The challenges of cellular compartmentalization in plant metabolic engineering

Current Opinion in Biotechnology

Volumn 24, Issue 2, 2013, Pages 239-246

  Heinig, Uwe ^a   Gutensohn, Michael ^b   Dudareva, Natalia ^b   Aharoni, Asaph ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR COMPARTMENTS; COMPLEX METABOLIC NETWORKS; ENGINEERING EXPERIMENTS; METABOLIC NETWORK MODELS; PLANT METABOLIC ENGINEERING; SUBCELLULAR LOCALIZATIONS; SUBCELLULAR LOCATION; SUBSTRATE AVAILABILITIES;

COMPLEX NETWORKS;

METABOLIC ENGINEERING;

CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME SPECIFICITY; ENZYME SYNTHESIS; METABOLIC ENGINEERING; MULTIGENE FAMILY; NONHUMAN; PLANT CELL; PLANT GENOME; PLANT METABOLISM; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEIN TRANSPORT; PROTOPLAST; REVIEW; TRANSGENIC PLANT;

CELL COMPARTMENTATION; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; ORGANELLES; PLANT CELLS; PLANT PROTEINS; PLANTS; SYNTHETIC BIOLOGY;

EID: 84874971922     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2012.11.006     Document Type: Review

References (58)

1. Verma P., Mathur A.K., Srivastava A., Mathur A. Emerging trends in research on spatial and temporal organization of terpenoid indole alkaloid pathway in Catharanthus roseus: a literature update. Protoplasma 2012, 249:255-268.
2. Farhi M., Marhevka E., Ben-Ari J., Algamas-Dimantov A., Liang Z., Zeevi V., Edelbaum O., Spitzer-Rimon B., Abeliovich H., Schwartz B., et al. Generation of the potent anti-malarial drug artemisinin in tobacco. Nat Biotechnol 2011, 29:1072-1074.
3. Wu S., Chappell J. Metabolic engineering of natural products in plants; tools of the trade and challenges for the future. Curr Opin Biotechnol 2008, 19:145-152.
4. Seaver S.M., Henry C.S., Hanson A.D. Frontiers in metabolic reconstruction and modeling of plant genomes. J Exp Bot 2012, 63:2247-2258.
5. Kueger S., Steinhauser D., Willmitzer L., Giavalisco P. High-resolution plant metabolomics: from mass spectral features to metabolites and from whole-cell analysis to subcellular metabolite distributions. Plant J 2012, 70:39-50.
6. O'Grady J., Schwender J., Shachar-Hill Y., Morgan J.A. Metabolic cartography: experimental quantification of metabolic fluxes from isotopic labelling studies. J Exp Bot 2012, 63:2293-2308.
7. Wu S., Schalk M., Clark A., Miles R.B., Coates R., Chappell J. Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat Biotechnol 2006, 24:1441-1447.
8. Aharoni A., Giri A.P., Deuerlein S., Griepink F., de Kogel W.J., Verstappen F.W., Verhoeven H.A., Jongsma M.A., Schwab W., Bouwmeester H.J. Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 2003, 15:2866-2884.
9. Kappers I.F., Aharoni A., van Herpen T.W., Luckerhoff L.L., Dicke M., Bouwmeester H.J. Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 2005, 309:2070-2072.
10. Di Fiore S., Li Q., Leech M.J., Schuster F., Emans N., Fischer R., Schillberg S. Targeting tryptophan decarboxylase to selected subcellular compartments of tobacco plants affects enzyme stability and in vivo function and leads to a lesion-mimic phenotype. Plant Physiol 2002, 129:1160-1169.
11. Kumar S., Hahn F.M., Baidoo E., Kahlon T.S., Wood D.F., McMahan C.M., Cornish K., Keasling J.D., Daniell H., Whalen M.C. Remodeling the isoprenoid pathway in tobacco by expressing the cytoplasmic mevalonate pathway in chloroplasts. Metab Eng 2012, 14:19-28.
12. Wu S., Jiang Z., Kempinski C., Eric Nybo S., Husodo S., Williams R., Chappell J. Engineering triterpene metabolism in tobacco. Planta 2012.
13. Fujisawa M., Takita E., Harada H., Sakurai N., Suzuki H., Ohyama K., Shibata D., Misawa N. Pathway engineering of Brassica napus seeds using multiple key enzyme genes involved in ketocarotenoid formation. J Exp Bot 2009, 60:1319-1332.
14. Sugiyama A., Linley P.J., Sasaki K., Kumano T., Yamamoto H., Shitan N., Ohara K., Takanashi K., Harada E., Hasegawa H., et al. Metabolic engineering for the production of prenylated polyphenols in transgenic legume plants using bacterial and plant prenyltransferases. Metab Eng 2011, 13:629-637.
15. Petrie J.R., Shrestha P., Mansour M.P., Nichols P.D., Liu Q., Singh S.P. Metabolic engineering of omega-3 long-chain polyunsaturated fatty acids in plants using an acyl-CoA Delta6-desaturase with omega3-preference from the marine microalga Micromonas pusilla. Metab Eng 2010, 12:233-240.
16. Sayanova O., Ruiz-Lopez N., Haslam R.P., Napier J.A. The role of Δ6-desaturase acyl-carrier specificity in the efficient synthesis of long-chain polyunsaturated fatty acids in transgenic plants. Plant Biotechnol J 2012, 10:195-206.
17. Tzin V., Malitsky S., Ben Zvi M.M., Bedair M., Sumner L., Aharoni A., Galili G. Expression of a bacterial feedback-insensitive 3-deoxy-D-arabino heptulosonate-7-phosphate synthase of the shikimate pathway in Arabidopsis elucidates potential metabolic bottlenecks between primary and secondary metabolism. New Phytol 2012, 194:430-439.
18. Yogev O., Pines O. Dual targeting of mitochondrial proteins: mechanism, regulation and function. Biochim Biophys Acta 2011, 1808:1012-1020.
19. Mackenzie S.A. Plant organellar protein targeting: a traffic plan still under construction. Trends Cell Biol 2005, 15:548-554.
20. Carrie C., Small I. A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Biochim Biophys Acta 2012.
21. Taira M., Valtersson U., Burkhardt B., Ludwig R.A. Arabidopsis thaliana GLN2-encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplasts. Plant Cell 2004, 16:2048-2058.
22. Guirimand G., Guihur A., Phillips M.A., Oudin A., Glévarec G., Melin C., Papon N., Clastre M., St-Pierre B., Rodríguez-Concepción M., et al. A single gene encodes isopentenyl diphosphate isomerase isoforms targeted to plastids, mitochondria and peroxisomes in Catharanthus roseus. Plant Mol Biol 2012, 79:443-459.
23. Sapir-Mir M., Mett A., Belausov E., Tal-Meshulam S., Frydman A., Gidoni D., Eyal Y. Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol 2008, 148:1219-1228.
24. Cunillera N., Boronat A., Ferrer A. The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J Biol Chem 1997, 272:15381-15388.
25. Thabet I., Guirimand G., Courdavault V., Papon N., Godet S., Dutilleul C., Bouzid S., Giglioli-Guivarc'h N., Clastre M., Simkin A.J. The subcellular localization of periwinkle farnesyl diphosphate synthase provides insight into the role of peroxisome in isoprenoid biosynthesis. J Plant Physiol 2011, 168:2110-2116.
26. Kunze R., Frommer W.B., Flügge U.I. Metabolic engineering of plants: the role of membrane transport. Metab Eng 2002, 4:57-66.
27. Linka N., Weber A.P. Intracellular metabolite transporters in plants. Mol Plant 2010, 3:21-53.
28. Häusler R.E., Schlieben N.H., Nicolay P., Fischer K., Fischer K.L., Flügge U.I. Control of carbon partitioning and photosynthesis by the triose phosphate/phosphate translocator in transgenic tobacco plants (Nicotiana tabacum L.) I. Comparative physiological analysis of tobacco plants with antisense repression and overexpression of the triose phosphate/phosphate translocator. Planta 2000, 210:371-382.
29. Bräutigam A., Hoffmann-Benning S., Hofmann-Benning S., Weber A.P. Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol 2008, 148:568-579.
30. Gowik U., Bräutigam A., Weber K.L., Weber A.P., Westhoff P. Evolution of C4 photosynthesis in the genus Flaveria: how many and which genes does it take to make C4?. Plant Cell 2011, 23:2087-2105.
31. Kajala K., Covshoff S., Karki S., Woodfield H., Tolley B.J., Dionora M.J., Mogul R.T., Mabilangan A.E., Danila F.R., Hibberd J.M., et al. Strategies for engineering a two-celled C(4) photosynthetic pathway into rice. J Exp Bot 2011, 62:3001-3010.
32. Weber A.P., von Caemmerer S. Plastid transport and metabolism of C3 and C4 plants-comparative analysis and possible biotechnological exploitation. Curr Opin Plant Biol 2010, 13:257-265.
33. Zhang L., Häusler R.E., Greiten C., Hajirezaei M.R., Haferkamp I., Neuhaus H.E., Flügge U.I., Ludewig F. Overriding the co-limiting import of carbon and energy into tuber amyloplasts increases the starch content and yield of transgenic potato plants. Plant Biotechnol J 2008, 6:453-464.
34. McNeil S.D., Rhodes D., Russell B.L., Nuccio M.L., Shachar-Hill Y., Hanson A.D. Metabolic modeling identifies key constraints on an engineered glycine betaine synthesis pathway in tobacco. Plant Physiol 2000, 124:153-162.
35. Nuccio M.L., McNeil S.D., Ziemak M.J., Hanson A.D., Jain R.K., Selvaraj G. Choline import into chloroplasts limits glycine betaine synthesis in tobacco: analysis of plants engineered with a chloroplastic or a cytosolic pathway. Metab Eng 2000, 2:300-311.
36. Chaudhuri B., Hörmann F., Lalonde S., Brady S.M., Orlando D.A., Benfey P., Frommer W.B. Protonophore- and pH-insensitive glucose and sucrose accumulation detected by FRET nanosensors in Arabidopsis root tips. Plant J 2008, 56:948-962.
37. Chen L.Q., Hou B.H., Lalonde S., Takanaga H., Hartung M.L., Qu X.Q., Guo W.J., Kim J.G., Underwood W., Chaudhuri B., et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 2010, 468:527-532.
38. Chen L.Q., Qu X.Q., Hou B.H., Sosso D., Osorio S., Fernie A.R., Frommer W.B. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 2012, 335:207-211.
39. Kim H.K., Choi Y.H., Verpoorte R. NMR-based plant metabolomics: where do we stand, where do we go?. Trends Biotechnol 2011, 29:267-275.
40. Kaspar S., Peukert M., Svatos A., Matros A., Mock H.P. MALDI-imaging mass spectrometry-an emerging technique in plant biology. Proteomics 2011, 11:1840-1850.
41. McDowell E.T., Kapteyn J., Schmidt A., Li C., Kang J.H., Descour A., Shi F., Larson M., Schilmiller A., An L., et al. Comparative functional genomic analysis of Solanum glandular trichome types. Plant Physiol 2011, 155:524-539.
42. Rogers E.D., Jackson T., Moussaieff A., Aharoni A., Benfey P.N. Cell type-specific transcriptional profiling: implications for metabolite profiling. Plant J 2012, 70:5-17.
43. Wen F., VanEtten H.D., Tsaprailis G., Hawes M.C. Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 2007, 143:773-783.
44. 13C metabolic flux analysis of plants. Phytochemistry 2007, 68:2197-2210.
45. Chaudhuri B., Hörmann F., Frommer W.B. Dynamic imaging of glucose flux impedance using FRET sensors in wild-type Arabidopsis plants. J Exp Bot 2011, 62:2411-2417.
46. Agrawal G.K., Bourguignon J., Rolland N., Ephritikhine G., Ferro M., Jaquinod M., Alexiou K.G., Chardot T., Chakraborty N., Jolivet P., et al. Plant organelle proteomics: Collaborating for optimal cell function. Mass Spectrom Rev 2010, 10.1002/mas.20301.
47. Krueger S., Giavalisco P., Krall L., Steinhauser M.C., Büssis D., Usadel B., Flügge U.I., Fernie A.R., Willmitzer L., Steinhauser D. A topological map of the compartmentalized Arabidopsis thaliana leaf metabolome. PLoS ONE 2011, 6:e17806.
48. Klie S., Krueger S., Krall L., Giavalisco P., Flügge U.I., Willmitzer L., Steinhauser D. Analysis of the compartmentalized metabolome-a validation of the non-aqueous fractionation technique. Front Plant Sci 2011, 2:55.
49. Tohge T., Ramos M.S., Nunes-Nesi A., Mutwil M., Giavalisco P., Steinhauser D., Schellenberg M., Willmitzer L., Persson S., Martinoia E., et al. Toward the storage metabolome: profiling the barley vacuole. Plant Physiol 2011, 157:1469-1482.
50. Deal R.B., Henikoff S. A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev Cell 2010, 18:1030-1040.
51. Deal R.B., Henikoff S. The INTACT method for cell type-specific gene expression and chromatin profiling in Arabidopsis thaliana. Nat Protoc 2011, 6:56-68.
52. Mintz-Oron S., Meir S., Malitsky S., Ruppin E., Aharoni A., Shlomi T. Reconstruction of Arabidopsis metabolic network models accounting for subcellular compartmentalization and tissue-specificity. Proc Natl Acad Sci U S A 2012, 109:339-344.
53. Purnick P.E., Weiss R. The second wave of synthetic biology: from modules to systems. Nat Rev Mol Cell Biol 2009, 10:410-422.
54. Naqvi S., Farré G., Sanahuja G., Capell T., Zhu C., Christou P. When more is better: multigene engineering in plants. Trends Plant Sci 2010, 15:48-56.
55. Geu-Flores F., Nielsen M.T., Nafisi M., Møldrup M.E., Olsen C.E., Motawia M.S., Halkier B.A. Glucosinolate engineering identifies a gamma-glutamyl peptidase. Nat Chem Biol 2009, 5:575-577.
56. Oey M., Lohse M., Kreikemeyer B., Bock R. Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J 2009, 57:436-445.
57. Ruhlman T., Verma D., Samson N., Daniell H. The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol 2010, 152:2088-2104.
58. Bohmert-Tatarev K., McAvoy S., Daughtry S., Peoples O.P., Snell K.D. High levels of bioplastic are produced in fertile transplastomic tobacco plants engineered with a synthetic operon for the production of polyhydroxybutyrate. Plant Phys 2011, 155:1690-1708.