochondria. The variations in the structural and biochemical features involved in photorespiration found among C4 species might reflect differences in the O2/CO2 partial pressure and in the potential photorespiratory capacity of the BS cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a–e
Fig. 2
Fig. 3
Fig. 4a–f
Fig. 5
Fig. 6a,b

Similar content being viewed by others

Abbreviations

BS :

Bundle sheath

GDC :

Glycine decarboxylase

M :

Mesophyll

NAD-ME :

NAD-malic enzyme

NADP-ME :

NADP-malic enzyme

PCK :

Phosphoenolpyruvate carboxykinase

References

  • Brown RH, Hattersley PW (1989) Leaf anatomy of C3–C4 species as related to evolution of C4 photosynthesis. Plant Physiol 91:1543–1550

    Google Scholar 

  • Brown RH, Bouton JH, Rigsby L, Rigler M (1983) Photosynthesis of grass species differing in carbon dioxide fixation pathways. VIII. Ultrastructural characteristics of Panicum species in the Laxa group. Plant Physiol 71:425–431

    Google Scholar 

  • Carnal NW, Agostino A, Hatch MD (1993) Photosynthesis in phosphoenolpyruvate carboxykinase-type C4 plants: mechanism and regulation of C4 acid decarboxylation in bundle sheath cells. Arch Biochem Biophys 306:360–367

    Article  CAS  PubMed  Google Scholar 

  • Dai Z, Ku MSB, Edwards GE (1993) C4 photosynthesis: the CO2-concentrating mechanism and photorespiration. Plant Physiol 103:83–90

    CAS  PubMed  Google Scholar 

  • Dai Z, Ku MSB, Edwards GE (1995) C4 photosynthesis: the effects of leaf development on the CO2-concentrating mechanism and photorespiration in maize. Plant Physiol 107:815–825

    CAS  PubMed  Google Scholar 

  • 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 133–172

  • Dengler NG, Dengler RE, Donnelly PM, Hattersley PW (1994) Quantitative leaf anatomy of C3 and C4 grasses (Poaceae): bundle sheath and mesophyll surface area relationships. Ann Bot 73:241–255

    Article  Google Scholar 

  • de Veau EJ, Burris JE (1989) Photorespiratory rates in wheat and maize as determined by 18O-labeling. Plant Physiol 90:500–511

    Google Scholar 

  • Douce R, Heldt H-W (2000) Photorespiration. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: physiology and metabolism. Kluwer, Dordrecht, pp 115–136

  • Edwards GE, Francheschi 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

    Article  CAS  PubMed  Google Scholar 

  • Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112:285–299

    Article  Google Scholar 

  • Ellis RP, Vogel JC, Fuls A (1980) Photosynthetic pathways and the geographical distribution of grasses in South West Africa/Namibia. S Afr J Sci 76:307–314

    Google Scholar 

  • Farineau J, Lelandais M, Morot-Gaudry J-F (1984) Operation of the glycolate pathway in isolated bundle sheath strands of maize and Panicum maximum. Physiol Plant 60:208–214

    CAS  Google Scholar 

  • Frederick SE, Newcomb EH (1971) Ultrastructure and distribution of microbodies in leaves of grasses with and without CO2-photorespiration. Planta 96:152–174

    CAS  Google Scholar 

  • Furbank RT, Badger MR (1982) Oxygen exchange in leaves of C4 plants. Aust J Plant Physiol 9:553–558

    CAS  Google Scholar 

  • Furbank RT, Badger MR (1983) Photorespiratory characteristics of isolated bundle sheath strands of C4 monocotyledons. Aust J Plant Physiol 10:451–458

    CAS  Google Scholar 

  • Gardestrom P, Edwards GE (1985) Leaf mitochondria (C3 + C4 + CAM). In: Douce R, Day DA (eds) Encyclopedia of plant physiology, NS, vol 18, Higher plant cell respiration. Springer, Berlin Heidelberg New York, pp 314–346

  • Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895:81–106

    CAS  Google Scholar 

  • Hattersley PW (1984) Characterization of C4 type leaf anatomy in grasses (Poaceae). Mesophyll: bundle sheath area ratios. Ann Bot 53:163–179

    Google Scholar 

  • Hattersley PW, Browning AJ (1981) Occurrence of the suberized lamella in leaves of grasses of different photosynthetic types. In parenchymatous bundle sheath and PCR (Kranz) sheaths. Protoplasma 109:371–401

    Google Scholar 

  • Hylton CM, 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

    CAS  Google Scholar 

  • Ikeda M (1985) Photosynthetic carbon metabolism in corn leaves treated with methionine sulfoximine and ammonium. Soil Sci Plant Nutr 31:469–474

    CAS  Google Scholar 

  • Kinsman EA, Pyke KA (1998) Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves. Development 125:1815–1822

    CAS  PubMed  Google Scholar 

  • Koroleva OA, Tomos AD, Farrar J, Roberts P, Pollock CJ (2000) Tissue distribution of primary metabolism between epidermal, mesophyll, and parenchymatous bundle sheath cells in barley leaves. Aust J Plant Physiol 27:747–755

    Article  CAS  Google Scholar 

  • Lacuesta ML, Dever LV, Munoz-Rueda, Lea PJ (1997) A study of photorespiratory ammonia production in the C4 plant Amaranthus edulis, using mutants with altered photosynthetic capacities. Physiol Plant 99:447–455

    Article  CAS  Google Scholar 

  • Lawlor DW, Fock H (1978) Photosynthesis, respiration, and carbon assimilation in water-stressed maize at two oxygen concentrations. J Exp Bot 29:579–593

    CAS  Google Scholar 

  • Leegood RC (1997) The regulation of C4 photosynthesis. Adv Bot Res 26:251–316

    CAS  Google Scholar 

  • Leegood RC (2002) C4 photosynthesis: principles of CO2 concentration and prospects for its induction into C3 plants. J Exp Bot 53:581–590

    Article  CAS  PubMed  Google Scholar 

  • Liu AY, Black CC Jr (1972) Glycolate metabolism in mesophyll cells and bundle sheath cells isolated from crabgrass, Digitaria sanguinalis (L.) Scop., leaves. Arch Biochem Biophys 149:269–280

    CAS  PubMed  Google Scholar 

  • Maroco JP, Ku MSB, Lea PJ, Dever LV, Leegood RC, Furbank RT, Edwards GE (1998) Oxygen requirement and inhibition of C4 photosynthesis: an analysis of C4 plants deficient in the C3 and C4 cycles. Plant Physiol 116:823–832

    Article  CAS  PubMed  Google Scholar 

  • Morgan CL, Turner SR, Rawsthorne S (1993) Coordination of the cell-specific distribution of the four subunits of glycine decarboxylase and of serine hydroxymethyltransferase in leaves of C3–C4 intermediate species from different genera. Planta 190:468–473

    CAS  Google Scholar 

  • 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 24:1411–1420

    CAS  Google Scholar 

  • Ohnishi J, Kanai R (1985) Differentiation of photorespiratory activity between mesophyll and bundle sheath cells of C4 plants. II. Peroxisomes of Panicum miliaceum L. Plant Cell Physiol 26:797–803

    CAS  Google Scholar 

  • Ohsugi R, Ueno O, Komatsu T, Sasaki H, Murata T (1997) Leaf anatomy and carbon discrimination in NAD-malic enzyme Panicum species and their hybrids differing in bundle sheath cell ultrastructure. Ann Bot 79:179–184

    Article  CAS  Google Scholar 

  • Oliver DJ (1994) The glycine decarboxylase complex from plant mitochondria. Annu Rev Plant Physiol Plant Mol Biol 45:323–337

    Article  CAS  Google Scholar 

  • Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot 46:1351–1362

    CAS  Google Scholar 

  • Osmond CB, Harris B (1971) Photorespiration during C4 photosynthesis. Biochim Biophys Acta 234:270–282

    Article  CAS  PubMed  Google Scholar 

  • Pfundel E, Neubohn B (1999) Assessing photosystem I and II distribution in leaves from C4 plants using confocal laser scanning microscopy. Plant Cell Environ 22:1569–1577

    Article  CAS  Google Scholar 

  • Popov VN, Dmitrieva EA, Eprintsev AT, Igamberdiev AU (2003) Glycolate oxidase isoforms are distributed between the bundle sheath and mesophyll tissues of maize leaves. J Plant Physiol 160:851–857

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Schulze E-D, Ellis R, Schulze W, Trimborn P, Ziegler H (1996) Diversity, metabolic types and δ13C carbon isotope ratios in the grass flora of Namibia in relation to growth form, precipitation and habitat conditions. Oecologia 106:352–369

    Google Scholar 

  • Ueno O (1996) Structural characterization of photosynthetic cells in an amphibious sedge, Eleocharis vivipara, in relation to C3 and C4 metabolism. Planta 199:382–393

    CAS  Google Scholar 

  • Ueno O (2001) Ultrastructural localization of photosynthetic and photorespiratory enzymes in epidermal, mesophyll, bundle sheath and vascular bundle cells of the C4 dicot Amaranthus viridis. J Exp Bot 52:1003–1013

    Article  CAS  PubMed  Google Scholar 

  • Ueno O, Agarie S (1997) The intercellular distribution of glycine decarboxylase in leaves of cassava in relation to the photosynthetic mode and leaf anatomy. Jpn J Crop Sci 66:268–278

    CAS  Google Scholar 

  • Ueno O, Bang SW, Wada Y, Kondo A, Ishihara K, Kaneko Y, Matsuzawa Y (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

    Article  CAS  PubMed  Google Scholar 

  • Usuda H, Edwards GE (1980) Localization of glycerate kinase and some enzymes for sucrose synthesis in C3 and C4 plants. Plant Physiol 65:1017–1022

    CAS  Google Scholar 

  • Usuda H, Shimogawara K (1994) Induction of the inactivation and degradation of phosphoenolpyruvate carboxylase and ribulose-1,5-bisphosphate carboxylase/oxygenase in maize leaves by freezing and thawing. Plant Cell Physiol 35:363–370

    CAS  Google Scholar 

  • Walker RP, Trevanion SJ, Leegood RC (1995) Phosphoenolpyruvate carboxykinase from higher plants: purification from cucumber and evidence of rapid proteolytic cleavage in extracts from a range of plant tissues. Planta 196:58–63

    CAS  Google Scholar 

  • Wingler A, Lea P, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B 355:1517–1529

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Kubota F, Hirao K (2001) Estimation of photorespiration rate by simultaneous measurements of CO2, gas exchange rate, and chlorophyll fluorescence quenching in the C3 plant Vigna radiata (L.) Wilczek and the C4 plant Amaranthus mongostanus L. Photosynthetica 39:377–382

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. D.J. Oliver for his kind gift of the antiserum against the P protein of GDC. The seeds of Eriachne and Urochloa species were supplied by the USDA National Germplasm Resources Laboratory, Beltsville, Maryland, USA. This study was partly supported by a grant-in-aid to O.U. from the Ministry of Agriculture, Forestry, and Fisheries of Japan (Bio-Design Project).

Author information

Author notes

  1. Yasuyuki Yoshimura

    Present address: National Institute of Agro-Environmental Science, Tsukuba, Ibaraki 305-8604, Japan

Authors and Affiliations

  1. Plant Physiology Department, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan

    Yasuyuki Yoshimura & Osamu Ueno

  2. Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, Hakozaki, Fukuoka 812-8581, Japan

    Yasuyuki Yoshimura & Fumitake Kubota

Authors
  1. Yasuyuki Yoshimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fumitake Kubota
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Osamu Ueno
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Osamu Ueno.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yoshimura, Y., Kubota, F. & Ueno, O. Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase. Planta 220, 307–317 (2004). https://doi.org/10.1007/s00425-004-1335-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1335-1

Keywords

Search

Navigation