Abstract
Cyanobacteria, the closest living relatives of the ancient endosymbiont that gave rise to modern-day chloroplasts, offer a rich source of genes for plant genetic engineering, due to both similarities with and differences from the plant genetic systems. On the one hand, cyanobacteria share many metabolic pathways with plant cells, and especially with chloroplasts, which may be critical when the transgenic product needs to interact with endogenous systems or substrates to exert its function. On the other hand, most mechanisms involved in plant regulation of gene expression have arisen after endosymbiosis, permitting a more rational manipulation of the introduced trait, free from host regulatory networks. In addition, sequence divergence between plant genes and their cyanobacterial orthologues prevents, in most cases, the unwanted consequences of gene silencing and cosuppression. Finally, a few cyanobacterial genes involved in tolerance to environmental and/or nutritional stresses have disappeared from the plant genome during the evolutionary pathway from cyanobacteria to vascular plants, raising the possibility of recovering these adaptive advantages by introducing those lost genes into transgenic plants. In spite of their obvious potential, the use of cyanobacterial genes to engineer plants for increased productivity or stress tolerance has been relatively rare. In this chapter, we review several examples in which this approach has been applied to plant genetic engineering with considerable success. They include modification of central metabolic pathways to improve carbon assimilation and allocation by expressing unregulated cyanobacterial enzymes, development of chilling tolerance by increasing desaturation of membrane-bound fatty acids, pigment manipulation, shifts in light quality perception, production of biodegradable polymers, and synthesis of ketocarotenoids not present in crops. Tolerance to adverse environments could be achieved by the introduction of cyanobacterial genes lost from the plant genome during evolution, such as flavodoxin. The results obtained illustrate the power of gene and data mining in cyanobacterial genomes as a biotechnological tool for the design of transgenic plants with higher productivity, enhanced tolerance to environmental stress, and potential for biofarming.
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References
Boyer, J.S. 1982. Plant productivity and environment. Science 218: 443–448.
Brenner, R.R. 1976. Regulatory function of Δ6 desaturase: key enzyme of polyunsaturated fatty acid synthesis. Adv. Exp. Med. Biol. 83: 85–101.
Casal, J.J., Luccioni, L.G., Oliverio, K.A. and Boccalandro, H.E. 2003. Light, phytochrome signalling and photomorphogenesis in Arabidopsis. Photochem. Photobiol. Sci. 2: 625–636.
Chen, L.M., Omiya, O., Hata, S. and Izui, K. 2002. Molecular characterization of a phosphoenolpyruvate carboxylase from a thermophilic cyanobacterium, Synechococcus vulcanus with unusual allosteric properties. Plant. Cell Physiol. 43: 159–169.
Chen, L.M., Li, K.Z., Miwa, T. and Izui, K. 2004. Overexpression of a cyanobacterial phosphoenolpyruvate carboxylase with diminished sensitivity to feedback inhibition in Arabidopsis changes amino acid metabolism. Planta 219: 440–449.
Chen, Y.M., Ferrar, T.S., Lohmeir-Vogel, E., Morrice, N., Mizuno, Y., Berenger, B., Ng, K.K.S., Muench, D.G. and Moorhead, G.B.G. 2006. The PII signal transduction protein of Arabidopsis thaliana forms and arginine-regulated complex with plastid N -acetyl glutamate kinase. J. Biol. Chem. 281: 5726–5733.
Chida, H., Nakazawa, A., Akazaki, H., Hirano, T., Suruga, K., Ogawa, M., Satoh, T., Kadokura, K., Yamada, S., Hakamata, W., Isobe, K., Ito, T., Ishii, R., Nishio, T., Sonoike, K. and Oku, T. 2007. Expression of the algal cytochrome c 6 gene in Arabidopsis enhances photosynthesis and growth. Plant Cell Physiol. 48: 948–957.
Chin, H.G., Kim, G.D., Marin, I., Mersha, F., Evans, T.C., Chen, L., Xu, M.Q. and Pradhan, S. 2003. Protein trans-splicing in transgenic plant chloroplast: reconstruction of herbicide resistance from split genes. Proc. Natl. Acad. Sci. USA, 100: 4510–4515.
Chollet, R. 1996. Phosphenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 273–298.
Curatti, L., Folco, E., Desplats, P., Abratti, G., Limones, V., Herrera-Estrella, L. and Salerno, G. 1998. Sucrose-phosphate synthase from Synechocystis sp. strain PCC 6803: identification of the spsA gene and characterization of the enzyme expressed in Escherichia coli. J. Bacteriol. 180: 6776–6779.
Cushman, J.C. and Bohnert, H.J. 2000. Genomic approaches to plant stress tolerance. Curr. Opin. Plant Biol. 3: 117–124.
De la Rosa, M.A., Navarro, J.A., Díaz-Quintana, A., de la Cerda, B., Molina-Heredia, F.P., Balme, A., Murdoch, P.S., Díaz-Moreno, I., Durán, R.V. and Hervás, M. 2002. An evolutionary analysis of the reaction mechanisms of photosystem I reduction by cytochrome c (6) and plastocyanin. Bioelectrochem. 55: 41–45.
Erdner, D.L., Price, N.M., Doucette, D.G., Peleato, M.L. and Anderson, D.M. 1999. Characterization of ferredoxin and flavodoxin as markers of iron limitation in marine phytoplankton. Mar. Ecol. Prog. Ser. 184: 43–53.
Fischer, R., Stoger, E., Schillberg, S., Christou, P. and Twyman, R.M. 2004. Plant based production of biopharmaceuticals. Curr. Opin. Plant Biol. 7: 152–158.
Frankenberg, N., Mukougawa, K., Kohchi, T. and Lagarias, J.C. 2001. Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13: 965–978.
Fromme, P., Jordan, P. and Krauss, N. 2001. Structure of photosystem I. Biochim. Biophys. Acta 1507: 5–31.
Frommer, W.B. and Sonnewald, U. 1995. Molecular analysis of carbon partitioning in solanaceous species. J. Exp. Bot. 287: 587–607.
Fukuchi-Mizutani, M., Tasaka, Y., Tanaka, Y., Ashikari, T., Kusumi, T. and Murata, N. 1998. Characterization of Δ9 acyl-lipid desaturase homologues from Arabidopsis thaliana. Plant Cell Physiol. 39: 247–253.
Galtier, N., Foyer, C.H., Huber, J.L.A., Voelker, T.A. and Huber, S.C. 1993. Effects of elevated sucrose phosphate synthase activity on photosynthesis, assimilate partitioning and growth in tomato. Plant Phys. 101: 535–443.
Geigenberger, P., Stitt, M. and Fernie, A.R. 2004. Metabolic control analysis and regulation of the conversion of sucrose to starch in growing potato tubers. Plant Cell Environ. 27: 655–673.
Gerjets, T. and Sandmann, G. 2006. Ketocarotenoid formation in transgenic potato. J. Exp. Bot. 57: 3639–3645.
Gomord, V., Chamberlain, P., Jefferis, R. and Faye, L. 2005. Biopharmaceutical production in plants: problems, solutions and opportunities. Trends Biotechnol. 23: 559–565.
Guerin, M., Huntley, M.E. and Olaizola, M. 2003. Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol. 21: 210–216.
Guerinot, M.L. 2007. It’s elementary: enhancing Fe3+ reduction improves rice yields. Proc. Natl. Acad. Sci. USA 104: 7311–7312.
Harrison, E.P., Willingham, N.M., Lloyd, J.C. and Raines, C.A. 1998. Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204: 27–36.
Harrison, E.P., Olcer, H., Lloyd, J.C., Long, S.P. and Raines, C.A. 2001. Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubisco carboxylation capacity. J. Exp. Bot. 52: 1779–1784.
Hase, T., Schürmann, P. and Knaff, D.B. 2006. The interaction of ferredoxin with ferredoxin-dependent enzymes. In Photosystem I: The light-driven plastocyanin-ferredoxin oxidoreductase (Golbeck, J.H., ed.), pp. 477–498, Springer, Dordrecht, The Netherlands.
Hellwig, S., Drossard, J., Twyman, R.M. and Fischer, R. 2004. Plant cell cultures for the production of recombinant proteins. Nat Biotechnol. 22: 1415–1422.
Higuera-Ciapara, I., Félix-Valenzuela, L. and Goycoolea, F.M. 2006. Astaxanthin: a review of its chemistry and applications. Crit. Rev. Food Sci. Nutr. 46: 185–196.
Hirashima, M., Satoh, S., Tanaka, R. and Tanaka, A. 2006. Pigment shuffling in antenna systems achieved by expressing prokaryotic chlorophyllide a oxygenase in Arabidopsis. J. Biol. Chem. 281: 15385–15393.
Huber, S.C. and Huber, J.L. 1992. Role of sucrose-phosphate synthase in sucrose metabolism in leaves. Plant Physiol. 99: 1275–1278.
Hühns, M., Neumann, K., Hausmann, T., Ziegler, K., Klemke, F., Kahmann, U., Staiger, D., Lockau, W., Pistorius, E.K. and Broer, I. 2008. Plastid targeting strategies for cyanophycin synthetase to achieve high-level polymer accumulation in Nicotiana tabacum. Plant Biotechnol. J. 6: 321–336.
Ishizaki-Nishizawa, O., Fujii, T., Azuma, M., Sekiguchi, K., Murata, N., Ohtani, T. and Toguri, T. 1996. Low-temperature resistance of higher plants is significantly enhanced by a nonspecific cyanobacterial desaturase. Nat. Biotechnol. 14: 1003–1006.
Jube, S. and Borthakur, D. 2007. Expression of bacterial genes in transgenic tobacco: methods, applications and future prospects. Electronic J. Biotechnol. 10: 452–467.
Kami, C., Mukougawa, K., Muramoto, T., Yokota, A., Shinomura, T., Lagarias, J.C. and Kohchi, T. 2004. Complementation of phytochrome chromophore-deficient Arabidopsis by expression of phycocyanobilin: ferredoxin oxidoreductase. Proc. Natl. Acad. Sci. USA 101:1099–1104.
Khan, M.S., Khalid, A.M. and Malik, K.A. (2005). Intein-mediated protein trans-splicing and transgene containment in plastids. Trends Biotechnol. 23: 217–220.
Kim, S.A. and Guerinot, M.L. 2007. Mining iron: iron uptake and transport in plants. FEBS Lett. 581: 2273–2280.
Krause, K.P. 1994. Zur Regulation von Saccharosephosphatsynthase. PhD Thesis, Universität Bayreuth, Germany.
Krause, K.P., Hill, L., Reimhotz, R., Hamborg-Nielsen, T., Sonnewald, U. and Stitt, M. 1998. Sucrose metabolism in cold-stored potato tubers with decreased expression of sucrose phosphate synthase. Plant Cell Environ. 21: 285–299.
Krehenbrink, M., Oppermann-Sanio, F.B. and Steinbüchel, A. 2002. Evaluation of non-cyanobacterial genome sequences for occurrence of genes encoding proteins homologous to cyanophycin synthetase and cloning of an active cyanophycin synthetase from Acinetobacter sp. strain DSM 587. Arch. Microbiol. 177: 371–380.
Kossmann, J., Sonnewald, U. and Willmitzer, L. 1994. Reduction of the chloroplast fructose-1,6-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. Plant J. 6: 637–650.
Lieman-Hurwitz, J., Rachmilevitch, S., Mittler, R., Marcus, Y. and Kaplan, A. 2003. Enhanced photosynthesis and growth of transgenic plants that express ictB , a gene involved in HCO3 − accumulation in cyanobacteria. Plant Biotechnol. J. 1: 43–50.
Long, S.P., Zhu, X.G., Naidu, S.L. and Ort, D.R. 2006. Can improvement in photosynthesis increase crop yields? Plant Cell Environ. 29: 315–330.
Lunn, J.E., Price, G.D. and Furbank, R.T. 1999. Cloning and expression of a prokaryotic sucrose-phosphate synthase gene from the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol. 40: 297–305.
Lunn, J.E., Gillespie, V.J. and Furbank, R.T. 2003. Expression of a cyanobacterial sucrose-phosphate synthase from Synechocystis sp. PCC 6803 in transgenic plants. J. Exp. Bot. 381: 223–237.
Miyagawa, Y., Tamoi, M. and Shigeoka, S. 2001. Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nat. Biotechnol. 19: 965–969.
Morandini, P. and Salamini, F. 2003. Plant biotechnology and breeding: allied for years to come. Trends Plant Sci. 8: 70–75.
Neumann, K., Stephan, D.P., Ziegler, K., Hühns, M., Broer, I., Lockau, W. and Pistorius, E.K. 2005. Production of cyanophycin, a suitable source for the biodegradable polymer polyaspartate, in transgenic plants. Plant Biotechnol. J. 3: 249–258.
Oppermann-Sanio, F.B. and Steinbüchel, A. 2002. Occurrence, functions and biosynthesis of polyamides in microorganisms and biotechnological production. Naturwissenschaften 89:11–22.
Orlova, I.V., Serebriiskaya, T.S., Popov, V., Merkulova, N., Nosov, A.M., Trunova, T.I., Tsydendambaev, V.D. and Los, D.A. 2003. Transformation of tobacco with a gene for the thermophilic acyl-lipid desaturase enhances the chilling tolerance of plants. Plant Cell Physiol. 44:447–450.
Palenik, B., Ren, Q., Dupont, C.L., Myers, G.S., Heidelberg, J.F., Badger, J.H., Madupu, R., Nelson, W.C., Brinkac, L.M., Dodson, R.J., Durkin, A.S., Daugherty, S.C., Sullivan, S.A., Khouri, H., Mohamoud, Y., Halpin, R. and Paulsen, I.T. 2006. Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment. Proc. Natl. Acad. Sci. USA 103: 13555–13559.
Perler, F.B. 1998. Protein splicing of inteins and hedgehog autoproteolysis: structure, function, and evolution. Cell 92: 1–4.
Quick, W.P. and Neuhaus, H.E. 1997. A molecular approach to primary metabolism in higher plants. In The regulation and control of photosynthetic carbon assimilation (Foyer, C.H. and Quick, W.P., eds.), pp. 41–62, Taylor and Francis Ltd, London.
Reddy, A.S., Nuccio, M.L., Gross, L.M. and Thomas, T.L. 1993. Isolation of a Δ6-desaturase gene from the cyanobacterium Synechocystis sp. strain PCC 6803 by gain-of-function expression in Anabaena sp. strain PCC 7120. Plant Mol. Biol. 22: 293–300.
Reddy, A.S. and Thomas, T.L. 1996. Expression of a cyanobacterial Δ6-desaturase gene results in γ-linolenic acid production in transgenic plants. Nat. Biotechnol. 14: 639–642.
Rolletschek, H., Borisjuk, L., Radchuk, R., Miranda, M., Heim, U., Wobus, U. and Weber, H. 2004. Seed-specific expression of a bacterial phosphoenolpyruvate carboxylase in Vicia narbonensis increases protein content and improves carbon economy. Plant Biotechnol. J. 2: 211–219.
Ryu, J.Y., Jeong, S.W., Lim, A.Y., Ko, Y., Yoon, S., Choi, A.B. and Park, Y.I. 2008. Cyanobacterial glucokinase complements the glucose sensing role of Arabidopsis thaliana hexokinase 1. Biochem. Biophys. Res. Commun. 374: 454–459.
Sandmann, G. 2001. Carotenoid biosynthesis and biotechnological application. Arch. Biochem. Biophys. 385: 4–12.
Sharkey, T.D. 1985. Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot. Rev. 51: 53–105.
Singh, A.K., Li, H. and Sherman, L.A. 2004. Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803. Physiol. Plant. 120: 27–35.
Tamoi, M., Nagaoka, M., Miyagawa, Y. and Shigeoka, S. 2006. Contribution of fructose-1,6-bisphosphatase and sedoheptulose-1,7-bisphosphatase to the photosynthetic rate and carbon flow in the Calvin cycle in transgenic plants. Plant Cell Physiol. 47: 380–390.
Thimm, O., Essigmann, B., Kloska, S., Altmann, T. and Buckhout, T.J. 2001. Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol. 127:1030–1043.
Tognetti, V.B., Palatnik, J.F., Fillat, M.F., Melzer, M., Hajirezaei, M.-R., Valle, E.M. and Carrillo, N. 2006. Functional replacement of ferredoxin by a cyanobacterial flavodoxin in tobacco confers broad-range stress tolerance. Plant Cell 18: 2035–2050.
Tognetti, V.B., Zurbriggen, M.D., Morandi, E.N., Fillat, M.F., Valle, E.M., Hajirezaei, M.-R. and Carrillo, N. 2007. Enhanced plant tolerance to iron starvation by functional substitution of chloroplast ferredoxin with a bacterial flavodoxin. Proc. Natl. Acad. Sci. USA 104: 11495–11500.
Tognetti, V., Zurbriggen, M., Valle, E., Carrillo, N., Morandi, E., Melzer, M., Hajirezaei, M.-R. and Fillat, M. 2008. Recovering the cyanobacterial heritage in land plants: the case of flavodoxin. In Flavins and flavoproteins (Frago, S., Gómez-Moreno, C. and Medina, M., eds.), Vol. 16, pp. 527–536, Prensas Universitarias de Zaragoza.
Twyman, R.M., Stoger, E., Schillberg, S., Christou, P. and Fischer, R. 2003. Molecular farming in plants: host systems and expression technology. Trends Biotechnol. 21: 570–578.
Vij, S. and Tyagi, A.K. 2007. Emerging trends in the functional genomics of the abiotic stress response in crop plants. Plant. Biotechnol. J. 5: 361–380.
Vinocur, B. and Altman, A. 2005. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr. Opin. Biotechnol. 16: 123–132.
Yang, J., Fox, G.C. and Henry-Smith, T.V. 2003. Intein-mediated assembly of a functional β-glucuronidase in transgenic plants. Proc. Natl. Acad. Sci. USA 100: 3513–3518.
Zhu, C., Gerjets, T. and Sandmann, G. 2007. Nicotiana glauca engineered for the production of ketocarotenoids in flowers and leaves by expressing the cyanobacterial crtO ketolase gene. Transgenic Res. 16: 813–821.
Ziegler, K., Deutzmann, R. and Lockau, W. 2002. Cyanophycin synthetase-like enzymes of non-cyanobacterial eubacteria: characterization of the polymer produced by a recombinant synthetase of Desulfitobacterium hafniense. Z. Naturforschung Teil C 57: 522–529.
Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. 2004. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136: 2621–2632.
Zurbriggen, M.D., Tognetti, V.B. and Carrillo, N. 2007. Stress-inducible flavodoxin from photosynthetic microorganisms. The mystery of flavodoxin loss from the plant genome. IUBMB Life 59: 355–360.
Zurbriggen, M.D., Tognetti, V.B., Fillat, M., Hajirezaei, M.R., Valle, E. and Carrillo, N. 2008. Combating stress with flavodoxin: a promising route for crop improvement. Trends Biotechnol. 26: 531–537.
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Zurbriggen, M.D., Néstor Carrillo, Hajirezaei, MR. (2009). Use of Cyanobacterial Proteins to Engineer New Crops. In: Recent Advances in Plant Biotechnology. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-0194-1_4
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