A coumaroyl-ester-3-hydroxylase insertion mutant reveals the existence of nonredundant meta-hydroxylation pathways and essential roles for phenolic precursors in cell expansion and plant growth

Plant Physiology

Volumn 140, Issue 1, 2006, Pages 30-48

  Abdulrazzak, Nawroz ^a   Pollet, Brigitte ^b   Ehlting, Jürgen ^a   Larsen, Kim ^c   Asnaghi, Carole ^a   Ronseau, Sebastien ^a   Proux, Caroline ^d   Erhardt, Mathieu ^a   Seltzer, Virginie ^a   Renou, Jean Pierre ^d   Ullmann, Pascaline ^a   Pauly, Markus ^c   Lapierre, Catherine ^b   Werck Reichhart, Danièle ^a  

^a CNRS   (France)

^b AGROPARISTECH   (France)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^d INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; GROWTH KINETICS; HYDROXYLATION; LIGNIN; PLANTS (BOTANY); POLYSACCHARIDES;

CELL EXPANSION; CRYSTALLINE CELLULOSE; FLAVONOL GLYCOSIDES; GENE EXPRESSION; HOMEOSTASIS; PHENYLPROPANOID;

ENZYMES;

CELLS; ENZYMES; GROWTH; HYDROXYLATION; LIGNINS; PLANTS; POLYSACCHARIDES;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; BACTERIAL DNA; COUMARIC ACID; CYP98A3 PROTEIN, ARABIDOPSIS; CYTOCHROME P450; LIGNIN; MIXED FUNCTION OXIDASE; PHENYLPROPIONIC ACID DERIVATIVE; PLANT RNA; POLYSACCHARIDE; T DNA; T-DNA;

ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; CELL ENLARGEMENT; CELL WALL; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; HYDROXYLATION; METABOLISM; MOLECULAR GENETICS; MUTATION; PLANT ROOT; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL ENLARGEMENT; CELL WALL; COUMARIC ACIDS; CYTOCHROME P-450 ENZYME SYSTEM; DNA, BACTERIAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; HYDROXYLATION; LIGNIN; MIXED FUNCTION OXYGENASES; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; PHENYLPROPIONATES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; POLYSACCHARIDES; RNA, PLANT;

EID: 33645809365     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.069690     Document Type: Article

References (77)

1. Adler E, Bjorkquist KJ, Haggroth S (1948) Ûber die Ursache der Farbreaktionen des Holzes. Acta Chem Scand 2: 93-94
2. Albersheim P, Nevins DJ, English PD, Karr A (1967) A method for the analysis of sugars in plant cell-wall polysaccharides by gas-liquid chromatography. Carbohydr Res 5: 340-345
3. Baskin TI (2001) On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215: 150-171
4. Binns AN, Chen RH, Wood HN, Lynn DG (1987) Cell division promoting activity of naturally occurring dehydrodiconiferyl glucosides: Do cell wall components control cell division? Proc Natl Acad Sci USA 84: 980-984
5. Bloor SJ, Abrahams S (2002) The structure of the major anthocyanin in Arabidopsis thaliana. Phytochemistry 59: 343-346
6. Blumenkrantz N, Asboe-Hansen G (1973) New methods for quantitative determination or uronic acids. Anal Biochem 54: 484-489
7. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54: 519-546
8. Booij-James IS, Dube SK, Jansen MAK, Edelman M, Mattoo AK (2000) Ultraviolet-B radiation impact tight-mediated turnover of the photosystem II reaction center heterodimer in Arabidopsis mutants altered in phenolic metabolism. Plant Physiol 124: 1275-1283
9. Cano-Delgado A, Penfield S, Smith C, Catley M, Bevan M (2003) Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J 34: 351-362
10. Caño-Delgado AI, Metzlaff K, Bevan MW (2000) The eli1 mutation reveals a link between cell expansion and secondary cell wall formation in Arabidopsis thaliana. Development 127: 3395-3405
11. Chomczynski P, Sacchi N (1987) Single step method of RNA isolation by guanidinum thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159
12. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J16: 735-743
13. Crowe ML, Serizet C, Thareau V, Aubourg S, Rouze P, Hilson P, Beynon J, Weisbeek P, van Hummelen P, Reymond P, et al (2003) CATMA: a complete Arabidopsis GST database. Nucleic Acids Res 31: 156-158
14. Debeaujon I, Leon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122: 403-413
15. Dence CW (1992) The determination of lignin. In SY Lin, CW Dence, eds, Methods in Lignin Chemistry. Springer-Verlag, New York, pp 33-61
16. Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135: 1893-1902
17. Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cevl links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14: 1557-1566
18. Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM, Chapple C (2002a) Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis. Plant J 30: 47-59
19. Franke R, Humphreys JM, Hemm MR, Denault JW, Ruegger MO, Cusumano JC, Chapple C (2002b) The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J 30: 33-45
20. Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol 13: 207-209
21. Gang DR, Beuerle T, Ullmann P, Werck-Reichhart D, Pichersky E (2002) Differential production of meta-hydroxylated phenylpropanoids in sweet basil peltate glandular trichomes and leaves is controlled by the activities of specific acyltransferases and hydroxylases. Plant Physiol 130: 1536-1544
22. Garcia-Hernandez M, Berardini TZ, Chen G, Crist D, Doyle A, Huala E, Knee E, Lambrecht M, Miller N, Mueller LA, et al (2002) TAIR: a resource for integrated Arabidopsis data. Funct Integr Genomics 2: 239-253
23. Goujon T, Minic Z, Amrani AE, Lerouxel O, Aletti E, Lapierre C, Joseleau JP, Jouanin L (2003) AtBXL1, a novel higher plant (Arabidopsis thaliana) putative beta-xylosidase gene, is involved in secondary cell wall metabolism and plant development. Plant J 33: 677-690
24. Grace SC, Logan BA (2000) Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Philos Trans R Soc Lond B Biol Sci 355: 1499-1510
25. Graham TL (1988) Flavonoids and flavonol glycoside metabolism in Arabidopsis. Plant Physiol Biochem 36: 135-144
26. Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50: 473-503
27. Hilson P, Allemeersch J, Altmann T, Aubourg S, Avon A, Beynon J, Bhalerao RP, Bitton F, Caboche M, Cannoot B, et al (2004) Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res 14: 2176-2189
28. Hoffmann L, Besseau S, Geoffroy P, Ritzenthaler C, Meyer D, Lapierre C, Pollet B, Legrand M (2004) Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16: 1446-1465
29. Hoffmann L, Maury S, Martz F, Geoffroy P, Legrand M (2003) Purification, cloning and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J Biol Chem 278: 95-103
30. Humphreys JM, Chapple C (2002) Rewriting the lignin roadmap. Curr Opin Plant Biol 5: 224-229
31. Johannesson H, Wang Y, Hanson J, Engström P (2003) The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Mol Biol 51: 719-729
32. Karimi M, Inze D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Plant Sci 7: 193-195
33. Kitamura S, Shikazono N, Tanaka A (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J 37: 104-114
34. Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5: 33-36
35. Krysan PJ, Young JC, Sussman MR (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11: 2283-2290
36. Landry LG, Chapple CCS, Last R (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol 109: 1159-1166
37. Lapierre C, Pollet B, Rolando C (1995) New insight into the molecular architecture of hardwood lignins chemical degradative methods. Res Chem Intermediates 21: 397-412
38. Lauvergeat V, Lacomme C, Lacombe E, Lasserre E, Roby D, Grima-Pettenati J (2001) Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria. Phytochemistry 57: 1187-1195
39. Lee Y, Choi D, Kende H (2001) Expansins: ever-expanding numbers and functions. Curr Opin Plant Biol 4: 527-532
40. 2+/calmodulin in Arabidopsis thaliana. Mol Gen Genet 258: 412-419
41. Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41: 455-496
42. Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C, Caboche M, Debast C, Gualberto J, Hoffmann B, et al (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103
43. Lynn DG, Chen RH, Manning KS, Wood HN (1987) The structural characterization of endogenous factors from Vinca rosea crown gall tumors that promote cell division of tobacco cells. Proc Natl Acad Sci USA 84: 615-619
44. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419: 399-403
45. Mathew S, Abraham TE (2004) Ferulic acid: an antioxidant found naturally in plant cell walls and feruloyl esterases involved in its release and their applications. Crit Rev Biotechnol 24: 59-83
46. Matsuno M, Nagatsu A, Ogihara Y, Ellis BE, Mizukami H (2002) CYP98A6 from Lithospermum erythrorhizon encodes 4-coumaroyl-4′-hydroxyphenyllactic acid 3-hydroxylase involved in rosmarinic acid biosynthesis. FEBS Lett 514: 219-224
47. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361-371
48. Nair RB, Xia Q, Kartha CJ, Kurylo E, Hirji RN, Datla R, Selvaraj G (2002) Arabidopsis CYP98A3 mediating aromatic 3-hydroxylation: developmental regulation of the gene, and expression in yeast. Plant Physiol 130: 210-220
49. Nicholson RL, Hammerschmidt R (1992) Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol 30: 369-389
50. Niggeweg R, Michael AJ, Martin C (2004) Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat Biotechnol 22: 746-754
51. Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress: the central role of "redox" and abscisic acid-mediated controls. Plant Physiol 129: 460-468
52. Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16: 1898-1911
53. Pelletier MK, Burbulis IA, Winkel-Shirley B (1999) Disruption of specific flavonoid genes enhances the accumulation of flavonoid enzymes and end-products in Arabidopsis seedlings. Plant Mol Biol 40: 45-54
54. Perez-Amador MA, Leon J, Green PJ, Carbonell J (2002) Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiol 130: 1454-1463
55. Petersen M, Strack D, Matern U (1999) Biosynthesis of phenylpropanoïds and related compounds. In M Wink, ed, Biochemistry of Plant Secondary Metabolism, Annual Plant Reviews. CRC Press, Boca Raton, FL, pp 151-221
56. Puskas LG, Zvara A, Hackler L Jr, Van Hummelen P (2002) RNA amplification results in reproducible microarray data with slight ratio bias. Biotechniques 32: 1330-1334
57. Rogers LA, Dubos C, Cullis IF, Surman C, Poole M, Willment J, Mansfield SD, Campbell MM (2005) Light, the circadian clock, and sugar perception in the control of lignin biosynthesis. J Exp Bot 56: 1651-1663
58. Rohde A, Morreel K, Ralph J, Goeminne G, Hostyn V, De Rycke R, Kushnir S, Van Doorsselaere J, Joseleau JP, Vuylsteke M, et al (2004) Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell 16: 2749-2771
59. Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 276: 36566-36574
60. Schoof H, Zaccaria P, Gundlach H, Lemcke K, Rudd S, Kolesov G, Arnold R, Mewes HW, Mayer KF (2002) MIPS Arabidopsis thaliana database (MAtDB): an integrated biological knowledge resource based on the first complete plant genome. Nucleic Acids Res 30: 91-93
61. Schumacher K, Vafeados D, McCarthy M, Sze H, Wilkins T, Chory J (1999) The Arabidopsis det3 mutant reveals a central role for the vacuolar H(+)-ATPase in plant growth and development. Genes Dev 13: 3259-3270
62. Selvendran RR, March JF, Ring SG (1979) Determination of aldoses and uronic acid content of vegetable fiber. Anal Biochem 96: 282-292
63. Sibout R, Eudes A, Pollet B, Goujon T, Mila I, Granier F, Seguin A, Lapierre C, Jouanin L (2003) Expression pattern of two paralogs encoding cinnamyl alcohol dehydrogenases in Arabidopsis: isolation and characterization of the corresponding mutants. Plant Physiol 132: 848-860
64. Söderman E, Mattsson J, Engstiöm P (1996) The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J 10: 375-381
65. Stafford H (1990) Flavonoid Metabolism. CRC Press, Boca Raton, FL
66. Stotz HU, Pittendrigh BR, Kroymann J, Weniger K, Fritsche J, Bauke A, Mitchell-Olds T (2000) Induced plant defense responses against chewing insects: Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol 124: 1007-1018
67. Tamagnone L, Merida A, Stacey N, Plaskitt K, Parr A, Chang CF, Lynn D, Dow JM, Roberts K, Martin C (1998) Inhibition of phenolic acid metabolism results in precocious cell death and altered cell morphology in leaves of transgenic tobacco plants. Plant Cell 10: 1801-1816
68. Tohge T, Nishiyama Y, Hirai MY, Yano M, Nakajima J, Awazuhara M, Inoue E, Takahashi H, Goodenowe DB, Kitayama M, et al (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 42: 218-235
69. Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32: 420-424
70. Vandepoele K, Raes J, de Veylder L, Rouzé P, Rombauts S, Inzé D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14: 903-916
71. Veit M, Pauli GF (1999) Major flavonoids from Arabidopsis thaliana leaves. J Nat Prod 62: 1301-1303
72. Wasteneys GO (2004) Progress in understanding the role of microtubules in plant cells. Curr Opin Plant Biol 7: 651-660
73. Weisshaar B, Jenkins GI (1998) Phenylpropanoid biosynthesis and its regulation. Curr Opin Plant Biol 1: 251-257
74. Xiong L, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133: 29-36
75. Yamaguchi-Shinozaki K, Shinozaki K (1993) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 238: 17-25
76. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15
77. Zhong R, Kays SJ, Schroeder BP, Ye ZH (2002) Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14: 165-179