Taming the hydra of specialized metabolism: How systems biology and comparative approaches are revolutionizing plant biochemistry

Current Opinion in Plant Biology

Volumn 15, Issue 3, 2012, Pages 338-344

  Schilmiller, Anthony L ^a   Pichersky, Eran ^b   Last, Robert L ^a,c  

^a Michigan State University   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

ANIMAL; CYTOLOGY; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; HYDRA; METABOLISM; METABOLOMICS; METHODOLOGY; PLANT; PLANT CELL; PROTEOMICS; REVIEW; SYSTEMS BIOLOGY;

ANIMALS; GENOMICS; HYDRA; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; PLANT CELLS; PLANTS; PROTEOMICS; SYSTEMS BIOLOGY; TRANSCRIPTOME;

HYDRA;

EID: 84861660809     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2011.12.005     Document Type: Review

References (56)

1. Pichersky E., Lewinsohn E. Convergent evolution in plant specialized metabolism. Ann Rev Plant Biol 2011, 62:549-566.
2. Bak S., Beisson F., Bishop G., Hamberger B., Hofer R., Paquette S., Werck-Reichhart D. Cytochromes P450. The Arabidopsis Book 2011, p. e0144.
3. Chen F., Tholl D., Bohlmann J., Pichersky E. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 2011, 66:212-229.
4. Fraenkel G.S. The raison d'être of secondary plant substances. Science 1959, 129:1466-1470.
5. Kajikawa M., Shoji T., Kato A., Hashimoto T. Vacuole-localized berberine bridge enzyme-like proteins are required for a late step of nicotine biosynthesis in tobacco. Plant Physiol 2011, 155:2010-2022.
6. Nagel J., Culley L.K., Lu Y., Liu E., Matthews P.D., Stevens J.F., Page J.E. EST analysis of hop glandular trichomes identifies an O-methyltransferase that catalyzes the biosynthesis of xanthohumol. Plant Cell 2008, 20:186-200.
7. Last R.L., Jones A.D., Shachar-Hill Y. Towards the plant metabolome and beyond. Nat Rev Mol Cell Biol 2007, 8:167-174.
8. Zhang J., Chiodini R., Badr A., Zhang G. The impact of next-generation sequencing on genomics. J Genet Genomics 2011, 38:95-109.
9. Remmerie N., De Vijlder T., Laukens K., Dang T.H., Lemiere F., Mertens I., Valkenborg D., Blust R., Witters E. Next generation functional proteomics in non-model plants: a survey on techniques and applications for the analysis of protein complexes and post-translational modifications. Phytochemistry 2011, 72:1192-1218.
10. Saito K., Matsuda F. Metabolomics for functional genomics, systems biology, and biotechnology. Annu Rev Plant Biol 2010, 61:463-489.
11. Fukushima A., Kusano M., Redestig H., Arita M., Saito K. Integrated omics approaches in plant systems biology. Curr Opin Chem Biol 2009, 13:532-538.
12. Hirai M.Y., Sugiyama K., Sawada Y., Tohge T., Obayashi T., Suzuki A., Araki R., Sakurai N., Suzuki H., Aoki K., et al. Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci USA 2007, 104:6478-6483.
13. Sønderby I.E., Hansen B.G., Bjarnholt N., Ticconi C., Halkier B.A., Kliebenstein D.J. A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE 2007, 2:e1322.
14. Lee J.M., Joung J.-G., McQuinn R., Chung M.-Y., Fei Z., Tieman D., Klee H., Giovannoni J. Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals the ethylene response factor SlERF6 to play an important role in ripening and carotenoid accumulation. Plant J 2011, 10.1111/j.1365-1313X.2011.04863.x.
15. Farag M.A., Deavours B.E., de Fatima A., Naoumkina M., Dixon R.A., Sumner L.W. Integrated metabolite and transcript profiling identify a biosynthetic mechanism for hispidol in Medicago truncatula cell cultures. Plant Physiol 2009, 151:1096-1113.
16. Desgagne-Penix I., Khan M.F., Schriemer D.C., Cram D., Nowak J., Facchini P.J. Integration of deep transcriptome and proteome analyses reveals the components of alkaloid metabolism in opium poppy cell cultures. BMC Plant Biol 2010, 10.
17. Schilmiller A.L., Last R.L., Pichersky E. Harnessing plant trichome biochemistry for the production of useful compounds. Plant J 2008, 54:702-711.
18. Lange B.M., Wildung M.R., Stauber E.J., Sanchez C., Pouchnik D., Croteau R. Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proc Natl Acad Sci USA 2000, 97:2934-2939.
19. Schilmiller A.L., Schauvinhold I., Larson M., Xu R., Charbonneau A.L., Schmidt A., Wilkerson C., Last R.L., Pichersky E. Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate. Proc Natl Acad Sci USA 2009, 106:10865-10870.
20. Schilmiller A.L., Miner D.P., Larson M., McDowell E., Gang D.R., Wilkerson C., Last R.L. Studies of a biochemical factory: tomato trichome deep expressed sequence tag sequencing and proteomics. Plant Physiol 2010, 153:1212-1223.
21. McDowell E.T., Kapteyn J., Schmidt A., Li C., Kang J.H., Descour A., Shi F., Larson M., Schilmiller A., An L.L., et al. Comparative functional genomic analysis of Solanum glandular trichome types. Plant Physiol 2011, 155:524-539.
22. Rios-Estepa R., Turner G.W., Lee J.M., Croteau R.B., Lange B.M. A systems biology approach identifies the biochemical mechanisms regulating monoterpenoid essential oil composition in peppermint. Proc Natl Acad Sci USA 2008, 105:2818-2823.
23. Wang G., Tian L., Aziz N., Broun P., Dai X., He J., King A., Zhao P.X., Dixon R.A. Terpene biosynthesis in glandular trichomes of hop. Plant Physiol 2008, 148:1254-1266.
24. 9-tetrahydrocannabinol biosynthesis in Cannabis sativa. J Exp Bot 2009, 60:3715-3726.
25. Aziz N., Paiva N., May G., Dixon R. Transcriptome analysis of alfalfa glandular trichomes. Planta 2005, 221:28-38.
26. Dai X., Wang G., Yang D.S., Tang Y., Broun P., Marks M.D., Sumner L.W., Dixon R.A., Zhao P.X. TrichOME: a comparative omics database for plant trichomes. Plant Physiol 2010, 152:44-54.
27. Zenk M.H., Juenger M. Evolution and current status of the phytochemistry of nitrogenous compounds. Phytochemistry 2007, 68:2757-2772.
28. Abbott E., Hall D., Hamberger B., Bohlmann J. Laser microdissection of conifer stem tissues: isolation and analysis of high quality RNA, terpene synthase enzyme activity and terpenoid metabolites from resin ducts and cambial zone tissue of white spruce (Picea glauca). BMC Plant Biol 2010, 10:106.
29. van Bakel H., Stout J.M., Cote A.G., Tallon C.M., Sharpe A.G., Hughes T.R., Page J.E. The draft genome and transcriptome of Cannabis sativa. Genome Biol 2011, 12:R102.
30. Hansen B.G., Kerwin R.E., Ober J.A., Lambrix V.M., Mitchell-Olds T., Gershenzon J., Halkier B.A., Kliebenstein D.J. A novel 2-oxoacid-dependent dioxygenase involved in the formation of the goiterogenic 2-hydroxybut-3-enyl glucosinolate and generalist insect resistance in Arabidopsis. Plant Physiol 2008, 148:2096-2108.
31. Hansen B.G., Kliebenstein D.J., Halkier B.A. Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J 2007, 50:902-910.
32. Pfalz M., Vogel H., Kroymann J. The gene controlling the Indole Glucosinolate Modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 2009, 21:985-999.
33. Kerwin R.E., Jimenez-Gomez J.M., Fulop D., Harmer S.L., Maloof J.N., Kliebenstein D.J. Network quantitative trait loci mapping of circadian clock outputs identifies metabolic pathway-to-clock linkages in Arabidopsis. Plant Cell 2011, 23:471-485.
34. Chan E.K.F., Rowe H.C., Corwin J.A., Joseph B., Kliebenstein D.J. Combining genome-wide association mapping and transcriptional networks to identify novel genes controlling glucosinolates in Arabidopsis thaliana. PLoS Biol 2011, 9:e1001125.
35. Kliebenstein D., Pedersen D., Barker B., Mitchell-Olds T. Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics 2002, 161:325-332.
36. Kliebenstein D.J., Kroymann J., Brown P., Figuth A., Pedersen D., Gershenzon J., Mitchell-Olds T. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol 2001, 126:811-825.
37. Kroymann J., Donnerhacke S., Schnabelrauch D., Mitchell-Olds T. Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proc Natl Acad Sci USA 2003, 100:14587-14592.
38. Ziegler J., Voigtländer S., Schmidt J., Kramell R., Miersch O., Ammer C., Gesell A., Kutchan T.M. Comparative transcript and alkaloid profiling in Papaver species identifies a short chain dehydrogenase/reductase involved in morphine biosynthesis. Plant J 2006, 48:177-192.
39. Ziegler J., Diaz-Chávez M., Kramell R., Ammer C., Kutchan T. Comparative macroarray analysis of morphine containing Papaver somniferum and eight morphine free Papaver species identifies an O-methyltransferase involved in benzylisoquinoline biosynthesis. Planta 2005, 222:458-471.
40. Ben-Israel I., Yu G., Austin M.B., Bhuiyan N., Auldridge M., Nguyen T., Schauvinhold I., Noel J.P., Pichersky E., Fridman E. Multiple biochemical and morphological factors underlie the production of methylketones in tomato trichomes. Plant Physiol 2009, 151:1952-1964.
41. Eshed Y., Zamir D. An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 1995, 141:1147-1162.
42. Schilmiller A., Shi F., Kim J., Charbonneau A.L., Holmes D., Jones A.D., Last R.L. Mass spectrometry screening reveals widespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines. Plant J 2010, 62:391-403.
43. Tieman D.M., Zeigler M., Schmelz E.A., Taylor M.G., Bliss P., Kirst M., Klee H.J. Identification of loci affecting flavour volatile emissions in tomato fruits. J Exp Bot 2006, 57:887-896.
44. Mathieu S., Cin V.D., Fei Z., Li H., Bliss P., Taylor M.G., Klee H.J., Tieman D.M. Flavour compounds in tomato fruits: identification of loci and potential pathways affecting volatile composition. J Exp Bot 2009, 60:325-337.
45. Frey M., Chomet P., Glawischnig E., Stettner C., Grun S., Winklmair A., Eisenreich W., Bacher A., Meeley R.B., Briggs S.P., et al. Analysis of a chemical plant defense mechanism in grasses. Science 1997, 277:696-699.
46. Field B., Osbourn A.E. Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 2008, 320:543-547.
47. Field B., Fiston-Lavier A.-S., Kemen A., Geisler K., Quesneville H., Osbourn A.E. Formation of plant metabolic gene clusters within dynamic chromosomal regions. Proc Natl Acad Sci USA 2011, 108:16116-16121.
48. Shimura K., Okada A., Okada K., Jikumaru Y., Ko K.-W., Toyomasu T., Sassa T., Hasegawa M., Kodama O., Shibuya N., et al. Identification of a biosynthetic gene cluster in rice for momilactones. J Biol Chem 2007, 282:34013-34018.
49. Swaminathan S., Morrone D., Wang Q., Fulton D.B., Peters R.J. CYP76M7 is an ent-cassadiene C11α-hydroxylase defining a second multifunctional diterpenoid biosynthetic gene cluster in rice. Plant Cell 2009, 21:3315-3325.
50. Falara V., Akhtar T.A., Nguyen T.T.H., Spyropoulou E.A., Bleeker P.M., Schauvinhold I., Matsuba Y., Bonini M.E., Schilmiller A.L., Last R.L., et al. The tomato terpene synthase gene family. Plant Physiol 2011, 157:770-789.
51. Sallaud C., Rontein D., Onillon S., Jabès F., Duffé P., Giacalone C., Thoraval S., Escoffier C., Herbette G., Leonhardt N., et al. A novel pathway for sesquiterpene biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 2009, 21:301-317.
52. Svatos A. Single-cell metabolomics comes of age: new developments in mass spectrometry profiling and imaging. Anal Chem 2011, 83:5037-5044.
53. Liscombe D.K., O'Connor S.E. A virus-induced gene silencing approach to understanding alkaloid metabolism in Catharanthus roseus. Phytochemistry 2011, 72:1969-1977.
54. Yu X.-H., Liu C.-J. Development of an analytical method for genome-wide functional identification of plant acyl-coenzyme A-dependent acyltransferases. Anal Biochem 2006, 358:146-148.
55. Hendricks C.L., Ross J.R., Pichersky E., Noel J.P., Zhou Z.S. An enzyme-coupled colorimetric assay for S-adenosylmethionine-dependent methyltransferases. Anal Biochem 2004, 326:100-105.
56. Pfalz M., Mikkelsen M.D., Bednarek P., Olsen C.E., Halkier B.A., Kroymann J. Metabolic engineering in Nicotiana benthamiana reveals key enzyme functions in Arabidopsis indole glucosinolate modification. Plant Cell 2011, 23:716-729.