Abstract
Flaveria bidentis, a C4 dicot, was transformed with sorghum (a monocot) cDNA clones encoding NADP-malate dehydrogenase (NADP-MDH; EC 1.1.1.82) driven by the cauliflower mosaic virus 35S promoter. Although these constructs were designed for over-expression, many transformants contained between 5 and 50% of normal NADP-MDH activity, presumably by cosense suppression of the native gene. The activities of a range of other photosynthetic enzymes were unaffected. Rates of photosynthesis in plants with less than about 10% of normal activity were reduced at high light and at high [CO2], but were unaffected at low light or at [CO2] below about 150 [mu]L L-1. The large decrease in maximum activity of NADP-MDH was accompanied by an increase in the activation state of the enzyme. However, the activation state was unaffected in plants with 50% of normal activity. Metabolic flux control analysis of plants with a range of activities demonstrates that this enzyme is not important in regulating the steady-state flux through C4 photosynthesis in F. bidentis. Cosense suppression of gene expression was similarly effective in both the mesophyll and bundle-sheath cells. Photosynthesis of plants with very low activity of NADP-MDH in the bundle-sheath cells was only slightly inhibited, suggesting that the presence of the enzyme in this compartment is not essential for supporting maximum rates of photosynthesis.
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- Ashton A. R., Hatch M. D. Regulation of C4 photosynthesis: physical and kinetic properties of active (dithiol) and inactive (disulfide) NADP-malate dehydrogenase from Zea mays. Arch Biochem Biophys. 1983 Dec;227(2):406–415. doi: 10.1016/0003-9861(83)90470-8. [DOI] [PubMed] [Google Scholar]
- Brusslan J. A., Tobin E. M. Isolation of new promoter-mediated co-suppressed lines in Arabidopsis thaliana. Plant Mol Biol. 1995 Feb;27(4):809–813. doi: 10.1007/BF00020233. [DOI] [PubMed] [Google Scholar]
- Flavell R. B. Inactivation of gene expression in plants as a consequence of specific sequence duplication. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3490–3496. doi: 10.1073/pnas.91.9.3490. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Furbank R. T., Chitty J. A., Von Caemmerer S., Jenkins CLD. Antisense RNA Inhibition of RbcS Gene Expression Reduces Rubisco Level and Photosynthesis in the C4 Plant Flaveria bidentis. Plant Physiol. 1996 Jul;111(3):725–734. doi: 10.1104/pp.111.3.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Furbank R. T., Taylor W. C. Regulation of Photosynthesis in C3 and C4 Plants: A Molecular Approach. Plant Cell. 1995 Jul;7(7):797–807. doi: 10.1105/tpc.7.7.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gallardo F., Miginiac-Maslow M., Sangwan R. S., Decottignies P., Keryer E., Dubois F., Bismuth E., Galvez S., Sangwan-Norreel B., Gadal P. Monocotyledonous C4 NADP(+)-malate dehydrogenase is efficiently synthesized, targeted to chloroplasts and processed to an active form in transgenic plants of the C3 dicotyledon tobacco. Planta. 1995;197(2):324–332. doi: 10.1007/BF00202654. [DOI] [PubMed] [Google Scholar]
- Hatch M. D., Agostino A. Bilevel disulfide group reduction in the activation of c(4) leaf nicotinamide adenine dinucleotide phosphate-malate dehydrogenase. Plant Physiol. 1992 Sep;100(1):360–366. doi: 10.1104/pp.100.1.360. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hudson G. S., Evans J. R., von Caemmerer S., Arvidsson Y. B., Andrews T. J. Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiol. 1992 Jan;98(1):294–302. doi: 10.1104/pp.98.1.294. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Issakidis E., Miginiac-Maslow M., Decottignies P., Jacquot J. P., Crétin C., Gadal P. Site-directed mutagenesis reveals the involvement of an additional thioredoxin-dependent regulatory site in the activation of recombinant sorghum leaf NADP-malate dehydrogenase. J Biol Chem. 1992 Oct 25;267(30):21577–21583. [PubMed] [Google Scholar]
- Issakidis E., Saarinen M., Decottignies P., Jacquot J. P., Crétin C., Gadal P., Miginiac-Maslow M. Identification and characterization of the second regulatory disulfide bridge of recombinant sorghum leaf NADP-malate dehydrogenase. J Biol Chem. 1994 Feb 4;269(5):3511–3517. [PubMed] [Google Scholar]
- Jacquot J. P., Gadal P., Nishizawa A. N., Yee B. C., Crawford N. A., Buchanan B. B. Enzyme regulation in C4 photosynthesis: mechanism of activation of NADP-malate dehydrogenase by reduced thioredoxin. Arch Biochem Biophys. 1984 Jan;228(1):170–178. doi: 10.1016/0003-9861(84)90058-4. [DOI] [PubMed] [Google Scholar]
- Johnson H. S., Hatch M. D. Properties and regulation of leaf nicotinamide-adenine dinucleotide phosphate-malate dehydrogenase and 'malic' enzyme in plants with the C4-dicarboxylic acid pathway of photosynthesis. Biochem J. 1970 Sep;119(2):273–280. doi: 10.1042/bj1190273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Landsmann J., Llewellyn D., Dennis E. S., Peacock W. J. Organ regulated expression of Parasponia andersonii haemoglobin gene in transgenic tobacco plants. Mol Gen Genet. 1988 Sep;214(1):68–73. doi: 10.1007/BF00340181. [DOI] [PubMed] [Google Scholar]
- Lazo G. R., Stein P. A., Ludwig R. A. A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Biotechnology (N Y) 1991 Oct;9(10):963–967. doi: 10.1038/nbt1091-963. [DOI] [PubMed] [Google Scholar]
- Lindbo J. A., Silva-Rosales L., Proebsting W. M., Dougherty W. G. Induction of a Highly Specific Antiviral State in Transgenic Plants: Implications for Regulation of Gene Expression and Virus Resistance. Plant Cell. 1993 Dec;5(12):1749–1759. doi: 10.1105/tpc.5.12.1749. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luchetta P., Crétin C., Gadal P. Organization and expression of the two homologous genes encoding the NADP-malate dehydrogenase in Sorghum vulgare leaves. Mol Gen Genet. 1991 Sep;228(3):473–481. doi: 10.1007/BF00260642. [DOI] [PubMed] [Google Scholar]
- Mate C. J., Hudson G. S., von Caemmerer S., Evans J. R., Andrews T. J. Reduction of ribulose biphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose biphosphate carboxylase carbamylation and impairs photosynthesis. Plant Physiol. 1993 Aug;102(4):1119–1128. doi: 10.1104/pp.102.4.1119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McGonigle B., Nelson T. C4 isoform of NADP-malate dehydrogenase. cDNA cloning and expression in leaves of C4, C3, and C3-C4 intermediate species of Flaveria. Plant Physiol. 1995 Jul;108(3):1119–1126. doi: 10.1104/pp.108.3.1119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Napoli C., Lemieux C., Jorgensen R. Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans. Plant Cell. 1990 Apr;2(4):279–289. doi: 10.1105/tpc.2.4.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rebeille F., Hatch M. D. Regulation of NADP-malate dehydrogenase in C4 plants: relationship among enzyme activity, NADPH to NADP ratios, and thioredoxin redox states in intact maize mesophyll chloroplasts. Arch Biochem Biophys. 1986 Aug 15;249(1):171–179. doi: 10.1016/0003-9861(86)90572-2. [DOI] [PubMed] [Google Scholar]
- Russel M., Model P. The role of thioredoxin in filamentous phage assembly. Construction, isolation, and characterization of mutant thioredoxins. J Biol Chem. 1986 Nov 15;261(32):14997–15005. [PubMed] [Google Scholar]
- Shure M., Wessler S., Fedoroff N. Molecular identification and isolation of the Waxy locus in maize. Cell. 1983 Nov;35(1):225–233. doi: 10.1016/0092-8674(83)90225-8. [DOI] [PubMed] [Google Scholar]
- Vanlerberghe G. C., Vanlerberghe A. E., McIntosh L. Molecular Genetic Alteration of Plant Respiration (Silencing and Overexpression of Alternative Oxidase in Transgenic Tobacco). Plant Physiol. 1994 Dec;106(4):1503–1510. doi: 10.1104/pp.106.4.1503. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van der Krol A. R., Mur L. A., Beld M., Mol J. N., Stuitje A. R. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell. 1990 Apr;2(4):291–299. doi: 10.1105/tpc.2.4.291. [DOI] [PMC free article] [PubMed] [Google Scholar]