Engineering secondary metabolism in maize cells by ectopic expression of transcription factors

Plant Cell

Volumn 10, Issue 5, 1998, Pages 721-740

  Grotewold, Erich ^a,e   Chamberlin, Mark ^b   Snook, Maurice ^c   Siame, Bupe ^d   Butler, Larry ^d   Swenson, Jan ^b   Maddock, Sheila ^b   St Clair, Grace ^b   Bowen, Ben ^b  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b PIONEER HI BRED INTERNATIONAL INC   (United States)

^c RUSSELL RESEARCH CENTER   (United States)

^d PURDUE UNIVERSITY   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENETIC ENGINEERING; GENETIC TRANSCRIPTION; MAIZE; PLANT CELL CULTURE;

EMBRYOPHYTA; INSECTA; ZEA MAYS;

EID: 0031772791     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.10.5.721     Document Type: Article

References (90)

1. Alfermann, A.W., and Petersen, M. (1995). Natural product formation by plant cell biotechnology. Plant Cell Tiss. Organ Cult. 43, 199-205.
2. ap Rees, T. (1995). Prospects of manipulating plant metabolism. Trends Biotechnol. 13, 375-378.
3. Athma, P., and Peterson, T. (1991). Ac induces homologous recombination at the maize P locus. Genetics 128, 163-173.
4. Athma, P., Grotewold, E., and Peterson, T. (1992). Insertional mutagenesis of the maize P gene by intragenic transposition of Ac. Genetics 131, 199-209.
5. Bennett, M.K. (1995). SNAREs and the specificity of transport vesicle targeting. Curr. Opin. Cell Biol. 7, 581-586.
6. Bennett, M.K., and Scheller, R.H. (1994). A molecular description of synaptic vesicle membrane trafficking. Annu. Rev. Biochem. 63, 63-100.
7. Bodeau, J.P., and Walbot, V. (1992). Regulated transcription of the maize Bronze-2 promoter in electroporated protoplasts requires the C1 and R gene products. Mol. Gen. Genet. 233, 379-387.
8. Bowen, B. (1992). Anthocyanin genes as visual markers in transformed maize tissues. In GUS Protocols: Using the GUS Gene as a Reporter of Gene Expression, S.R. Gallagher, ed (San Diego, CA: Academic Press), pp. 163-177.
9. Britsch, L. (1990). Purification and characterization of flavone synthase I, a 2-oxoglutarate-dependent desaturase. Arch. Biochem. Biophys. 282, 152-160.
10. Byrne, P.F., Darrah, L.L., Snook, M.E., Wiseman, B.R., Widstrom, N.W., Moellenbeck, D.J., and Barry, B.D. (1996a). Maize silkbrowning, maysin content, and antibiosis to the corn earworm, Helicoverpa zea (Boddie). Maydica 41, 13-18.
11. Byrne, P.F., McMullen, M.D., Snook, M.E., Musket, T.A., Theuri, J.M., Widstrom, N.W., Wiseman, B.R., and Coe, E.H., Jr. (1996b). Quantitative trait loci and metabolic pathways: Genetic control of the concentration of maysin, a corn earworm resistance factor, in maize silks. Proc. Natl. Acad. Sci. USA 93, 8820-8825.
12. Campbell, M.M., and Sederoff, R.R. (1996). Variation in lignin content and composition. Plant Physiol. 110, 3-13.
13. Chopra, S., Athma, P., and Peterson, T. (1996). Alleles of the maize P gene with distinct tissue specificities encode Myb-homologous proteins with C-terminal replacements. Plant Cell 8, 1149-1158.
14. Christensen, A.M., Sharrock, R.A., and Quail, P.M. (1992). Maize polyubiquitin genes: Structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol. Biol. 18, 675-689.
15. Coe, E.H., Jr., Neuffer, M.G., and Hoisington, D.A. (1988). The genetics of corn. In Corn and Corn Improvement, 3rd ed, G.F. Sprague and J. Dudley, eds (Madison, WI: American Society of Agronomy), pp. 81-258.
16. Deboo, G.B., Albertsen, M.C., and Taylor, L.P. (1995). Flavanone 3-hydroxylase transcripts and flavonol accumulation are temporally coordinate in maize anthers. Plant J. 7, 703-713.
17. Dooner, H.K., Weck, E., Adams, S., Ralston, E., Favreau, M., and English, J. (1985). A molecular genetic analysis of insertions in the bronze locus in maize. Mol. Gen. Genet. 200, 240-246.
18. Dooner, H.K., Robbins, T.P., and Jorgensen, R.A. (1991). Genetic and developmental control of anthocyanin biosynthesis. Annu. Rev. Genet. 25, 173-199.
19. Dörnenburg, H., and Knorr, D. (1996). Generation of colors and flavors in plant cell and tissue cultures. Crit. Rev. Plant Sci. 15, 141-168.
20. Eberhardt, T.L., Bernards, M.A., He, L., Davin, L.B., Wooten, J.B., and Lewis, N.G. (1993). Lignification in cell suspension cultures of Pinus taeda. J. Biol. Chem. 28, 21088-21096.
21. Elliger, C.A., Chan, B.G., Waiss, A.C., Lundin, R.E., and Haddon, W.F. (1980). C-Glycosyl flavones from Zea mays that inhibit insect development. Phytochemistry 19, 293-297.
22. Forkmann, G. (1991). Flavonoids as flower pigments: The formation of the natural spectrum and its extension by genetic engineering. Plant Breed. 106, 1-26.
23. Forkmann, G., and Dangelmayr, B. (1980). Genetic control of chalcone isomerase activity in flowers of Dianthus caryophyllus. Biochem. Genet. 18, 519-527.
24. Goff, S.A., Klein, T.M., Roth, B.A., Fromm, M.E., Cone, K.C., Radicella, J.P., and Chandler, V.L. (1990). Transactivation of anthocyanin biosynthetic genes following transfer of B regulatory genes into maize tissues. EMBO J. 9, 2517-2522.
25. Grotewold, E., and Peterson, T. (1994). Isolation and characterization of a maize gene encoding chalcone flavanone isomerase. Mol. Gen. Genet. 242, 1-8.
26. Grotewold, E., Athma, P., and Peterson, T. (1991a). Alternatively spliced products of the maize P gene encode proteins with homology to the DNA binding domain of Myb-like transcription factors. Proc. Natl. Acad. Sci. USA 88, 4587-4591.
27. Grotewold, E., Athma, P., and Peterson, T. (1991b). A possible hotspot for Ac insertion in the maize P gene. Mol. Gen. Genet. 230, 329-331.
28. Grotewold, E., Drummond, B., Bowen, B., and Peterson, T. (1994). The Myb-homologous P gene controls phobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76, 543-553.
29. Harborne, J.B., ed (1988). The Flavonoids: Advances in Research since 1980. (New York: Chapman and Hall).
30. Heller, W., and Forkmann, G. (1988). Biosynthesis. In The Flavonoids: Advances in Research since 1980, J.B. Harborne, ed (New York: Chapman and Hall), pp. 399-425.
31. Herbers, K., and Sonnewald, U. (1996). Manipulating metabolic partitioning in transgenic plants. Trends Biotechnol. 14, 198-205.
32. Herman, E.M., and Lamb, C.J. (1992). Arabinogalactan-rich glycoproteins are localized on the cell surface and in intravacuolar multivesicular bodies. Plant Physiol. 98, 264-272.
33. Howles, P.A., Sewalt, V.J.H., Paiva, N.L., Elkind, Y., Bate, N.J., Lamb, C., and Dixon, R.A. (1996). Overexpression of L-phenylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol. 112, 1617-1624.
34. Hrazdina, G., and Jensen, R.A. (1992). Spatial organization of enzymes in plant metabolic pathways. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 241-267.
35. Kacser, H., and Burns, J.A. (1973). The control of flux. Symp. Soc. Exp. Biol. 27, 65-104.
36. Kacser, H., and Burns, J.A. (1981). The molecular basis of dominance. Genetics 97, 639-666.
37. Kerscher, F., and Franz, G. (1987). Biosynthesis of vitexin and isovitexin: Enzymatic synthesis of the C-glucosyl flavones vitexin and isovitexin with an enzymatic preparation from Fagopyrum esculentum M. seedlings. Z. Naturforsch. 42c, 519-524.
38. Kerscher, F., and Franz, G. (1988). Isolation and some properties of an UDP-glucose:2-hydroxyflavanone-6(or 8)-C-glucosyltransferase from Fagopyrum esculentum M. cotyledons. J. Plant Physiol. 132, 110-115.
39. Klein, M., Weissenboeck, G., Dufaud, A., Gaillard, C., Kreuz, K., and Martinoia, E. (1996). Different energization mechanisms drive the vacuolar uptake of a flavonoid glycoside and a herbicide glucoside. J. Biol. Chem. 271, 29666-29671.
40. Koes, R.E., Quattrocchio, F., and Mol, J.N.M. (1994). The flavonoid biosynthetic pathway in plants: Function and evolution. Bioessays 16, 123-132.
41. Larson, R.L. (1989). Flavonoid 3′-O-methylation by a Zea mays L. preparation. Biochem. Physiol. Pflanz. 184, 453-460.
42. Larson, R.L., and Coe, E.H. (1977). Gene-dependent flavonoid glucosyltransferase in maize. Biochem. Genet. 15, 153-156.
43. Larson, R.L., Bussard, J.B., and Coe, E.H., Jr. (1986). Genedependent flavonoid 3′-hydroxylation in maize. Biochem. Genet. 24, 615-624.
44. Les, D.H., and Sheridan, D.J. (1990). Biochemical heterophylly and flavonoid evolution in North American Potamogeton (Potamogetonaceae). Am. J. Bot. 77, 453-465.
45. Levings, C.S., and Stuber, C.W. (1971). A maize gene controlling silk browning in response to wounding. Genetics 69, 491-498.
46. Lloyd, A.M., Walbot, V., and Davis, R.W. (1992). Arabidopsis and Nicotiana anthocyanin production activated by maize regulators R and C1. Science 258, 1773-1775.
47. Luckner, M., ed (1990). Secondary Metabolism in Microorganisms, Plants, and Animals, 3rd ed. (Berlin: Springer-Verlag).
48. Ludwig, S.R., Bowen, B., Beach, L., and Wessler, S.R. (1990). A regulatory gene as a novel visible marker for maize transformation. Science 247, 449-450.
49. Marrs, K.A., Alfenito, M.R., Lloyd, A.M., and Walbot, V. (1995). A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375, 397-400.
50. Menssen, A., Hohmann, S., Martin, W., Schnable, P.S., Peterson, P.A., Saedler, H., and Gierl, A. (1990). The En/Spm transposable element of Zea mays contains splice sites at the termini generating a novel intron from a dSpm element in the A2 gene. EMBO J. 9, 3051-3057.
51. Middleton, E. (1996). The flavonoids as potential therapeutic agents. In Immunopharmaceuticals, E.S. Kimball, ed (Boca Raton, FL: CRC Press), pp. 227-257.
52. Mol, J.N.M., Robbins, M.P., Dixon, R.A., and Veitkamp, E. (1985). Spontaneous and enzymic rearrangement of naringenin chalcone to flavanone. Phytochemistry 24, 2267-2269.
53. Moreno, M.A., Chen, J., Greenblatt, I., and Dellaporta, S.L. (1992). Reconstitutional mutagenesis of the maize P gene by short range Ac transpositions. Genetics 131, 939-956.
54. Moustafa, E., and Wong, E. (1967). Purification and properties of chalcone-flavanone isomerase from soya bean seed. Phytochemistry 6, 625-632.
55. Moyano, E., Martínez-Garcia, J.F., and Martin, C. (1996). Apparent redundancy in myb gene function provides gearing for the control of flavonoid biosynthesis in Antirrhinum flowers. Plant Cell 8, 1519-1532.
56. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
57. Nash, J., Luehrsen, K.R., and Walbot, V. (1990). Bronze-2 gene of maize: Reconstruction of a wild-type allele and analysis of transcription and splicing. Plant Cell 2, 1039-1049.
58. Niederberger, P., Prasad, R., Miozzari, G., and Kacser, H. (1992). A strategy for increasing an in vivo flux by genetic manipulations. Biochem. J. 287, 473-479.
59. Nozzolillo, C., and Ishikura, N. (1988). An investigation of the intracellular site of anthocyanoplasts using isolated protoplasts and vacuoles. Plant Cell Rep. 7, 389-392.
60. Paris, N., Stanley, C.M., Jones, R.L., and Rogers, J.C. (1996). Plant cells contain two functionally distinct vacuolar compartments. Cell 85, 563-572.
61. Pecket, C.R., and Small, C.J. (1980). Occurrence, location and development of anthocyanoplasts. Phytochemistry 19, 2571-2576.
62. Quattrocchio, F., Wing, J.F., Leppen, H.T.C., Mol, J.N.M., and Koes, R.E. (1993). Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. Plant Cell 5, 1497-1512.
63. Ralph, J., Quideau, S., Grabber, J.H., and Hatfield, R.D. (1994). Identification and synthesis of new ferulic acid dehydrodimers present in grass cell walls. J. Chem. Soc. Perkin Trans. 1, 3485-3498.
64. Ramarathnam, N., Osawa, T., Namiki, M., and Kawakishi, S. (1989). Chemical studies on novel rice hull antioxidants. 2. Identification of isovitexin, a C-glycosyl flavonoid. J. Agric. Food Chem. 37, 316-319.
65. Randolph, L.F. (1936), Developmental morphology of the caryopsis in maize. J. Agric. Res. 53, 881-917.
66. Reid, L.M., Mather, D.E., Arnason, J.T., Hamilton, R.I., and Bolton, A.T. (1992). Changes in phenolic constituents of maize silk infected with Fusarium graminearum. Can. J. Bot. 70, 1697-1702.
67. Schwarz-Sommer, Z., Shepherd, N., Tacke, E., Gierl, A., Rohde, W., Leclercq, L., Mattes, M., Berndtgen, R., Peterson, P.A., and Saedler, H. (1987). Influence of transposable elements on the structure and function of the A1 gene of Zea mays. EMBO J. 6, 287-294.
68. Sheridan, W.F. (1982). Black Mexican Sweet corn: Its use for tissue culture. In Maize for Biological Research, W.F. Sheridan, ed (Charlottesville, VA: Plant Molecular Biology Association), pp. 385-388.
69. Shibamoto, T., Hagiwara, Y., Hagiwara, H., and Osawa, T. (1994). Flavonoid with strong antioxidative activity isolated from young green barley leaves. Am. Chem. Soc. Symp. Ser. 547, 153-163.
70. Shirley, B.W. (1996). Flavonoid biosynthesis: 'New' functions for an 'old' pathway. Trends Plant Sci. 1, 377-382.
71. Snook, M.E., Widstrom, N.W., and Gueldner, R.C. (1989). Reversed-phase high-performance liquid chromatographic procedure for the determination of maysin in corn silks. J. Chromatogr. 477, 439-447.
72. Snook, M.E., Widstrom, N.W., Wiseman, B.R., Byrne, P.F., Harwood, J.S., and Costello, C.E. (1995). New C-4″-hydroxy derivatives of maysin and 3′-methoxymaysin isolated from corn silks (Zea mays). J. Agric. Food Chem. 43, 2740-2745.
73. Snyder, B.A., and Nicholson, R.L. (1990). Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science 248, 1637-1639.
74. Stafford, H.A. (1990). Flavonoid Metabolism. (Boca Raton, FL: CRC Press).
75. Stich, K., and Forkmann, G. (1988). Biosynthesis of 3-deoxyanthocyanins with flower extracts from Sinningia cardinalis. Biochemistry 27, 785-789.
76. Styles, E.D., and Ceska, O. (1975). Genetic control of 3-hydroxyand 3-deoxy-flavonoids in Zea mays. Phytochemistry 14, 413-415.
77. Styles, E.D., and Ceska, O. (1977). The genetic control of flavonoid synthesis in maize. Can. J. Genet. Cytol. 19, 289-302.
78. Styles, E.D., and Ceska, O. (1989). Pericarp flavonoids in genetic strains of Zea mays. Maydica 34, 227-237.
79. Tevini, M., Braun, J., and Fieser, G. (1991). The protective function of the epidermal layer of rye seedlings against ultraviolet-B radiation. Photochem. Photobiol. 53, 329-333.
80. Tobias, R.B., and Larson, R.L. (1991). Characterization of maize pollen fiavonoid 3′-O-methyltransferase activity and its in vivo products. Biochem. Physiol. Pflanz. 187, 243-250.
81. Tuerck, J.A., and Fromm, M.E. (1994). Elements of the maize A1 promoter required for transactivation by the anthocyanin B/C1 or phlobaphene P regulatory genes. Plant Cell 6, 1655-1663.
82. Van der Meer, I.M., Stuitje, A.R., and Mol, J.N.M. (1993). Regulation of general phenylpropanoid and flavonoid gene expression. In Control of Plant Gene Expression, D.P.S. Verma, ed (Boca Raton, FL: CRC Press), pp. 125-155.
83. Van Tunen, A.J., Mur, L.A., Recourt, K., Gerats, A.G.M., and Mol, J.N.M. (1991). Regulation and manipulation of flavonoid gene expression in anthers of petunia: The molecular basis of the po mutation. Plant Cell 3, 39-48.
84. Wagner, A.M., and Van Brederode, J. (1996). Inhibition of mitochondrial respiration by the flavone aglycone isovitexin causes aberrant petal and leaf morphology in Silene latifolia. Plant Cell Rep. 15, 718-722.
85. Waiss, A.C., Jr., Chan, B.G., Elliger, C.A., Wiseman, B.R., McMillian, W.W., Widstrom, N.W., Zuber, M.S., and Keaster, A.J. (1979). Maysin, a flavone glycoside from corn silks with antibiotic activity toward corn earworm. J. Econ. Entomol. 72, 256-258.
86. Watterson, J.J., and Butler, L.G. (1983). Occurrence of an unusual leucoanthocyanidin and absence of proanthocyanidins in sorghum leaves. J. Agric. Food Chem. 31, 41-45.
87. Whetten, R., and Sederoff, R. (1995). Lignin biosynthesis. Plant Cell 7, 1001-1013.
88. Wienand, U., Weydemann, U., Niesbach-Klösgen, U., Peterson, P., and Saedler, H. (1986). Molecular cloning of the c2 locus of Zea mays, the gene encoding chalcone synthase. Mol. Gen. Genet. 203, 202-207.
89. Yeoman, M.M., and Yeoman, C.L. (1996). Manipulating secondary metabolism in cultured plant cells. New Phytol. 134, 553-569.
90. Ylstra, B., Busscher, J., Franken, J., Hollman, P.C.H., Mol, J.N.M., and Van Tunen, A.J. (1994). Flavonols and fertilization in Petunia hybrida: Localization and mode of action during pollen tube growth. Plant J. 6, 201-212.