Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems

Plant Cell

Volumn 23, Issue 3, 2011, Pages 1124-1137

  Berthet, Serge ^a   Demont Caulet, Nathalie ^a   Pollet, Brigitte ^a   Bidzinski, Przemyslaw ^a,c   Cézard, Laurent ^a   le Bris, Phillipe ^a   Herve, Jonathan ^a   Blondet, Eddy ^b   Balzergue, Sandrine ^b   Lapierre, Catherine ^a   Jouanin, Lise ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^c MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79955623368     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.082792     Document Type: Article

References (57)

1. Abdulrazzak, N., et al. (2006). A coumaroyl-ester-3-hydroxylase insertion mutant reveals the existence of nonredundant meta-hydroxyla-tion pathways and essential roles for phenolic precursors in cell expansion and plant growth. Plant Physiol. 140: 30-48.
2. Adler, E. (1977). Lignin chemistry. Past, present and future. Wood Sci. Technol. 11: 169-218.
3. Bao, W., O'malley, D.M., Whetten, R., and Sederoff, R.R. (1993). A laccase associated with lignification in loblolly pine xylem. Science 260: 672-674.
4. Baudry, A., Caboche, M., and Lepiniec, L. (2006). TT8 controls its own expression in a feedback regulation involving TTG1 and homologous MYB and bHLH factors, allowing a strong and cell-specific accumulation of flavonoids in Arabidopsis thaliana. Plant J. 46: 768-779.
5. Besseau, S., Hoffmann, L., Geoffroy, P., Lapierre, C., Pollet, B., and Legrand, M. (2007). Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19: 148-162.
6. Betz, G.A., Knappe, C., Lapierre, C., Olbrich, M., Welzl, G., Langebartels, C., Heller, W., Sandermann, H., and Ernst, D. (2009). Ozone affects shikimate pathway transcripts and monomeric lignin composition in European beech (Fagus sylvatica L.). Eur. J. For. Res. 128: 109-116.
7. Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R., and Gö rlach, J. (2001). Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510.
8. Brown, D.M., Zeef, L.A.H., Ellis, J., Goodacre, R., and Turner, S.R. (2005). Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17: 2281-2295.
9. Cabané, M., Pireaux, J.-C., Léger, E., Weber, E., Dizengremel, P., Pollet, B., and Lapierre, C. (2004). Condensed lignins are synthesized in poplar leaves exposed to ozone. Plant Physiol. 134: 586-594.
10. Cai, X.N., Davis, E.J., Ballif, J., Liang, M.X., Bushman, E., Haroldsen, V., Torabinejad, J., and Wu, Y.J. (2006). Mutant identification and characterization of the laccase gene family in Arabidopsis. J. Exp. Bot. 57: 2563-2569.
11. Caparros-Ruiz, D., Fornale, S., Civardi, L., Puigdomenech, P., and Rigau, J. (2006). Isolation and characterisation of a family of laccases in maize. Plant Sci. 171: 217-225.
12. Chapple, C.C., Vogt, T., Ellis, B.E., and Somerville, C.R. (1992). An Arabidopsis mutant defective in the general phenylpropanoid pathway. Plant Cell 4: 1413-1424.
13. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
14. Crowe, M.L., et al. (2003). CATMA: A complete Arabidopsis GST database. Nucleic Acids Res. 31: 156-158.
15. Dauwe, R., et al. (2007). Molecular phenotyping of lignin-modified tobacco reveals associated changes in cell-wall metabolism, primary metabolism, stress metabolism and photorespiration. Plant J. 52: 263-285.
16. Dean, J.F., LaFayette, P.R., Rugh, C., Tristram, A.H., Hoopes, J.T., Eriksson, K.E., and Merckle, S.A. (1998). Laccases associated with lignifying vascular tissue. In Lignin and Lignan Biosynthesis, N.G. Lewis and S. Sarkanen, eds (Washington, DC: American Chemical Society), pp. 96-108.
17. Dean, J.F.D., and Eriksson, K.E.L. (1994). Laccase and the deposition of lignin in vascular plants. Holzforschung 48: 21-33.
18. Debeaujon, I., Nesi, N., Perez, P., Devic, M., Grandjean, O., Caboche, M., and Lepiniec, L. (2003). Proanthocyanidin-accumulating cells in Arabidopsis testa: Regulation of differentiation and role in seed development. Plant Cell 15: 2514-2531.
19. Dence, C. (1992). Lignin determination. In Methods in Lignin Chemistry, S.Y. Lin and C.W. Dence, eds (Berlin: Springer-Verlag), pp. 33-61.
20. Do, C.T., Pollet, B., Thévenin, J., Sibout, R., Denoue, D., Barriére, Y., Lapierre, C., and Jouanin, L. (2007). Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis. Planta 226: 1117-1129.
21. Donaldson, L.A. (2001). Lignification and lignin topochemistry - An ultrastructural view. Phytochemistry 57: 859-873.
22. Dubos, C., Le Gourrierec, J., Baudry, A., Huep, G., Lanet, E., Debeaujon, I., Routaboul, J.M., Alboresi, A., Weisshaar, B., and Lepiniec, L. (2008). MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J. 55: 940-953.
23. Ehlting, J., et al. (2005). Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. Plant J. 42: 618-640.
24. Fagerstedt, K., Kukkola, E., Koistinen, V.V.T., Takahashi, J., and Marjamaa, K. (2010). Cell wall lignin is polymerized by class II secretable plant peroxidase in Norway spruce. J. Integr. Plant Biol. 52: 186-194.
25. Gagnot, S., Tamby, J.P., Martin-Magniette, M.L., Bitton, F., Taconnat, L., Balzergue, S., Aubourg, S., Renou, J.P., Lecharny, A., and Brunaud, V. (2008). CATdb: A public access to Arabidopsis tran-scriptome data from the URGV-CATMA platform. Nucleic Acids Res. 36 (Database issue): D986-D990.
26. Ge, Y.C., Dudoit, S., and Speed, T.P. (2003). Resampling-based multiple testing for microarray data analysis. Test 12: 1-77.
27. Goujon, T., Sibout, R., Pollet, B., Maba, B., Nussaume, L., Bechtold, N., Lu, F., Ralph, J., Mila, I., Barrié re, Y., Lapierre, C., and Jouanin, L. (2003). A new Arabidopsis thaliana mutant deficient in the expression of O-methyltransferase impacts lignins and sinapoyl esters. Plant Mol. Biol. 51: 973-989.
28. Gutiérrez, R.A., MacIntosh, G.C., and Green, P.J. (1999). Current perspectives on mRNA stability in plants: Multiple levels and mechanisms of control. Trends Plant Sci. 4: 429-438.
29. Hilson, P., et al. (2004). Versatile gene-specific sequence tags for Arabidopsis functional genomics: Transcript profiling and reverse genetics applications. Genome Res. 14: 2176-2189.
30. Hoegger, P.J., Kilaru, S., James, T.Y., Thacker, J.R., and Kües, U. (2006). Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J. 273: 2308-2326.
31. Higuchi, T., and Ito, Y. (1958). Dehydrogenation products of coniferyl alcohol formed by the action of mushroom phenol oxidase, rhus laccase and radish peroxidase. J. Biochem. 45: 575-579.
32. Karkonen, A., Koutaniemi, S., Mustonen, M., Syrjanen, K., Brunow, G., Kilpelainen, I., Teeri, T.H., and Simola, L.K. (2002). Lignification related enzymes in Picea abies suspension cultures. Physiol. Plant. 114: 343-353.
33. Kim, H., Ralph, J., Lu, F., Pilate, G., Leple ́, J.-C., Pollet, B., and Lapierre, C. (2002). Identification of the structure and origin of thioacidolysis marker compounds for cinnamyl alcohol dehydrogen-ase deficiency in angiosperms. J. Biol. Chem. 277: 47412-47419.
34. Koizumi, K., Yokoyama, R., and Nishitani, K. (2009). Mechanical load induces upregulation of transcripts for a set of genes implicated in secondary wall formation in the supporting tissue of Arabidopsis thaliana. J. Plant Res. 122: 651-659.
35. Lapierre, C. (2010). Determining lignin structure by chemical degradations. In Lignin and Lignans: Advances in Chemistry, C. Heitner, D. Dimmel, and J.A. Schmidt, eds (Boca Raton, FL: CRC Press, Taylor & Francis Group), pp. 11-48.
36. Lapierre, C., Pollet, B., and Rolando, C. (1995). New insights into the molecular architecture of hardwood lignins by chemical degradative methods. Res. Chem. Intermediat. 21: 397-412.
37. Leple ́, J.C., et al. (2007). Downregulation of cinnamoyl-coenzyme A reductase in poplar: Multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell 19: 3669-3691.
38. Li, X., Bonawitz, N.D., Weng, J.-K., and Chapple, C. (2010). The growth reduction associated with repressed lignin biosynthesis in Arabidopsis thaliana is independent of flavonoids. Plant Cell 22: 1620-1632.
39. Liang, M.X., Davis, E., Gardner, D., Cai, X.N., and Wu, Y.J. (2006). Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta 224: 1185-1196.
40. Lurin, C., et al. (2004). Genome-wide analysis of Arabidopsis penta- tricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103.
41. Masclaux-Daubresse, C., Reisdorf-Cren, M., Pageau, K., Lelandais, M., Grandjean, O., Kronenberger, J., Valadier, M.H., Feraud, M., Jouglet, T., and Suzuki, A. (2006). Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant Physiol. 140: 444-456.
42. McCaig, B.C., Meagher, R.B., and Dean, J.F.D. (2005). Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana. Planta 221: 619-636.
43. Mir Derikvand, M., Sierra, J.B., Ruel, K., Pollet, B., Do, C.-T., Thévenin, J., Buffard, D., Jouanin, L., and Lapierre, C. (2008). Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1. Planta 227: 943-956.
44. Nakano, J., and Meshitsuka, G. (1992). The detection of lignin. In Methods in Lignin Chemistry, S.Y. Lin and C.W. Dence, eds (Berlin: Springer-Verlag), pp 23-32.
45. Pourcel, L., Routaboul, J.M., Kerhoas, L., Caboche, M., Lepiniec, L., and Debeaujon, I. (2005). TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17: 2966-2980.
46. Ranocha, P., Chabannes, M., Chamayou, S., Danoun, S., Jauneau, A., Boudet, A.-M., and Goffner, D. (2002). Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiol. 129: 145-155.
47. Richardson, A., and McDougall, G.J. (1997). A laccase-type polyphe-nol oxidase from lignifying xylem of tobacco. Phytochemistry 44: 229-235.
48. Rohde, A., 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.
49. Ruel, K., Berrio-Sierra, J., Derikvand, M.M., Pollet, B., Thévenin, J., Lapierre, C., Jouanin, L., and Joseleau, J.P. (2009). Impact of CCR1 silencing on the assembly of lignified secondary walls in Arabidopsis thaliana. New Phytol. 184: 99-113.
50. Sibout, R., Eudes, A., Mouille, G., Pollet, B., Lapierre, C., Jouanin, L., and Séguin, A. (2005). CINNAMYL ALCOHOL DEHYDROGENASE-C and -D are the primary genes involved in lignin biosynthesis in the floral stem of Arabidopsis. Plant Cell 17: 2059-2076.
51. Sterjiades, R., Dean, J.F.D., and Eriksson, K.E.L. (1992). Laccase from sycamore maple (Acer pseudoplatanus) polymerizes mono-lignols. Plant Physiol. 99: 1162-1168.
52. Terashima, N., and Fukushima, K. (1993). Comprehensive model of the lignified plant cell wall. In Forage Cell Wall Structure and Digestibility, H.G. Jung, D.R. Buxton, R.D. Hatfield, and R. Ralph, eds (Madison, WI: American Society of Agronomy), pp. 247-270.
53. Tognolli, M., Penel, C., Greppin, H., and Simon, P. (2002). Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288: 129-138.
54. Vanholme, R., Morreel, K., Ralph, J., and Boerjan, W. (2008). Lignin engineering. Curr. Opin. Plant Biol. 11: 278-285.
55. Wang, G.D., Li, Q.J., Luo, B., and Chen, X.Y. (2004). Ex planta phytoremediation of trichlorophenol and phenolic allelochemicals via an engineered secretory laccase. Nat. Biotechnol. 22: 893-897.
56. Wang, J., Wang, C.L., Zhu, M.L., Yu, Y., Zhang, Y.B., and Wei, Z.M. (2008). Generation and characterization of transgenic poplar plants overexpressing a cotton laccase gene. Plant Cell Tissue Organ Cult. 93: 303-310.
57. Yoshida, H. (1883). Chemistry of lacquer (urushi). J. Chem. Soc. 43: 472-486.