Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen

Plant Physiology

Volumn 130, Issue 2, 2002, Pages 796-807

  Kao, Yu Ying ^a   Harding, Scott A ^a   Tsai, Chung Jui ^a  

^a MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CATALYSIS; CLONING; COENZYMES; DNA; GENES; LIGNIN; METABOLISM;

LIGNIFICATION;

PLANTS (BOTANY);

EMBRYOPHYTA; EUKARYOTA; POPULUS; POPULUS TREMULOIDES;

EID: 0036800967     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.006262     Document Type: Article

References (52)

1. Allina SM, Aviva P-H, Theilmann DA, Ellis BE, Douglas CJ (1998) 4-Coumarate:coenzyme A ligase in hybrid poplar. Plant Physiol 116: 743-754
2. Allwood EG, Davies DR, Gerrish C, Ellis BE, Bolwell GP (1999) Phosphorylation of phenylalanine ammonia-lyase: evidence for a novel protein kinase and identification of the phosphorylated residue. FEBS Lett 457: 47-52
3. Appert C, Logemann E, Hahlbrock K, Schmid J, Amrhein N (1994) Structural and catalytic properties of the four phenylalanine ammonia-lyase isoenzymes from parsley (Petroselinum crispum Nym.). Eur J Biochem 225: 491-499
4. Bolwell GP (1992) A role for phosphorylation in the down-regulation of phenylalanine ammonia-lyase in suspension-cultured cells of French bean. Phytochemistry 31: 4081-4086
5. Bolwell GP, Cramer CL, Lamb CJ, Schuch W, Dixon RA (1986) L- Phenylalanine ammonia-lyase from Phaseolus vulgaris: modulation of the levels of active enzyme by trans-cinnamic acid. Planta 169: 97-107
6. Bugos RC, Chiang VL, Campbell WH (1991) cDNA cloning, sequence analysis and seasonal expression of lignin-bispecific caffeic acid/5-hydroxyferulic acid O-methyltransferase of aspen. Plant Mol Biol 17: 1203-1215
7. Bugos RC, Chiang VL, Zhang XH, Campbell ER, Podila GK, Campbell WH (1995) RNA isolation from plant tissues recalcitrant to extraction in guanidine. BioTechniques 19: 734-737
8. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11: 113-116
9. Coquoz J-L, Buchala A, Metraux J-P (1998) The biosynthesis of salicylic acid in potato plants. Plant Physiol 117: 1095-1101
10. Cramer CL, Edwards K, Dron M, Liang X, Dildine SL, Bolwell GP, Dixon RA, Lamb CJ, Schuch W (1989) Phenylalanine ammonia-lyase gene organization and structure. Plant Mol Biol 12: 367-383
11. Davis JM, Egelkrout EE, Coleman GD, Chen THH, Haissig BE, Riemenschneider DE, Gordon MP (1993) A family of wound-induced genes in Populus shares common features with genes encoding vegetative storage proteins. Plant Mol Biol 23: 135-143
12. Davis JM, Gordon MP, Smit BA (1991) Assimilate movement dictates remote sites of wound-induced gene expression in poplar leaves. Proc Natl Acad Sci USA 88: 2393-2396
13. Ehness R, Ecker M, Godt DE, Roitsch T (1997) Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9: 1825-1841
14. Feucht W, Treutter D (1990) Flavan-3-ols in trichomes, pistils and phelloderm of some tree species. Ann Bot 65: 225-230
15. Gardner RO (1975) Vanillin-hydrochloric acid as a histochemical test for tannin. Stain Technol 50: 315-317
16. Ge L, Chiang VL (1996) A full length cDNA encoding trans-cinnamate 4-hydroxylase from developing xylem of Populus tremuloides (accession no. U47293) (PGR96-075). Plant Physiol 112: 861
17. Gray-Mitsumune M, Molitor EK, Cukovic D, Carslon JE, Douglas CJ (1999) Developmentally regulated patterns of expression directed by poplar PAL promoters in transgenic tobacco and poplar. Plant Mol Biol 39: 657-669
18. Hahlbrock K, Grisebach H (1979) Enzymic controls in the biosynthesis of lignin and flavonoids. Ann Rev Plant Physiol 30: 105-130
19. Harding SA, Leshkevich J, Chiang VL, Tsai C-J (2002) Differential substrate inhibition couples kinetically distinct 4-coumarate:CoA ligases with spatially distinct metabolic roles in quaking aspen. Plant Physiol 128: 428-438
20. Higuchi T (1997) Biochemistry and Molecular Biology of Wood. Springer-Verlag, New York, pp 93-99
21. Howles PA, Sewalt VJH, Paiva NL, Elkind Y, Pate NJ, Lamb CJ, Dixon RA (1996) Overexpression of L-phenylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol 112: 1617-1624
22. Hu W-J, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, Tsai C-J, Chiang VL (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat Biotechnol 17: 808-812
23. Hu W-J, Kawaoka A, Tsai C-J, Lung J, Osakabe K, Ebinuma H, Chiang VL (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
24. Jones HD (1984) Phenylalanine ammonia-lyase: regulation of its induction, and its role in plant development. Phytochemistry 23: 1349-1359
25. 2 and nutrient status changes affect phytomass and the production of plant defensive secondary chemicals in Salix myrsinifolia (Salisb.) Oecologia 95: 495-498
26. 14C-labeled photosynthate to allelochemicals and primary metabolites in source and sink leaves of aspen: evidence for secondary metabolite turnover. Oecologia 119: 408-418
27. Knogge W, Weissenbock G (1986) Tissue-distribution of secondary phenolic biosynthesis in developing primary leaves of Avena sativa L. Planta 167: 196-205
28. Kumar A, Ellis BE (2001) The phenylalanine ammonia-lyase gene family in raspberry. Structure, expression, and evolution. Plant Physiol 127: 230-239
29. Lee D, Douglas CJ (1996) Two divergent members of a tobacco 4-coumarate: coenzyme A ligase (4CL) gene family. cDNA structure, gene inheritance and expression, and properties of recombinant proteins. Plant Physiol 112: 193-205
30. Li L, Popko JL, Umezawa T, Chiang VL (2000) 5-Hydroxy-coniferyl aldehyde modulates enzymatic methylation for syringyl monolignol formation: a new view of monolignol biosynthesis in angiosperms. J Biol Chem 275: 6537-6545
31. Liang X, Dron M, Cramer CL, Dixon RA, Lamb CJ (1989) Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J Biol Chem 264: 14486-14492
32. Lindroth RL, Hwang S-Y (1996) Diversity, redundancy, and multiplicity in chemical defense systems of aspen. In JT Romeo, JA Saunders, P. Barbosa, eds, Phytochemical Diversity and Redundancy in Ecological Interactions. Plenum Press, New York, pp 25-51
33. Lindroth RL, Kinney YY, Platz CL (1993) Responses of deciduous trees to elevated atmospheric CO2: productivity, phytochemistry and insect performance. Ecology 74: 763-777
34. Logemann E, Parniske M, Hahlbrock K (1995) Modes of expression and common structural features of the complete phenylalanine ammonia-lyase gene family in parsley. Proc Natl Acad Sci USA 92: 5905-5909
35. Lois R, Dietrich A, Hahlbrock K, Schultz W (1989) A phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J 8: 1641-1648
36. Nagai N, Kitauchi F, Okamoto K, Kanda T, Shimosaka M, Okazaki M (1994) A transient increase of phenylalanine ammonia-lyase transcript in kinetin-treated tobacco cells. Biosci Biotechnol Biochem 58: 558-559.
37. O'Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59: 366-373
38. Osakabe Y, Nanto K, Kitamura H, Kawai S, Kondo Y, Fujii T, Takabe K, Katayama Y, Morohoshi N (1996) Immunocytochemical localization of phenylalanine ammonia-lyase in tissues of Populus kitakamiensis. Planta 200: 13-19
39. Osakabe Y, Ohtsubo Y, Kawai S, Katayama Y, Morohoshi N (1995a) Structure and tissue-specific expression of genes for phenylalanine ammonia-lyase from a hybrid aspen, Populus kitakamiensis. Plant Sci 105: 217-226
40. Osakabe Y, Osakabe K, Kawai S, Katayama Y, Morohoshi N (1995b) Characterization of the structure and determination of mRNA levels of phenylalanine ammonia-lyase gene family from Populus kitakamiensis. Plant Mol Biol 28: 1133-1141
41. Parsons TJ, Bradshaw HD Jr, Gordon MP (1989) Systemic accumulation of specific mRNAs in response to wounding in poplar trees. Proc Natl Acad Sci USA 86: 7895-7899
42. Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25: 223-230
43. Rasmussen S, Dixon RA (1999) Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Cell 11: 1537-1551
44. Reeve RM (1951) Histological tests for polyphenols in plant tissues. Stain Technol 26: 91-96
45. Ribnicky DM, Shulaev V, Raskin I (1998) Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiol 118: 565-572
46. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, Ed 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
47. Sarma AD, Sreelakshimi Y, Sharma R (1998) Differential expression and properties of phenylalanine ammonia-lyase isoforms in tomato leaves. Phytochemistry 49: 2233-2243
48. Shufflebottom D, Edwards K, Schuch W, Bevan M (1993) Transcription of two members of a gene family encoding phenylalanine ammonia-lyase leads to remarkably different cell specificities and induction patterns. Plant J 3: 835-845
49. Subramaniam R, Reinold S, Molitor EK, Douglas CJ (1993) Structure, inheritance, and expression of hybrid poplar (Populus trichocarpa x Populus deltoides) phenylalanine ammonia-lyase genes. Plant Physiol 102: 71-83
50. Tsai C-J, Podila GK, Chiang VL (1994) Agrobacterium-mediated transformation of quaking aspen (Populus tremuloides) and regeneration of transgenic plants. Plant Cell Rep 14: 94-97
51. Tsai C-J, Popko JL, Mielke MR, Hu W-J, Podila GK, Chiang VL (1998) Suppression of O-methyltransferase gene by homologous sense transgene in quaking aspen causes red-brown wood phenotypes. Plant Physiol 117: 101-112
52. Yalpani N, Leon J, Lawton MA, Raskin I (1993) Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol 103: 315-321