Abstract
Eleocharis vivipara, a unique leafless amphibious sedge, adopts the C4 mode of photosynthesis under terrestrial conditions and the C3 mode under submerged aquatic conditions. To analyze the molecular basis of these responses to the contrasting environments, we isolated and characterized two full-length cDNAs for a key C4 enzyme, pyruvate, orthophosphate dikinase (PPDK; EC 2.7.9.1). The isogenes for PPDK, designated ppdk1 and ppdk2, were highly homologous to one another but not identical. The PPDK1 protein, deduced from the nucleotide sequence of the cDNA, contained an extra domain at the amino terminus which, presumably, serves as a chloroplast transit peptide, while PPDK2 lacked this extra domain. It seems likely, therefore, that the ppdk1 and ppdk2 genes encode a chloroplastic and a cytosolic PPDK, respectively. Genomic Southern blot analysis revealed the existence of a small family of genes for PPDK in the genome of E. vivipara. Northern blot analysis indicate that both chloroplastic and cytosolic genes for PPDK are expressed simultaneously in the culms, a photosynthetic organ, of E. vivipara and that the pattern of expression of these genes differs between the growth forms.
References
Aoyagi K, Bassham JA: Pyruvate orthophosphate dikinase of C3 seeds and leaves as compared to the enzyme from maize. Plant Physiol 75: 387–392 (1984).
Aoyagi K, Bassham JA: Synthesis and uptake of cytoplasmically synthesized pyruvate Pi dikinase polypeptide by chloroplasts. Plant Physiol 78: 807–811 (1985).
Aoyagi K, Chua N-H: Cell-specific expression of pyruvate, Pi dikinase. In situ mRNA hybridization and immunolocalization labeling of protein in wheat seed. Plant Physiol 86: 364–368 (1988).
Bruchhaus I, Tannich E: Primary structure of the pyruvate phosphate dikinase in Entamoeba histolytica. Mol Biochem Parasitol 62: 153–156 (1993).
Budde RJA, Chollet R: Regulation of enzyme activity in plants by reversible phosphorylation. Physiol Plant 72: 435–439 (1988).
Cushman JC, Meyer G, Michalowski CB, Schmitt JM, Bohnert HJ: Salt stress leads to differential expression of two isogenes of phosphoenolpyruvate carboxylase during crassulacean acid metabolism induction in the common ice plant. Plant Cell 1: 715–725 (1989).
Edwards GE, Nakamoto H, Burnell JN, Hatch MD: Pyruvate, Pi dikinase and NADP-malate dehydrogenase in C4 photosynthesis: properties and mechanism of light/dark regulation. Annu Rev Plant Physiol 36: 255–286 (1985).
Ehleringer JR, Monson RK: Evolutionary and ecological aspects of photosynthetic pathway variation. Annu Rev Ecol Syst 24: 411–439 (1993).
Fiß lthaler B, Meyer G, Bohnert HJ, Schmitt JM: Agedependent induction of pyruvate, orthophosphate dikinase in Mesembryanthemum crystallinum L. Planta 196: 492–500 (1995).
Fromm H, Devic M, Fluhr R, Edelman M: Control of psbA gene expression: in mature Spirodela chloroplasts light regulation of 32-kd protein synthesis is independent of transcript level. EMBO J 4: 291–295 (1985).
Glackin C, Grula JW: Organ-specific transcripts of different size and abundance derive from the same pyruvate, orthophosphate dikinase gene in maize. Proc Natl Acad Sci USA 87: 3004–3008 (1990).
Hague DR, Uhler M, Collins PD: Cloning of cDNA for pyruvate, Pi dikinase from maize leaves. Nucl Acids Res 11: 4853–4865 (1983).
Hata S, Matsuoka M: Immunological studies on pyruvate orthophosphate dikinase in C3 plants. Plant Cell Physiol 28: 635–641 (1987).
Hatch MD: C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895: 81–106 (1987).
Hudspeth RL, Glackin CA, Bonner J, Grula JW: Genomic and cDNA clones for maize phosphoenolpyruvate carboxylase and pyruvate, orthophosphate dikinase: expression of different gene-family members in leaves and roots. Proc Natl Acad Sci USA 83: 2884–2888 (1986).
Ku MSB, Kano-Murakami Y, Matsuoka M: Evolution and expression of C4 photosynthesis genes. Plant Physiol. 111: 947–957 (1996).
Langdale JA, Metzler MC, Nelson T: The argentia mutation delays normal development of photosynthetic cell-types in Zea mays. Devel Biol 122: 243–255 (1987).
Matsuoka M: Structure, genetic mapping, and expression of the gene for pyruvate, orthophosphate dikinase from maize. J Biol Chem. 265: 16 772–16 777 (1990).
Matsuoka M, Ozeki Y, Yamamoto N, Hirano H, Kano-Murakami Y, Tanaka Y: Primary structure of maize pyruvate, orthophosphate dikinase as deduced from cDNA sequence. J Biol Chem 263: 11 080–11 083 (1988).
Murray MG, Thompson WF: Rapid isolation of highmolecular weight plant DNA. Nucl Acids Res 8: 4321–4325 (1980).
Nelson T, Langdale JA: Developmental genetics of C4 photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 43: 25–47 (1992).
Osmond CB, Winter K, Ziegler H: Functional significance of different pathways of CO2 fixation in photosynthesis. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of Plant Physiology, vol. 12B: Physiological Plant Ecology II, pp. 479–547. Springer, Berlin (1982).
Pocalyko DJ, Caroll LJ, Martin BM, Babbitt PC, Dunaway-Mariano D: Analysis of sequence homologies in plant and bacterial pyruvate-phosphate dikinase, enzyme I of bacterial phosphoenolpyryvate:sugar phosphotransferase system and other PEP-utilizing enzymes. Identification of potential catalytic and regulatory motif. Biochemistry 29: 10 757–10 765 (1990).
Rosche E, Streubel M, Westhoff P: Primary structure of the photosynthetic pyruvate orthophosphate dikinase of the C3 plant Flaveria pringlei and expression analysis of pyruvate orthophosphate dikinase sequences in C3, C3-C4 and C4 Flaveria species. Plant Mol Biol 26: 763–769 (1994).
Rosche E, Westhoff P: Primary structure of pyruvate, orthophosphate dikinase in the dicotyledonous C4 plant Flaveria trinervia. FEBS Lett 273: 116–121 (1990).
Rosche E, Westhoff P: Genomic structure and expression of the pyruvate, orthophosphate dikinase gene of the dicotyledonous C4 plant Flaveria trinervia (Asteraceae). Plant Mol Biol 29: 663–678 (1995).
Sheen J: Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell 3: 225–245 (1991).
Sheen JY, Bogorad L: Regulation of levels of nuclear transcripts for C4 photosynthesis in bundle sheath and mesophyll cells of maize leaves. Plant Mol Biol 8: 227–238 (1987).
Sheen JY, Bogorad L: Differential expression of C4 pathway genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem 24: 11 726–11 730 (1987).
Sugiyama T: Purification, molecular, and catalytic properties of pyruvate phosphate dikinase from themaize leaf. Biochemistry 12: 2862–2868 (1973).
Ueno O: Structural characterization of photosynthetic cells in an amphibious sedge, Eleocharis vivipara, in relation to C3 and C4 metabolism. Planta 199: 382–393 (1996).
Ueno O: Immunocytochemical localization of enzymes involved in the C3 and C4 pathways in the photosynthetic cells of an amphibious sedge, Eleocharis vivipara. Planta 199: 394–403 (1996).
Ueno O, Samejima M, Muto S, Miyachi S: Photosynthetic characteristics of an amphibious plant, Eleocharis vivipara: expression of C4 and C3 modes in contrasting environments. Proc Natl Acad Sci USA 85: 6733–6737 (1988).
Usami S, Ohta S, Konami T, Burnell JN: Cold stability of pyruvate, orthophosphate dikinase of Flaveria brownii. Plant Mol Biol 27: 969–980 (1995).
Wagner DB, Furnier GR, Saghai-Maroof MA, Williams SM, Dancik BP, Allard RW: Chloroplast DNA polymorphisms in lodgepole and jack pines and their hybrids. Proc Natl Acad Sci USA 84: 2097–2100 (1987).
Winter K: Crassulacean acid metabolism. In: Barber J, Baker NR (eds) Topics in Photosynthesis, vol 6: Photosynthetic Mechanisms and the Environment, pp. 329–387. Elsevier, Amsterdam (1985).
Wu R, Wu T, Ray A: Adaptors, linkers, and methylation. Meth Enzymol 152: 343–349 (1987).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Agarie, S., Kai, M., Takatsuji, H. et al. Expression of C3 and C4 photosynthetic characteristics in the amphibious plant Eleocharis vivipara: structure and analysis of the expression of isogenes for pyruvate, orthophosphate dikinase. Plant Mol Biol 34, 363–369 (1997). https://doi.org/10.1023/A:1005897118660
Issue Date:
DOI: https://doi.org/10.1023/A:1005897118660