Comparative analysis of biochemical properties of mesophyll and bundle sheath chloroplasts from various subtypes of C4 plants grown at moderate irradiance
Languages of publication
The photochemical characteristics of mesophyll and bundle sheath chloroplasts isolated from the leaves of C4 species were investigated in Zea mays (NADP-ME type), Panicum miliaceum (NAD-ME type) and Panicum maximum (PEP-CK type) plants. The aim of this work was to gain information about selected photochemical properties of mesophyll and bundle sheath chloroplasts isolated from C4 plants grown in the same moderate light conditions. Enzymatic as well as mechanical methods were applied for the isolation of bundle sheath chloroplasts. In the case of Z. mays and P. maximum the enzymatic isolation resulted in the loss of some thylakoid polypeptides. It was found that the PSI and PSII activities of mesophyll and bundle sheath chloroplasts of all species studied differed significantly and the differences correlated with the composition of pigment-protein complexes, photophosphorylation efficiency and fluorescence emission characteristic of these chloroplasts. This is the first report showing differences in the photochemical activities between mesophyll chloroplasts of C4 subtypes. Our results also demonstrate that mesophyll and bundle sheath chloroplasts of C4 plants grown in identical light conditions differ significantly with respect to the activity of main thylakoid complexes, suggesting a role of factor(s) other than light in the development of photochemical activity in C4 subtypes.
- Andersen KS, Bain JM, Bishop DG, Smillie RM (1972) Photosystem II activity in agranal bundle sheath chloroplasts from Zea mays. Plant Physiol 49: 461-466.
- Anderson JM (1986) Photoregulation of the composition, function and structure of thylakoid membranes. Ann Rev Plant Physiol 37: 93-136.
- Anderson JM, Woo KC, Bordman NK (1971) Photochemical system in mesophyll and bundle sheath chloroplasts of C4> plants. Biochim Biophys Acta 245: 398-408.
- Andersson B, Aro EM (1997) Proteolytic activities and proteases of plant chloroplasts. Physiol Plantarum 100: 780-793.
- Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24: 1-15.
- Bradford M (1976) A rapid and sensitive method for the quantitation of micrograms quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72: 248-254.
- Bassi R, Marquardt J, Lavergne J (1995) Biochemical and functional properties of photosystem II in agranal membranes from maize mesophyll and bundle sheath chloroplasts. Eur J Biochem 233: 709-719.
- Chapman KSR, Hatch MD (1983) Intracellular location of phosphoenolpyruvate carboxykinase and other C4> photosynthetic enzymes in mesophyll and bundle sheath protoplasts of Panicum maximum. Plant Sci Lett 29: 145-154.
- Chapman KSR, Berry JA, Hatch MD (1980) Photosynthetic metabolism in bundle sheath cells of the C4> species Zea mays: sources of ATP and NADPH and the contribution of photosystem II. Arch Biochem Biophys 202: 330-341.
- Dainese P, Hoyer-Hansen G, Bassi R (1990) The resolution of chlorophyll a/b binding proteins by a preparative method based on flat bed isoelectric focusing. Photochem Photobiol 51: 693-703.
- Danahay TG, Staehelin LA, Seibert M, Olgivie PD, Berg SP (1984) Structural, biochemical and biophysical characterization of four oxygen-evolving photosystem II preparation from spinach. Biochim Biophys Acta 764: 179-193.
- Dengler NG, Nelson T (1999) Leaf structure and development in C4> plants. In C4 Plant Biology (Sage RF, Monson RK, eds) pp 133-172. Academic Press, New York.
- Downton WJS, Pyliotis NA (1971) Loss of photosystem II during ontogeny of sorghum bundle sheath chloroplasts. Can J Bot 49: 179-180.
- Edwards GE, Huber SC (1981) The C4> pathway. In The biochemistry of Plants, Photosynthesis (Hatch MD, Boardman NK, eds) vol 8, pp 237-281. Academic Press.
- Edwards GE, Walker D (1983) C3>, C4>: Mechanisms, and Cellular and Environmental Regulation of Photosynthesis. Blackwell Scientific, Oxford.
- Edwards GE, Huber SC, Ku SB, Gutierrez M, Rathnam CK, Mayne BC (1976) CO2> Metabolism and Productivity of Plants (Burris RH, Black CC, eds) pp 83-112. Univ. Park Press, Baltimore.
- Edwards GE, Mac Liley R, Hatch MD (1979) Isolation of intact and functional chloroplasts from mesophyll and bundle sheath protoplasts of the C4> plant Panicum miliaceum. Plant Physiol 63: 821-827.
- 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.
- Gardeström P, Wigge B (1988) Influence of photorespiration on ATP/ADP ratios in the chloroplasts, mitochondria, and cytosol, studied by rapid fractionation of barley (Hordeum vulgare) protoplasts. Plant Physiol 88: 69-76.
- Georgakopoulos JH, Sokolenko A, Arkas M, Sofou G, Herrmann RG, Argyroudi-Akoyunoglou JH (2002) Proteolytic activity against the light-harvesting complex and the D1/D2 core proteins of photosystem II in close association to the light-harvesting complex II trimer. Biochim Biophys Acta 1556: 53-64.
- Ghirardi ML, Melis A (1983) Localization of photosynthetic electron transport components in mesophyll and bundle sheath chloroplasts of Zea mays. Arch Biochem Biophys 224: 19-28.
- Haldimann P, Fracheboud Y, Stamp P (1995) Carotenoid composition in Zea mays developed at sub-optimal temperature and different light intensities. Physiol Plant 95: 409-414.
- Hatch MD (1999) C4> photosynthesis: a historical overview. In C4> Plant Biology (Sage RF, Monson RK, eds) pp 17-46. Academic Press, New York.
- Hattersley PW, Watson L (1992) Diversification of photosynthesis. In Grass Evolution and Domestication (Chapman GP, ed) pp 38-116. Cambridge University Press, Cambridge.
- Homann PH, Schmid GH (1967) Photosynthetic reactions of chloroplasts with unusual structures. Plant Physiol 42: 1619-1632.
- Krall JP, Edwards GE, Ku MSB (1991) Quantum yield of photosystem II and efficiency of CO2> fixation in Flaveria (Asteracae) species under varying light and CO2>. Aust J Plant Physiol 18: 369-383.
- Krömer S, Gardeström P, Samuelsson G (1996) Regulation of the supply of cytosolic oxaloacetate for mitochondrial metabolism via phosphoenolpyruvate carboxylase in barley leaf protoplasts. I. The effect of covalent modification on PEPC activity, pH response, and kinetic properties. Biochim Biophys Acta 1289: 343-350.
- Ku MSB, Spalding MH, Edwards GE (1980) Intracellular localization of phosphoenolpyruvate karboxykinase in leaves of C4> and CAM plants. Plant Sci Lett 19: 1-8.
- Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
- Lavergne J, Leci E (1993) Properties of inactive photosystem II centers. Photosynth Res 35: 323-343.
- Leatsch WM (1971) Chloroplasts structural relationships in leaves of C4> plants. In Photosynthesis and Photorespiration (Hatch MD, Osmond CB, Slater RO, eds) pp 323-349. John Wiley and Sons, Inc.
- Leegood R, Crowther D, Walker DA, Hind G (1981) Photosynthetic electron transport in the bundle sheath of maize. FEBS Lett 126: 89-92.
- Maroc J, Trémolièrs A, Garnier J, Guyon D (1987) Oligomeric form of the light-harvesting chlorophyll a +b-protein complex CPII, phosphatidyldiacylglycerol, Δ3-trans-hexadecenoic acid and energy transfer in Chlamydomonas reinhardii, wild type and mutants. Biochim Biophys Acta 893: 91-99.
- Maroco JP, Ku MSB, Furbank RT, Lea PJ, Leegood RC (1998) CO2> and O2> dependence of PSII activity in C4> plants having genetically produced deficiencies in the C3> or C4> cycle. Photosynth Res 58: 91-101.
- Mayne BC, Dee AM, Edwards GE (1974) Photosynthesis in mesophyll protoplasts and bundle sheath cells of various type of C4> plants. III. Fluorescence emission spectra, delayed light emission, and P700 content. Z Pflanzenphysiol 74: 275-291.
- Meierhoff K, Westhoff P (1993) Differential biogenesis of photosystem II in mesophyll and bundle-sheath cells of monocotyledonous NADP-malic enzyme-type C4> plants: the non-stoichiometric abundance of the subunits of photosystem II in the bundle-sheath chloroplasts and translational activity of the plastome-encoded genes. Planta 191: 23-33.
- Metz JG, Kruege RW, Miles D (1984) Chlorophyll-protein complexes of a photosystem II mutant of maize. Evidence that chlorophyll-protein a-2 and a chlorophyll-protein complex derived from a photosystem I antennae system co migrates on polyacrylamide gels. Plant Physiol 75: 238-241.
- Parys E, Romanowska E, Lechowicz W, Poskuta J (1989) Postillumination burst of CO2> in maize and reed grass determined in a closed gas exchange system. Plant Physiol Biochem 27: 27-34.
- Peter GF, Thornber JP (1991) Electrophoretic procedures for fractionating of photosystem I and II pigment-proteins of higher plants and for determination of their subunit composition. Methods Plant Biochem 5: 195-209.
- Pfündel E (1998) Estimating the contribution of photosystem I to total leaf chlorophyll fluorescence. Photosynth Res 56: 185-195.
- Pfündel E, Nagel E, Meister A (1996) Analyzing the light energy distribution in the photosynthetic apparatus of C4> plants using highly purified mesophyll and bundle-sheath thylakoids. Plant Physiol 112: 1055-1070.
- Polya GM, Osmond CB (1972) Photophosphorylation by mesophyll and bundle sheath chloroplasts of C4> plants. Plant Physiol 49: 267-269.
- Romanowska E, Drożak A, Pokorska B, Shiell BJ, Michalski WP (2006) Organization and activity of photosystems in the mesophyll and bundle sheath chloroplasts of maize. J Plant Physiol 163: 607-618.
- Sailaja MV, Rama Das VS (2000) Differential photosynthetic acclimation pattern to limiting growth-irradiance in two types of C4> plants. Photosynthetica 38: 267-273.
- Sarry JE, Montillet JL, Sauvaire Y, Havax M (1994) The protective function of the xanthophyll cycle in photosynthesis. FEBS Lett 353: 147-150.
- Schuster G, Ohad I, Martineau B, Taylor WC (1985) Differentiation and development of bundle sheath and mesophyll thylakoids in maize. Thylakoid polypeptide composition, phosphorylation, and organization of photosystem II. J Biol Chem 260: 11866-11873.
- Sheen J-Y, Bogorad L (1986) Differential expression of six light-harvesting chlorophyll a/b binding protein genes in maize leaf cell types. Proc Natl Acad Sci USA 83: 7811-7815.
- Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354.
- Vainstein A, Ferreira P, Peterson CC, Verbeke JA, Thornber JP (1989) Expression of the major light-harvesting chlorophyll a/b-protein and its import into thylakoids of mesophyll and bundle sheath chloroplasts of maize. Plant Physiol 89: 602-609.
- Watanabe M, Ohnishi J, Kanai R (1984) Intracellular localization of phosphoenolpyruvate carboxykinase in bundle sheath cells of C4> plants. Plant Cell Physiol 25: 69-76.
- Wingler A, Walker RP, Chen Z-H Leegood RC (1999) Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol 120: 539-545.
Publication order reference