Molecular analysis of herbivore-induced condensed tannin synthesis: Cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides)

Plant Journal

Volumn 32, Issue 5, 2002, Pages 701-712

  Peters, Darren J ^a   Constabel, C Peter ^b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Forest tree; Herbivory; Plant defense; Proanthocyanidins

Indexed keywords

BACTERIA; CLONING; DNA; ENZYMES;

HERVIBORES;

PLANTS (BOTANY);

ALCOHOL OXIDOREDUCTASES; AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; ENZYME INDUCTION; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HYDROLYZABLE TANNINS; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MOTHS; PLANT DISEASES; POPULUS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TIME FACTORS;

BACTERIA (MICROORGANISMS); EMBRYOPHYTA; EUKARYOTA; LEPIDOPTERA; MALACOSOMA; MALACOSOMA DISSTRIA; POPULUS; POPULUS TREMULOIDES; STILPNOTIA SALICIS;

EID: 0036914168     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2002.01458.x     Document Type: Article

References (49)

1. Arnold, T.M. and Schultz, J.C. (2002) Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia, 130, 585-593.
2. Ayres, M.P., Clausen, T.P., MacLean,S.F., Jr, Redman, A.M. and Reichardt, P.B. (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology, 78, 1696-1712.
3. Barbehenn, R.V. and Martin, M.M. (1994) Tannin sensitivity of larvae of Malacosoma disstria (Lepidoptera): Roles of the peritrophic envelope and midgut oxidation. J. Chem. Ecol. 8, 1985-2001.
4. Bergey, D.R., Howe, G.A. and Ryan, C.A. (1996) Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc. Natl. Acad. Sci. USA, 93, 12053-12058.
5. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal. Biochem. 71, 248-254.
6. Bradshaw, H.D., Jr, Hollick, J.B., Parsons, T.J., Clarke, H.R.G. and Gordon, M.P. (1989) Systemically wound-responsive genes in poplar trees encode proteins similar to sweet potato sporamins and legume Kunitz trypsin inhibitors. Plant Mol. Biol. 14, 51-59.
7. Burbulis, I.E. and Winkel-Shirley, B. (1999) Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proc. Natl. Acad. Sci. USA, 96, 12929-12934.
8. Constabel, C.P. (1999) A survey of herbivore-inducible defensive proteins and phytochemicals. In Induced Plant Defenses Against Herbivores and Pathogens (Agrawaal, A.A., Tuzun, S. and Bent, E., eds). St. Paul: APS Press, pp. 137-166.
9. Constabel, C.P., Yip, L., Patton, J.J. and Christopher, M.E. (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol. 124, 285-295.
10. Devic, M., Guilleminot, J., Debeaujon, I., Bechtold, N., Bensaude, E., Koornneef, M., Pelletier, G. and Delseny, M. (1999) The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. Plant J. 19, 387-398.
11. Dixon, R.A. and Paiva, N.L. (1995) Stress-induced phenylpropanoid metabolism. Plant Cell, 7, 1085-1097.
12. Duffey, S.S. and Felton, G.W. (1991) Enzymatic antinutritive defenses of the tomato plant against insects. In Naturally Occurring Pest Bioregulators (Hedin, P.A., ed.). Washington, DC: ACS Press, pp. 167-197.
13. Gíner-Chavez, B.I., Van Soest, P.J., Robertson, J.B., Lascano, C. and Pell, A.N. (1997) Comparison of the precipitation of alfalfa leaf protein and bovine serum albumin by tannins in the radial diffusion method. J. Sci. Food Agric. 74, 513-523.
14. Gruppe, A., Fusseder, M. and Schopf, R. (1999) Short rotation plantations of aspen and balsam poplar on former arable land in Germany: Defoliating insects and leaf constituents. For. Ecol. Manag. 121, 113-122.
15. Hagerman, A.E. (1987) Radial diffusion method for determining tannin in plant extracts. J. Chem. Ecol. 13, 437-449.
16. Hagerman, A.E. and Butler, L.G. (1989) Choosing appropriate methods and standards for assaying tannins. J. Chem. Ecol. 15, 1795-1810.
17. Hagerman, A.E. and Butler, L.G. (1991) Tannins and lignins. In Herbivores: Their Interaction with Secondary Plant Metabolites, Vol. I (Rosenthal, G.A. and Berenbaum, M.R., eds). San Diego: Academic Press, pp. 355-387.
18. Hahlbrock, K. and Scheel, D. (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 347-369.
19. Harmer, S.L. Hogenesch, J.B., Straume, M., Chang, H.-S., Han, B., Zhu, T., Wang, X., Kreps, J.A. and Kay, S.A. (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science, 290, 2110-2113.
20. Hartley, S.E. and Lawton, J.H. (1991) Biochemical aspects and significance of the rapidly induced accumulation of phenolics in birch foliage. In Phytochemical Induction by Herbivores (Tallamy, D.W. and Raupp, M.J., eds). New York: John Wiley, pp. 105-132.
21. Haruta, M., Major, I.T., Christopher, M.E., Patton, J.J. and Constabel, C.P. (2001a) A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): Cloning, functional expression, and induction by wounding and herbivory. Plant Mol. Biol. 46, 347-359.
22. Haruta, M., Pedersen, J.A. and Constabel, C.P. (2001b) Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol. Plant. 112, 552-558.
23. Hasegawa, H., Fukasawa-Akada, T., Okuno, T., Niizeki, M. and Suzuki, M. (2001) Anthocyanin accumulation and related gene expression in Japanese parsley (Oenanthe stolonifera, DC.) induced by low temperature. J. Plant Physiol. 158, 71-78.
24. Haslam, E. (1993) Polyphenols: Phytochemical chameleons. In Phytochemistry and Agriculture (van Beek, T.A. and Breteler, H., eds). Oxford: Clarendon Press, pp. 215-262.
25. Hemming, J.D.C. and Lindroth, R.L. (1995) Intraspecific variation in aspen phytochemistry: Effects on performance of gypsy moths and forest tent caterpillars. Oecologia, 103, 79-88.
26. Hu, W.-J., Kawaoka, A., Tsai, C.-J., Lung, J., Osakabe, K., Ebinuma, H. and Chiang, V.L. (1998) Compartmentalized expression of two structurally and functionally distinct 4-coumarate: CoA ligase genes in aspen (Populus tremuloides). Proc. Natl. Acad. Sci. USA, 95, 5407-5412.
27. Hwang, S.-Y. and Lindroth, R.L. (1997) Clonal variation in foliar chemistry of aspen: Effects on gypsy moths and forest tent caterpillars. Oecologia, 111, 99-108.
28. Ives, W.G.H. and Wong, H.R. (1988) Tree and Shrub Insects of the Prairie Provinces. Information report NOR-X-292. Edmonton: Canadian Forestry Service.
29. Johnson, E.T., Ryu, S., Yi, H., Shin, B., Cheong, H. and Choi, G. (2001) Alteration of a single amino acid changes the substrate specificity of dihydroflavonol 4-reductase. Plant J. 25, 325-333.
30. Karban, R. and Baldwin, I.T. (1997) Induced Reponses to Herbivory. Chicago: The University of Chicago Press.
31. Koupai-Abyazani, M.R., McCallum, J., Muir, A.D., Bohm, B.A., Towers, G.H.N. and Gruber, M.Y. (1993) Developmental changes in the composition of proanthocyanidins from leaves of sainfoin (Onobrychis viciifolia Scop.) as determined by HPLC analysis. J. Agric. Food Chem. 41, 1066-1070.
32. Lacombe, E., Hawkins, S., Doorsselaere, J.V., Piquemal, J., Goffner, D., Poeydomenge, O., Boudet, A.-M. and Grima-Pattenati, J. (1997) Cinnamoyl CoA reductase, the first committed enzyme of the lignin branch biosynthetic pathway: Cloning, expression and phylogenetic relationships. Plant J. 11, 429-441.
33. Larson, P.R. and Isebrands, J.G. (1971) The plastochron index as applied to developmental studies of cottonwood. Can. J. For. Res. 1, 1-11.
34. Lindroth, R.L. and Hwang, S.-Y. (1996) Diversity, redundancy, and multiplicity in chemical defense systems of aspen. In Phytochemical Diversity and Redundancy in Ecological Interactions (Romeo, J.T., Saunders, J.A. and Barbosa, P., eds). New York: Plenum Press, pp. 25-56.
35. Marchuk, D., Drumm, M., Saulino, A. and Collins, F.S. (1991) Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucl. Acids Res. 19, 1154.
36. Olsen, O., Wang, X. and von Wettstein, D. (1993) Sodium azide mutagenesis: Preferential generation of AT → GC transitions in the barley Ant18 gene. Proc. Natl. Acad. Sci. USA, 90, 8043-8047.
37. Osier, T.L. and Lindroth, L.R. (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J. Chem. Ecol. 27, 1289-1313.
38. Porter, L.J., Hrstich, L.N. and Chan, B.G. (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry, 25, 223-230.
39. Richard, S., Lapointe, G., Rutledge, R.G. and Seguin, A. (2000) Induction of chalcone synthase expression in white spruce by wounding and jasmonate. Plant Cell Physiol. 41, 982-987.
40. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
41. Saslowsky, D. and Winkel-Shirley, B. (2001) Localization of flavonoid enzymes in Arabidopsis roots. Plant J. 27, 37-48.
42. Schultz, J.C. and Baldwin, I.T. (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science, 217, 149-151.
43. Shirley, B.W., Kubasek, W.L., Storz, G., Bruggemann, E., Koornneef, M., Ausubel, F.M. and Goodman, H.M. (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J. 8, 659-671.
44. Stafford, H.A. and Lester, H.H. (1982) Enzymic and non-enzymic reduction of (+)-dihydroquercitin to its 3,4-diol. Plant Physiol. 70, 695-698.
45. Subramaniam, R., Reinold, S., Molitor, E.K. and Douglas, C.J. (1993) Structure, inheritance, and expression of hybrid poplar (Populus trichocarpa x Populus deltoides) phenylalanine ammonia-lyase genes. Plant Physiol. 102, 73-83.
46. Swain, T. (1979) Tannins and lignins. In Herbivores: Their Interaction with Secondary Plant Metabolites (Rosenthal, G.A. and Janzen, D.H., eds). San Díego: Academic Press, pp. 657-682.
47. Tamari, G., Borochov, A., Atzorn, R. and Weiss, D. (1995) Methyl jasmonate induces pigmentation and flavonoid gene expression in petunia corollas: A possible role in wound response. Physiol. Plant. 94, 45-50.
48. Walling, L.L. (2000) The myriad plant responses to herbivores. J. Plant Growth Regul. 19, 195-216.
49. Weiler, E.W. (1997) Octadecanoid mediated signal transduction in higher plants. Naturwissenschaften, 84, 340-349.