Transcription factors as tools for metabolic engineering in plants

Current Opinion in Plant Biology

Volumn 7, Issue 2, 2004, Pages 202-209

  Broun, Pierre ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

AN1; ANT1; ANTHOCYANIN1; B; Basic helix loop helix; bHLH; BOOSTER; C1; CHALCONE ISOMERASE; CHALCONE SYNTHASE A; CHI; CHSA; COLORLESS1; CUC; CUP SHAPED COTYLEDON1; ERF; ETHYLENE RESPONSE FACTOR; IFS; IN1; INTENSIFIER1; Isoflavone synthase; Lc; Leaf colour; o2

Indexed keywords

ENZYME; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

GENETIC ENGINEERING; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; REVIEW; TRANSGENIC PLANT;

ENZYMES; EVOLUTION, MOLECULAR; GENETIC ENGINEERING; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; TRANSCRIPTION FACTORS;

EID: 1542351251     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2004.01.013     Document Type: Review

References (58)

1. Ruuska S.A., Girke T., Benning C., Ohlrogge J.B. Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell. 14:2002;1191-1206 The authors of this paper present a thorough analysis of gene expression during seed development in Arabidopsis, and provide thoughtful insight into the relation between the metabolic processes and changing gene expression profiles.
2. Latchman DS: Eucaryotic Transcription Factors, edn4. San Diego: Academic Press; 2003.
3. Goff S.A., Klein T.M., Roth B.A., Fromm M.E., Cone K.C., Radicella J.P., Chandler V.L. Transactivation of anthocyanin biosynthetic genes following transfer of B regulatory genes into maize tissues. EMBO J. 9:1990;2517-2522.
4. Mahmoud S.S., Croteau R.B. Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proc Natl Acad Sci USA. 98:2001;8915-8920.
5. Falco S.C., Guida T., Locke M., Mauvais J., Sanders C., Ward R.T., Webber P. Transgenic canola and soybean seeds with increased lysine. Biotechnology. 13:1995;577-582.
6. Dong X., Braun E.L., Grotewold E. Functional conservation of plant secondary metabolic enzymes revealed by complementation of Arabidopsis flavonoid mutants with maize genes. Plant Physiol. 127:2001;46-57.
7. Fraser P.D., Romer S., Shipton C.A., Mills P.B., Kiano J.W., Misawa N., Drake R.G., Schuch W., Bramley P.M. Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc Natl Acad Sci USA. 99:2002;1092-1097.
8. Shewmaker C.K., Sheehy J.A., Daley M., Colburn S., Ke D.Y. Seed-specific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects. Plant J. 20:1999;401-412.
9. Ye X., Al-Babili S., Kloti A., Zhang J., Lucca P., Beyer P., Potrykus I. Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science. 287:2000;303-305.
10. Muir S.R., Collins G.J., Robinson S., Hughes S., Bovy A., Ric De Vos C.H., van Tunen A.J., Verhoeyen M.E. Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat Biotechnol. 19:2001;470-474.
11. Bovy A., de Vos R., Kemper M., Schijlen E., Almenar Pertejo M., Muir S., Collins G., Robinson S., Verhoeyen M., Hughes S.et al. High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell. 14:2002;2509-2526 This study exemplifies the potential of transcription factors for the metabolic engineering of an important pathway in a crop plant. The authors present a detailed analysis of metabolic and gene expression changes that occur as the result of transcription-factor overexpression in the fruit of transgenic tomato plants.
12. Grotewold E., Chamberlin M., Snook M., Siame B., Butler L., Swenson J., Maddock S., Clair G.S., Bowen B. Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell. 10:1998;721-740.
13. Goldsbrough A.P., Tong Y., Yoder J.I., Tong Y.S. Lc as a non-destructive visual reporter and transposition excision marker gene for tomato. Plant J. 9:1996;927-933.
14. Mooney M., Desnos T., Harrison K., Jones J., Carpenter R., Coen E. Altered regulation of tomato and tobacco pigmentation genes caused by the delila gene of Antirrhinum. Plant J. 7:1995;333-339.
15. Lloyd A.M., Walbot V., Davis R.W. Arabidopsis and Nicotiana anthocyanin production activated by maize regulators R and C1. Science. 258:1992;1773-1775.
16. Nesi N., Jond C., Debeaujon I., Caboche M., Lepiniec L. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell. 13:2001;2099-2114.
17. Nesi N., Debeaujon I., Jond C., Pelletier G., Caboche M., Lepiniec L. The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell. 12:2000;1863-1878.
18. Yu O., Shi J., Hession A.O., Maxwell C.A., McGonigle B., Odell J.T. Metabolic engineering to increase isoflavone biosynthesis in soybean seed. Phytochemistry. 63:2003;753-763 Yu et al. present a strategy that combines the overexpression of the transcription factors R and C1 (in the form of the fusion protein CRC) with the silencing of a structural enzyme, flavanone 3-hydroxylase. The consequences for metabolism and gene expression are analysed in detail. The authors achieve significant increases in the isoflavone content of transgenic soybean seeds.
19. Yu O., Jung W., Shi J., Croes R.A., Fader G.M., McGonigle B., Odell J.T. Production of the isoflavones genistein and daidzein in non-legume dicot and monocot tissues. Plant Physiol. 124:2000;781-794.
20. 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.
21. Bruce W., Folkerts O., Garnaat C., Crasta O., Roth B., Bowen B. Expression profiling of the maize flavonoid pathway genes controlled by estradiol-inducible transcription factors CRC and P. Plant Cell. 12:2000;65-80.
22. Debeaujon I., Peeters A.J., Leon-Kloosterziel K.M., Koornneef M. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell. 13:2001;853-871.
23. Mathews H., Clendennen S.K., Caldwell C.G., Liu X.L., Connors K., Matheis N., Schuster D.K., Menasco D.J., Wagoner W., Lightner J.et al. Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell. 15:2003;1689-1703 Mathews et al. use an activation-tagging approach to isolate a gene encoding ANT1, a putative C1 orthologue. They present a very detailed analysis of metabolic and expression profiles. Using a suppression subtractive hybridisation approach, the authors also isolated novel genes, some of which may play a role in the intracellular transport of flavonoids.
24. Spelt C., Quattrocchio F., Mol J., Koes R. ANTHOCYANIN1 of petunia controls pigment synthesis, vacuolar pH, and seed coat development by genetically distinct mechanisms. Plant Cell. 14:2002;2121-2135 This study identifies new roles for AN1, a transcriptional activator of anthocyanin biosynthesis in petunia. In particular, the authors demonstrate that AN1 also controls vacuolar pH (it is allelic to PH6) and seed coat morphogenesis. The study illustrates the diversity of cellular functions that may be affected by a transcription factor that controls a metabolic pathway.
25. Broun P, Poindexter P, Osborne E, Jiang C-Z, Riechmann JL: WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA 2004, in press.
26. Schmidt R.J., Burr F.A., Aukerman M.J., Burr B. Maize regulatory gene opaque-2 encodes a protein with a 'leucine-zipper' motif that binds to zein DNA. Proc Natl Acad Sci USA. 87:1990;46-50.
27. Hunter B.G., Beatty M.K., Singletary G.W., Hamaker B.R., Dilkes B.P., Larkins B.A., Jung R. Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell. 14:2002;2591-2612.
28. Kawaoka A., Kaothien P., Yoshida K., Endo S., Yamada K., Ebinuma H. Functional analysis of tobacco LIM protein Ntlim1 involved in lignin biosynthesis. Plant J. 22:2000;289-301.
29. Burr F.A., Burr B., Scheffler B.E., Blewitt M., Wienand U., Matz E.C. The maize repressor-like gene intensifier1 shares homology with the r1/b1 multigene family of transcription factors and exhibits missplicing. Plant Cell. 8:1996;1249-1259.
30. Tamagnone L., Merida A., Parr A., Mackay S., Culianez-Macia F.A., Roberts K., Martin C. The AmMYB308 and AmMYB330 transcription factors from antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell. 10:1998;135-154.
31. Jin H., Cominelli E., Bailey P., Parr A., Mehrtens F., Jones J., Tonelli C., Weisshaar B., Martin C. Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J. 19:2000;6150-6161.
32. Aharoni A., De Vos C.H., Wein M., Sun Z., Greco R., Kroon A., Mol J.N., O'Connell A.P. The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J. 28:2001;319-332.
33. Quattrocchio F., Wing J.F., van der Woude K., Mol J.N., Koes R. Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J. 13:1998;475-488.
34. Borevitz J.O., Xia Y., Blount J., Dixon R.A., Lamb C. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell. 12:2000;2383-2394.
35. Zhang F., Gonzalez A., Zhao M., Payne C.T., Lloyd A. A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development. 130:2003;4859-4869.
36. van der Fits L., Memelink J. ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science. 289:2000;295-297.
37. Quattrocchio F., Wing J.F., Leppen H., Mol J., Koes R.E. Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. Plant Cell. 5:1993;1497-1512.
38. Zhang J.Z. Overexpression analysis of plant transcription factors. Curr Opin Plant Biol. 6:2003;430-440.
39. Lloyd A.M., Schena M., Walbot V., Davis R.W. Epidermal cell fate determination in Arabidopsis: patterns defined by a steroid-inducible regulator. Science. 266:1994;436-439.
40. Gilmour S.J., Sebolt A.M., Salazar M.P., Everard J.D., Thomashow M.F. Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol. 124:2000;1854-1865.
41. Zuber M.E., Perron M., Philpott A., Bang A., Harris W.A. Giant eyes in Xenopus laevis by overexpression of XOptx2. Cell. 98:1999;341-352.
42. Ohashi Y., Brickman J.M., Furman E., Middleton B., Carey M. Modulating the potency of an activator in a yeast in vitro transcription system. Mol Cell Biol. 14:1994;2731-2739.
43. Seipel K., Georgiev O., Schaffner W. Different activation domains stimulate transcription from remote ('enhancer') and proximal ('promoter') positions. EMBO J. 11:1992;4961-4968.
44. Schwechheimer C., Smith C., Bevan M.W. The activities of acidic and glutamine-rich transcriptional activation domains in plant cells: design of modular transcription factors for high-level expression. Plant Mol Biol. 36:1998;195-204.
45. Aoyama T., Dong C.H., Wu Y., Carabelli M., Sessa G., Ruberti I., Morelli G., Chua N.H. Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco. Plant Cell. 7:1995;1773-1785.
46. Parcy F., Nilsson O., Busch M.A., Lee I., Weigel D. A genetic framework for floral patterning. Nature. 395:1998;561-566.
47. Markel H., Chandler J., Werr W. Translational fusions with the engrailed repressor domain efficiently convert plant transcription factors into dominant-negative functions. Nucleic Acids Res. 30:2002;4709-4719 This study demonstrates the potential of using the repressor domain of the Drosophila transcription factor ENGRAILED to convert transcription factors into dominant repressors. The technology is validated using a variety of known transcription factors.
48. •], in which the authors exploit repressor domains that are found in several Arabidopsis transcription factors. The strategy is validated using a number of unrelated transcription factors, showing the potential of this tool for the functional characterisation of a wide range of transcription factors of unknown function.
49. Ludwig S.R., Habera L.F., Dellaporta S.L., Wessler S.R. Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. Proc Natl Acad Sci USA. 86:1989;7092-7096.
50. Dellaporta SL, Wood J, Hicks JB: Molecular cloning of the maize R-nj allele by transposon-tagging with Ac. In Chromosome Structure and Function: Impact of New Concepts, 18th Stadler Genetics Symposium. Edited by Gustafson JP, Appels R. New York: Plenum Press; 1988:263-282.
51. Chandler V.L., Radicella J.P., Robbins T.P., Chen J., Turks D. Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. Plant Cell. 1:1989;1175-1183.
52. Cone K.C., Burr F.A., Burr B. Molecular analysis of the maize anthocyanin regulatory locus C1. Proc Natl Acad Sci USA. 83:1986;9631-9635.
53. Cone K.C., Cocciolone S.M., Burr F.A., Burr B. Maize anthocyanin regulatory gene pl is a duplicate of c1 that functions in the plant. Plant Cell. 5:1993;1795-1805.
54. Goodrich J., Carpenter R., Coen E.S. A common gene regulates pigmentation pattern in diverse plant species. Cell. 68:1992;955-964.
55. Spelt C., Quattrocchio F., Mol J.N., Koes R. Anthocyanin1 of petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell. 12:2000;1619-1632.
56. Quattrocchio F., Wing J., van der Woude K., Souer E., de Vetten N., Mol J., Koes R. Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell. 11:1999;1433-1444.
57. Kubo H., Peeters A.J., Aarts M.G., Pereira A., Koornneef M. ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell. 11:1999;1217-1226.
58. Bender J., Fink G.R. A Myb homologue, ATR1, activates tryptophan gene expression in Arabidopsis. Proc Natl Acad Sci USA. 95:1998;5655-5660.