Metabolite profiling as an aid to metabolic engineering in plants

Current Opinion in Plant Biology

Volumn 7, Issue 2, 2004, Pages 196-201

  Trethewey, Richard N ^a  

^a Metanomics GmbH   (Germany)

Author keywords

Gas chromatography; GC; Mass spectrometry; MS

Indexed keywords

VEGETABLE PROTEIN;

BIOTECHNOLOGY; GENETIC ENGINEERING; GENETICS; METABOLISM; METHODOLOGY; REVIEW; TRANSGENIC PLANT;

BIOTECHNOLOGY; GENETIC ENGINEERING; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED;

EID: 1542351248     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2003.12.003     Document Type: Review

References (62)

1. Wink M. Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor. Appl. Genet. 75:1988;225-233.
2. Fernie A.R., Willmitzer L., Trethewey R.N. Sucrose to starch: a transition in molecular plant physiology. Trends Plant Sci. 7:2002;35-41. This review provides an overview of the many diverse metabolic-engineering approaches that have been used to alter carbohydrate metabolism in potato tubers.
3. Carrari F., Urbanczyk-Wochniak E., Willmitzer L., Fernie A.R. Engineering central metabolism in crop species: learning the system. Metab. Eng. 5:2003;191-200. The authors of this article introduce and review the full range of technologies that are required to support metabolic engineering in crop plants.
4. Lessard P.A., Kulaveerasingam H., York G.M., Strong A., Sinskey A.J. Manipulating gene expression for the metabolic engineering of plants. Metab. Eng. 4:2002;67-79.
5. Cahoon E.B., Hall S.E., Ripp K.G., Ganzke T.S., Hitz W.D., Coughlan S.J. Metabolic redesign of vitamin E biosynthesis in plants for tocotrienol production and increased antioxidant content. Nat. Biotechnol. 21:2003;1082-1087. This is an excellent example of crop metabolic engineering. Overexpression of the barley homogentisic acid geranylgeranyl transferase in corn seeds increased the tocotrienol and tocopherol contents of the seeds up to six-fold. In Arabidopsis, a 10-15-fold increase in total Vitamin E antioxidants resulted from the overexpression of this enzyme.
6. Galili G., Hofgen R. Metabolic engineering of amino acids and storage proteins in plants. Metab. Eng. 4:2002;3-11.
7. Hughes E.H., Shanks J.V. Metabolic engineering of plants for alkaloid production. Metab. Eng. 4:2002;41-48.
8. Verpoorte R., Memelink J. Engineering secondary metabolite production in plants. Curr. Opin. Biotechnol. 13:2002;181-187.
9. Galili G., Galili S., Lewinsohn E., Tadmor Y. Genetic, molecular, and genomic approaches to improve the value of plant foods and feeds. CRC Crit. Rev. Plant Sci. 21:2002;167-204.
10. DellaPenna D. Plant metabolic engineering. Plant Physiol. 125:2001;160-163.
11. Stark D.M., Timmermann K.P., Barry G.F., Preiss J., Kishore G.M. Regulation of the amount of starch in plant tissues by ADP glucose pyrophosphorylase. Science. 258:1992;287-292.
12. Romer S., Lubeck J., Kauder F., Steiger S., Adomat C., Sandmann G. Genetic engineering of a zeaxanthin-rich potato by antisense inactivation and co-suppression of carotenoid epoxidation. Metab. Eng. 4:2002;263-272.
13. Rees T., Hill S.A. Metabolic control analysis of plant metabolism. Plant Cell. Environ. 17:1994;587-599.
14. Kacser H., Burns J.A. The control of flux. Symp. Soc. Exp. Biol. 27:1973;65-104.
15. Henkes S., Sonnewald U., Badur R., Flachmann R., Stitt M. A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell. 13:2001;535-551.
16. Haake V., Zrenner R., Sonnewald U., Stitt M. A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. Plant J. 14:1998;147-157.
17. Hoefnagel M.H., Starrenburg M.J., Martens D.E., Hugenholtz J., Kleerebezem M., Van Swam I.I., Bongers R., Westerhoff H.V., Snoep J.L. Metabolic engineering of lactic acid bacteria, the combined approach: kinetic modelling, metabolic control and experimental analysis. Microbiol. 148:2002;1003-1013.
18. Beyer P., Al-Babili S., Ye X., Lucca P., Schaub P., Welsch R., Potrykus I.J. Golden rice: introducing the beta-carotene biosynthesis pathway into rice endosperm by genetic engineering to defeat vitamin A deficiency. J. Nutr. 132:2002;506S-510S. This work provides the classic example of the introduction of a novel biochemical pathway, the beta-carotene synthesis pathway, into a crop plant (Golden Rice) with obvious biotechnological applications. There are many publications on this work; this article is an accessible review of the current status.
19. Bohnert K., Balbo I., Steinbuchel A., Tischendorf G., Willmitzer L. Constitutive expression of the beta-ketothiolase gene in transgenic plants. A major obstacle for obtaining polyhydroxybutyrate-producing plants. Plant Physiol. 128:2002;1282-1290.
20. Houmiel K.L., Slater S., Broyles D., Casagrande L., Colburn S., Gonzalez K., Mitsky T.A., Reiser S.E., Shah D., Taylor N.B.et al. Poly(beta- hydroxybutyrate) production in oilseed leukoplasts of Brassica napus. Planta. 209:1999;547-550.
21. Rontein D., Basset G., Hanson A.D. Metabolic engineering of osmoprotectant accumulation in plants. Metab. Eng. 4:2002;49-56.
22. Thelen J.J., Ohlrogge J.B. Metabolic engineering of fatty acid biosynthesis in plants. Metab. Eng. 4:2002;12-21.
23. Sweetlove L.J., Last R.L., Fernie A.R. Predictive metabolic engineering: a goal for systems biology. Plant Physiol. 132:2003;420-425. This review makes the case that successful metabolic engineering of plants in the future will require a change in the way that science is approached. The article highlights the need for developments in experimental technologies and mathematical methods of data interpretation and modelling.
24. Regierer B., Fernie A.R., Springer F., Perez-Melis A., Leisse A., Koehl K., Willmitzer L., Giegenberger P., Kossmann J. Starch content and yield increase as a result of altering adenylate pools in transgenic plants. Nat. Biotechnol. 20:2002;1256-1260. The authors describe how higher starch accumulation in potato was achieved through antisense repression of plastidial adenylate kinase. Importantly, this work demonstrates how pathway flux can be manipulated by engineering steps that are removed from the pathway in question. It also highlights the network nature of metabolism, which involves wide-ranging interconnections through metabolites such as the adenylates.
25. Bohmert K., Balbo I., Kopka J., Mittendorf V., Nawrath C., Poirier Y., Tischendorf G., Trethewey R.N., Willmitzer L. Transgenic Arabidopsis plants can accumulate polyhydroxybutyrate to up to 4% of their fresh weight. Planta. 211:2000;841-845.
26. Roessner U., Willmitzer L., Fernie A.R. High-resolution metabolic phenotyping of genetically and environmentally diverse potato tuber systems. Identification of phenocopies. Plant Physiol. 127:2001;749-764.
27. Kuiper H.A., Kok E.J., Engel K.-H. Exploitation of molecular profiling techniques for GM food safety assessment. Curr. Opin. Biotechnol. 14:2003;238-243. A good introduction to the issues that are associated with assessments of genetically modified food. The authors thoroughly discuss the potential future role of metabolite profiling in these assessments.
28. Fiehn O. Metabolic networks of Cucurbita maxima phloem. Phytochemistry. 62:2003;875-886.
29. Fiehn O., Weckwerth W. Deciphering metabolic networks. Eur. J. Biochem. 270:2003;579-588.
30. Steuer R., Kurths J., Fiehn O., Weckwerth W. Observing and interpreting correlations in metabolomic networks. Bioinformatics. 19:2003;1019-1026. A pioneering study on the analysis and interpretation of high-throughput metabolomics data. The authors relate empirically determined correlation networks to the underlying biochemical pathways.
31. Kell D.B. Metabolomics and machine learning: explanatory analysis of complex metabolome data using genetic programming to produce simple, robust rules. Mol. Biol. Rep. 29:2002;237-241.
32. Kose F., Weckwerth W., Linke T., Fiehn O. Visualizing plant metabolomic correlation networks using clique-metabolite matrices. Bioinformatics. 17:2001;1198-1208.
33. Larson T.R., Graham I.A. Technical advance: a novel technique for the sensitive quantification of acyl CoA esters from plant tissues. Plant J. 25:2001;115-125.
34. Sumner L.W., Mendes P., Dixon R.A. Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry. 62:2003;817-836. A readable and logical contemporary review of plant metabolomics. The authors place particular emphasis on introducing the sometimes bewildering range of technologies that are used in this field. Definitions and nomenclature are also given careful treatment.
35. Fiehn O. Metabolomics - the link between genotypes and phenotypes. Plant Mol. Biol. 48:2002;155-171.
36. Fiehn O. Combining genomics, metabolome analysis, and biochemical modeling to understand metabolic networks. Comp. Funct Genomics. 2:2001;155-168.
37. Nicholson J.K., Connelly J., Lindon J.C., Holmes E. Metabonomics: a platform for studying drug toxicity and gene function. Nat. Rev. Drug Discov. 1:2002;153-161.
38. Nicholson J.K., Lindon J.C., Holmes E. 'Metabonomics': understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica. 29:1999;1181-1189.
39. Lindon J.C., Holmes E., Nicholson J.K. Pattern recognition methods and applications in biomedical magnetic resonance. Prog. Nuc. Mag. Res. Spec. 39:2001;1-40.
40. Roessner U., Wagner C., Kopka J., Trethewey R.N., Willmitzer L. Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J. 23:2000;131-142.
41. Roessner U., Luedemann A., Brust D., Fiehn O., Linke T., Willmitzer L., Fernie A.R. Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell. 13:2001;11-29.
42. Roessner U., Willmitzer L., Fernie A.R. Metabolic profiling and biochemical phenotyping of plant systems. Plant Cell. Rep. 21:2002;189-196.
43. Fiehn O., Kopka J., Dörmann P., Altmann T., Trethewey R.N., Willmitzer L. Metabolic plant functional genomics. Nat. Biotechnol. 18:2000;1157-1161.
44. Roessner-Tunali U., Hegemann B., Lytovchenko A., Carrari F., Bruedigam C., Granot D., Fernie A.R. Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol. 133:2003;84-99. This paper illustrates the power of metabolite profiling when applied to the study of metabolic-engineering approaches in tomato fruits. The authors conclude that the influence of hexose phosphorylation on metabolism in tomato fruits decreases during ripening, emphasising the importance of temporal resolution in metabolic-engineering studies.
45. Frenzel T., Miller A., Engel K.H. Metabolite profiling - a fractionation method for analysis of major and minor compounds in rice grains. Cereal Chem. 79:2002;215-221.
46. Dixon R.A., Achnine L., Kota P., Liu C.J., Reddy M.S.S., Wang L.J. The phenylpropanoid pathway and plant defence - a genomics perspective. Mol. Plant Pathol. 3:2002;371-390.
47. Anterola A.M., Lewis N.G. Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry. 61:2002;221-294.
48. Humphreys J.M., Chapple C. Rewriting the lignin roadmap. Curr. Opin. Plant Biol. 5:2002;224-229.
49. Meyermans H., Morreel K., Lapierre C., Pollet B., De Bruyn A., Busson R., Herdewijn P., Devreese B., Van Beeumen J., Marita J.M.et al. Modifications in lignin and accumulation of phenolic glucosides in poplar xylem upon down-regulation of caffeoyl-coenzyme A O-methyltransferase, an enzyme involved in lignin biosynthesis. J. Biol. Chem. 275:2000;36899-36909.
50. Guo D., Chen F., Inoue K., Blount J.W., Dixon R.A. Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa. Impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell. 13:2001;73-88.
51. Liu C.J., Blount J.W., Steele C.L., Dixon R.A. Bottlenecks for metabolic engineering of isoflavone glycoconjugates in Arabidopsis. Proc. Natl. Acad. Sci. USA. 99:2002;14578-14583.
52. Jung W., Yu O., Lau S.M., O'Keefe D.P., Odell J., Fader G., McGonigle B. Identification and expression of isoflavone synthase, the key enzyme for biosynthesis of isoflavones in legumes. Nat Biotechnol. 18:2000;208-212.
53. Lange B.M., Ketchum R.E.B., Croteau R.B. Isoprenoid biosynthesis. Metabolite profiling of peppermint oil gland secretory cells and application to herbicide target analysis. Plant Physiol. 127:2001;305-314.
54. Weichert H., Kolbe A., Kraus A., Wasternack C., Feussner I. Metabolic profiling of oxylipins in germinating cucumber seedlings lipoxygenase-dependent degradation of triacylglycerols and biosynthesis of volatile aldehydes. Planta. 215:2002;612-619.
55. Weichert H., Kohlmann M., Wasternack C., Feussner I. Metabolic profiling of oxylipins upon sorbitol treatment in barley leaves. Biochem. Soc. Trans. 28:2000;861-862.
56. Ketchum R.E.B., Rithner C.D., Qiu D., Kim Y.S., Williams R.M., Croteau R.B. Taxus metabolomics: methyl jasmonate preferentially induces production of taxoids oxygenated at C-13 in Taxus x media cell cultures. Phytochemistry. 62:2003;901-909.
57. Yamazaki Y., Urano A., Sudo H., Kitajima M., Takayama H., Yamazaki M., Aimi N., Saito K. Metabolite profiling of alkaloids and strictosidine synthase activity in camptothecin producing plants. Phytochemistry. 62:2003;461-470.
58. Yamazaki M., Nakajima J., Yamanashi M., Sugiyama M., Makita Y., Springob K., Awazuhara M., Saito K. Metabolomics and differential gene expression in anthocyanin chemo-varietal forms of Perilla frutescens. Phytochemistry. 62:2003;987-995.
59. Le Gall G., DuPont M.S., Mellon F.A., Davis A.L., Collins G.J., Verhoeyen M.E., Colquhoun I.J. Characterisation and content of flavonoid glycosides in genetically modified tomato (Lycopersicon esculentum) fruits. J. Agric. Food Chem. 51:2003;2438-2446.
60. Verdonk J.C., de Vos C.H.R., Verhoeven H.A., Haring M.A., van Tunen A.J., Schuurink R.C. Regulation of floral scent production in petunia revealed by targeted metabolomics. Phytochemistry. 62:2003;997-1008.
61. Flamini G., Cioni P.L., Morelli I. Differences in the fragrances of pollen, leaves, and floral parts of garland (Chrysanthemum coronarium) and composition of the essential oils from flowerheads and leaves. J. Agric. Food Chem. 51:2003;2267-2271.
62. Brown K. Plant genetics. Something to sniff at: unbottling floral scent. Science. 296:2002;2327-2329.