Reduced peroxisomal citrate synthase activity increases substrate availability for polyhydroxyalkanoate biosynthesis in plant peroxisomes

Plant Biotechnology Journal

Volumn 12, Issue 8, 2014, Pages 1044-1052

  Tilbrook, Kimberley ^a,c   Poirier, Yves ^b   Gebbie, Leigh ^a   Schenk, Peer M ^a   Mcqualter, Richard B ^a   Brumbley, Stevens M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Arabidopsis; Citrate synthase; Peroxisome; Plant metabolic engineering; Polyhydroxyalkanoate; oxidation

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); CUPRIAVIDUS NECATOR;

ARABIDOPSIS PROTEIN; CITRATE SYNTHASE; FATTY ACID; POLYHYDROXYALKANOIC ACID;

ARABIDOPSIS; BIOSYNTHESIS; ENZYME SPECIFICITY; ENZYMOLOGY; GENE SILENCING; GENETICS; METABOLIC ENGINEERING; METABOLISM; OXIDATION REDUCTION REACTION; PEROXISOME; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOSYNTHETIC PATHWAYS; CITRATE (SI)-SYNTHASE; FATTY ACIDS; GENE KNOCKDOWN TECHNIQUES; METABOLIC ENGINEERING; OXIDATION-REDUCTION; PEROXISOMES; PLANTS, GENETICALLY MODIFIED; POLYHYDROXYALKANOATES; SUBSTRATE SPECIFICITY;

EID: 84925945088     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12211     Document Type: Article

References (44)

1. Ahumada, I., Cairo, A., Hemmerlin, A., Gonzalez, V., Pateraki, I., Bach, T.J., Rodriguez-Concepcion, M., Campos, N. and Boronat, A. (2008) Characterisation of the gene family encoding acetoacetyl-CoA thiolase in Arabidopsis. Funct. Plant Biol. 35, 1100-1111.
2. Anderson, D.J., Gnanasambandam, A., Williams, E., O'Shea, M.G., Nielsen, L.K. and Brumbley, S.M. (2011) Synthesis of short-chain-length/medium-chain length polyhydroxyalkanoate (PHA) copolymers in peroxisomes of transgenic sugarcane plants. Trop. Plant Biol. 4, 170-184.
3. Arai, Y., Nakashita, H., Suzuki, Y., Kobayashi, Y., Shimizu, T., Yasuda, M., Doi, Y. and Yamaguchi, I. (2002) Synthesis of a novel class of polyhydroxyalkanoates in Arabidopsis peroxisomes, and their use in monitoring short-chain-length intermediates of beta-oxidation. Plant Cell Physiol. 43, 555-562.
4. Bohmert, K., Balbo, I., Kopka, J., Mittendorf, V., Nawrath, C., Poirier, Y., Tischendorf, G., Trethewey, R.N. and Willmitzer, L. (2000) Transgenic Arabidopsis plants can accumulate polyhydroxybutyrate to up to 4% of their fresh weight. Planta, 211, 841-845.
5. Bohmert-Tatarev, K., McAvoy, S., Daughtry, S., Peoples, O.P. and Snell, K.D. (2011) High levels of bioplastic are produced in fertile transplastomic tobacco plants engineered with a synthetic operon for production of polyhydroxybutyrate. Plant Physiol. 155, 1690-1708.
6. Carrie, C., Murcha, M.W., Millar, A.H., Smith, S.M. and Whelan, J. (2007) Nine 3-ketoacyl-CoA thiolases (KATs) and acetoacetyl-CoA thiolases (ACATs) encoded by five genes in Arabidopsis thaliana are targeted either to peroxisomes or cytosol but not to mitochondria. Plant Mol. Biol. 63, 97-108.
7. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
8. Dalton, D.A., Ma, C., Shrestha, S., Kitin, P. and Strauss, S.H. (2011) Trade-offs between biomass growth and inducible biosynthesis of polyhydroxybutyrate in transgenic poplar. Plant Biotechnol. J. 9, 759-767.
9. Eastmond, P.J., Germain, V., Lange, P.R., Bryce, J.H., Smith, S.M. and Graham, I.A. (2000) Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. Proc. Natl Acad. Sci. USA, 97, 5669-5674.
10. Eckardt, N.A. (2005) Peroxisomal citrate synthase provides exit route from fatty acid metabolism in oilseeds. Plant Cell, 17, 1863-1865.
11. Gnanasambandam, A., Anderson, D.J., Purnell, M.P., Nielsen, L.K. and Brumbley, S.M. (2008) The N-terminal presequence from F1-ATPase beta-subunit of Nicotiana plumbaginifolia efficiently targets green fluorescent fusion protein to the mitochondria in diverse commercial crops. Funct. Plant Biol. 35, 166-170.
12. Graham, I.A. (2008) Seed storage oil mobilization. Annu. Rev. Plant Biol. 59, 115-142.
13. Hahn, J.J., Eschenlauer, A.C., Sleytr, U.B., Somers, D.A. and Srienc, F. (1999) Peroxisomes as sites for synthesis of polyhydroxyalkanoates in transgenic plants. Biotechnol. Prog. 15, 1053-1057.
14. Hellens, R.P., Edwards, A., Leyland, N.R., Bean, S. and Mullineaux, P.M. (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
15. Katto, A., Hayashi, M., Mori, H. and Nishimura, M. (1995) Molecular characterization of a glyoxysomal citrate synthase that is synthesized as a precursor of higher molecular mass in pumpkin. Plant Mol. Biol. 27, 377-390.
16. Lee, I.Y., Kim, M.K., Park, Y.H. and Lee, S.Y. (1996) Regulatory effects of cellular nicotinamide nucleotides and enzyme activities on poly(3-hydroxybutyrate) synthesis in recombinant Escherichia coli. Biotechnol. Bioeng. 52, 707-712.
17. Li, Z.-J., Cai, L., Wu, Q. and Chen, G.-Q. (2009) Overexpression of NAD kinase in recombinant Escherichia coli harboring the phbCAB operon improves poly(3-hydroxybutyrate) production. Appl. Microbiol. Biotechnol. 83, 939-947.
18. Luckachan, G. and Pillai, C. (2011) Biodegradable polymers- A review on recent trends and emerging perspectives. J. Polym. Environ. 19, 637-676.
19. Maeda, I., Delessert, S., Hasegawa, S., Seto, Y., Zuber, S. and Poirier, Y. (2006) The peroxisomal acyl-CoA thioesterase pte1p from Saccharomyces cerevisiae is required for efficient degradation of short straight chain and branched chain fatty acids. J. Biol. Chem. 281, 11729-11735.
20. Matsumoto, K., Arai, Y., Nagao, R., Murata, T., Takase, K., Nakashita, H., Taguchi, S., Shimada, H. and Doi, Y. (2006) Synthesis of short-chain-length/medium-chain length polyhydroxyalkanoate (PHA) copolymers in peroxisome of the transgenic Arabidopsis thaliana harboring the PHA synthase gene from Pseudomonas sp 61-3. J. Polym. Environ. 14, 369-374.
21. Mittendorf, V., Robertson, E.J., Leech, R.M., Kruger, N., Steinbuchel, A. and Poirier, Y. (1998) Synthesis of medium-chain-length polyhydroxyalkanoates in Arabidopsis thaliana using intermediates of peroxisomal fatty acid beta-oxidation. Proc. Natl Acad. Sci. USA, 95, 13397-13402.
22. Mittendorf, V., Bongcam, V., Allenbach, L., Coullerez, G., Martini, N. and Poirier, Y. (1999) Polyhydroxyalkanoate synthesis in transgenic plants as a new tool to study carbon flow through beta-oxidation. Plant J. 20, 45-55.
23. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
24. Nawrath, C., Poirier, Y. and Somerville, C. (1994) Targeting of the polyhydroxybutyrate biosynthetic-pathway to the plastids of Arabidopsis thaliana results in high levels of polymer accumulation. Proc. Natl Acad. Sci. USA, 91, 12760-12764.
25. Penfield, S., Rylott, E.L., Gilday, A.D., Graham, S., Larson, T.R. and Graham, I.A. (2004) Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires phosphoenolpyruvate carboxykinase. Plant Cell, 16, 2718.
26. Petrasovits, L.A., Purnell, M.P., Nielsen, L.K. and Brumbley, S.M. (2007) Production of polyhydroxybutyrate in sugarcane. Plant Biotechnol. J. 5, 162-172.
27. Petrasovits, L.A., Zhao, L., McQualter, R.B., Snell, K.D., Somleva, M.N., Patterson, N.A., Nielsen, L.K. and Brumbley, S.M. (2012) Strategies to enhance polyhydroxybutryate production in transgenic sugarcane. Plant Biotechnol. J. 10, 569-578.
28. Petrasovits, L.A., McQualter, R.B., Gebbie, L.K., Blackman, D.M., Nielsen, L.K. and Brumbley, S.M. (2013) Chemical inhibition of acetyl coenzyme A carboxylase as a strategy to increase polyhydroxybutyrate yields in transgenic sugarcane. Plant Biotechnol. J. 11, 1146-1151.
29. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
30. Poirier, Y., Ventre, G. and Caldelari, D. (1999) Increased flow of fatty acids toward beta-oxidation in developing seeds of Arabidopsis deficient in diacylglycerol acyltransferase activity or synthesizing medium-chain-length fatty acids. Plant Physiol. 121, 1359-1366.
31. Poirier, Y., Antonenkov, V.D., Glumoff, T. and Hiltunen, J.K. (2006) Peroxisomal beta-oxidation - A metabolic pathway with multiple functions. Biochim. Biophys. Acta-Mol. Cell Res. 1763, 1413-1426.
32. Pracharoenwattana, I., Cornah, J.E. and Smith, S.M. (2005) Arabidopsis peroxisomal citrate synthase is required for fatty acid respiration and seed germination. Plant Cell, 17, 2037-2048.
33. Sanchez, A.M., Andrews, J., Hussein, I., Bennett, G.N. and San, K.Y. (2006) Effect of overexpression of a soluble pyridine nucleotide transhydrogenase (UdhA) on the production of poly(3-hydroxybutyrate) in Escherichia coli. Biotechnol. Prog. 22, 420-425.
34. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. and Weigel, D. (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell, 18, 1121-1133.
35. Snell, K.D. and Peoples, O.P. (2009) PHA bioplastic: a value-added coproduct for biomass biorefineries. Biofuels Bioprod. Biorefin.-Biofpr. 3, 456-467.
36. Somleva, M.N., Snell, K.D., Beaulieu, J.J., Peoples, O.P., Garrison, B.R. and Patterson, N.A. (2008) Production of polyhydroxybutyrate in switchgrass, a value-added co-product in an important lignocellulosic biomass crop. Plant Biotechnol. J. 6, 663-678.
37. Somleva, M.N., Peoples, O.P. and Snell, K.D. (2013) PHA bioplastics, biochemicals, and energy from crops. Plant Biotechnol. J. 11, 233-252.
38. Stefan, K., Michael, D., George, S., Birgit, K. and Bernard, W. (2000) Inactivation of isocitrate lyase leads to increased production of medium-chain-length poly(3-hydroxyalkanoates) in Pseudomonas putida. Appl. Environ. Microbiol. 66, 913.
39. Steinbüchel, A. and Valentin, H.E. (1995) Diversity of bacterial polyhydroxyalkanoic acids. FEMS Microbiol. Lett. 128, 219-228.
40. Takase, K., Taguchi, S. and Doi, Y. (2003) Enhanced synthesis of poly(3-hydroxybutyrate) in recombinant Escherichia coli by means of error-prone PCR mutagenesis, saturation mutagenesis, and in vitro recombination of the type II polyhydroxyalkanoate synthase gene. J. Biochem. 133, 139-145.
41. Takase, K., Matsumoto, K., Taguchi, S. and Doi, Y. (2004) Alteration of substrate chain length specificity of type II synthase for polyhydroxyalkanoate biosynthesis by in vitro evolution: in vivo and in vitro enzyme assays. Biomacromolecules, 5, 480-485.
42. Terzaghi, W.B. (1986) Metabolism of Tween-fatty acid-esters by cultured soybean cells: kinetics of incorporation into lipids, subsequent turnover, and associated changes in endogenous fatty-acid synthesis. Plant Physiol. 82, 780-786.
43. Tilbrook, K., Gebbie, L., Schenk, P.M., Poirier, Y. and Brumbley, S.M. (2011) Peroxisomal polyhydroxyalkanoate biosynthesis is a promising strategy for bioplastic production in high biomass crops. Plant Biotechnol. J. 9, 958-969.
44. Van Beilen, J. and Poirier, Y. (2012) Plants as factories for bioplastics and other biomaterials. In Plant Biotechnology and Agriculture: Prospects for the 21st Century (Altman, A. and Hasegawa, P.M., eds), pp. 481-494. London, UK: Academic Press.