Abstract
While laccases, multi-copper glycoprotein oxidases, are often able to catalyze oxidation of a broad range of substrates, such as phenols and amines in vitro, their precise physiological/biochemical roles in higher plants remain largely unclear, e.g., Arabidopsis thaliana contains 17 laccases with only 1 having a known physiological function. To begin to explore their roles in planta, spatial and temporal expression patterns of Arabidopsis laccases were compared and contrasted in different tissues at various development stages using RT-PCR and promoter-GUS fusions. Various cell-specific expressions were noted where specific laccases were uniquely expressed, such as LAC4 in interfascicular fibers and seed coat columella, LAC7 in hydathodes and root hairs, LAC8 in pollen grains and phloem, and LAC15 in seed coat cell walls. Such specific cell-type expression patterns provide new leads and/or strategies into determining their precise physiological/biochemical roles. In addition, there was an apparent redundancy of gene expression patterns for several laccases across a wide variety of tissues, lignified and non-lignified, perhaps indicative of overlapping function(s). Preliminary evidence, based on bioinformatics analyses, suggests that most laccases may also be tightly regulated at both transcriptional (antisense transcripts, histone and DNA methylation) and posttranscriptional (microRNAs) levels of gene expression.
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Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78
Altamura MM, Possenti M, Matteucci A, Baima S, Ruberti I, Morelli G (2001) Development of the vascular system in the inflorescence stem of Arabidopsis. New Phytol 151:381–389
Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbiol Rev 30:215–242
Bao W, O’Malley DM, Whetten R, Sederoff RR (1993) A laccase associated with lignification in loblolly pine xylem. Science 260:672–674
Becnel J, Natarajan M, Kipp A, Braam J (2006) Developmental expression patterns of Arabidopsis XTH genes reported by transgenes and Genevestigator. Plant Mol Biol 61:451–467
Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN (2003) A gene expression map of the Arabidopsis root. Science 302:1956–1960
Brady SM, Orlando DA, Lee J-Y, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–806
Brown DM, Zeef LAH, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295
Bülow L, Schindler M, Choi C, Hehl R (2004) PathoPlant®: a database on plant-pathogen interactions. In Silico Biol 4:529–536
Burkhead JL, Gogolin Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816
Caparrós-Ruiz D, Fornalé S, Civardi L, Puigdomènech P, Rigau J (2006) Isolation and characterization of a family of laccases in maize. Plant Sci 171:217–225
Cardon G, Höhmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237:91–104
Ceriotti A, Duranti M, Bollini R (1998) Effects of N-glycosylation on the folding and structure of plant proteins. J Exp Bot 49:1091–1103
Chan C-S, Guo L, Shih M-C (2001) Promoter analysis of the nuclear gene encoding the chloroplast glyceraldehyde-3-phosphate dehydrogenase B subunit of Arabidopsis thaliana. Plant Mol Biol 46:131–141
Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129:706–716
Claus H (2003) Laccases and their occurrence in prokaryotes. Arch Microbiol 179:145–150
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Cooper SJ, Trinklein ND, Anton ED, Nguyen L, Myers RM (2006) Comprehensive analysis of transcriptional promoter structure and function in 1% of the human genome. Genome Res 16:1–10
Davin LB, Wang H-B, Crowell AL, Bedgar DL, Martin DM, Sarkanen S, Lewis NG (1997) Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science 275:362–366
Dean JFD, Eriksson K-EL (1994) Laccase and the evolution of lignin in vascular plants. Holzforschung 48:S21–S33
Dean JFD, LaFayette PR, Rugh C, Tristram AH, Hoopes JT, Eriksson K-EL, Merkle SA (1998) Laccase associated with lignifying vascular tissues. In: Lewis NG, Sarkanen S (eds) Lignin and lignan biosynthesis, vol 697. American Chemical Society Symposium Series, Washington, DC, pp 96–108
Dharmawardhana DP, Ellis BE, Carlson JE (1992) Characterization of vascular lignification in Arabidopsis thaliana. Can J Bot 70:2238–2244
Dittmer NT, Suderman RJ, Jiang H, Zhu Y-C, Gorman MJ, Kramer KJ, Kanost MR (2004) Characterization of cDNAs encoding putative laccase-like multicopper oxidases and developmental expression in the tobacco hornworm, Manduca sexta, and the malaria mosquito, Anopheles gambiae. Insect Biochem Mol Biol 34:29–41
Driouich A, Lainé A-C, Vian B, Faye L (1992) Characterization and localization of laccase forms in stem and cell cultures of sycamore. Plant J 2:13–24
Ducros V, Brzozowski AM, Wilson KS, Brown SH, Østergaard P, Schneider P, Yaver DS, Pedersen AH, Davies GJ (1998) Crystal structure of the type-2 Cu depleted laccase from Coprinus cinereus at 2.2 Å resolution. Nat Struct Biol 5:310–316
Edlund AF, Swanson R, Preuss D (2004) Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16:S84–S97
Ehlting J, Mattheus N, Aeschliman DS, Li E, Hamberger B, Cullis IF, Zhuang J, Kaneda M, Mansfield SD, Samuels L, Ritland K, Ellis BE, Bohlmann J, Douglas CJ (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
Freudenberg K (1959) Biosynthesis and constitution of lignin. Nature 183:1152–1155
Galuszka P, Frébortová J, Luhová L, Bilyeu KD, English JT, Frébort I (2005) Tissue localization of cytokinin dehydrogenase in maize: possible involvement of quinone species generated from plant phenolics by other enzymatic systems in the catalytic reaction. Plant Cell Physiol 46:716–728
Gavnholt B, Larsen K, Rasmussen SK (2002) Isolation and characterization of laccase cDNAs from meristematic and stem tissues of ryegrass (Lolium perenne). Plant Sci 162:873–885
Graziani MT, Antonilli L, Sganga P, Citro G, Mondovi B, Rosei MA (1990) Biochemical and immunological studies of deglycosylated Rhus vernicifera laccase. Biochem Int 21:1113–1124
Hatton D, Sablowski R, Yung M-H, Smith C, Schuch W, Bevan M (1995) Two classes of cis sequences contribute to tissue-specific expression of a PAL2 promoter in transgenic tobacco. Plant J 7:859–876
Haughn G, Chaudhury A (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci 10:472–477
Heazlewood JL, Durek P, Hummel J, Selbig J, Weckwerth W, Walther D, Schulze WX (2008) PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor. Nucleic Acids Res 36:D1015–D1021
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300
Higuchi T, 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
Höfgen R, Willmitzer L (1988) Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res 16:9877
Hoopes JT, Dean JFD (2004) Ferroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipifera. Plant Physiol Biochem 42:27–33
Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics Article ID420747. doi:10.1155/2008/420747
Hülskamp M (2004) Plant trichomes: a model for cell differentiation. Nat Rev Mol Cell Biol 5:471–480
Hunter T (2000) Signaling—2000 and beyond. Cell 100:113–127
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53
Kang JS, Frank J, Kang CH, Kajiura H, Vikram M, Ueda A, Kim S, Bahk JD, Triplett B, Fujiyama K, Lee SY, von Schaewen A, Koiwa H (2008) Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proc Natl Acad Sci USA 105:5933–5938
Kim K-W, Franceschi VR, Davin LB, Lewis NG (2006) β-Glucuronidase as reporter gene: advantages and limitations. In: Salinas J, Sanchez-Serrano JJ (eds) Methods in molecular biology: Arabidopsis protocols, vol 323, 2nd edn. Humana Press, Totowa, NJ, pp 263–273
Kim S-J, Kim K-W, Cho M-H, Franceschi VR, Davin LB, Lewis NG (2007) Expression of cinnamyl alcohol dehydrogenases and their putative homologues during Arabidopsis thaliana growth and development: lessons for database annotations? Phytochemistry 68:1957–1974
LaFayette PR, Eriksson K-EL, Dean JFD (1995) Nucleotide sequence of a cDNA clone encoding an acidic laccase from sycamore maple (Acer pseudoplatanus L.). Plant Physiol 107:667–668
LaFayette PR, Eriksson K-EL, Dean JFD (1999) Characterization and heterologous expression of laccase cDNAs from xylem tissues of yellow-poplar (Liriodendron tulipifera). Plant Mol Biol 40:23–35
Lewis NG, Davin LB, Sarkanen S (1999) The nature and function of lignins. In: Barton Sir DHR, Nakanishi K, Meth-Cohn O (eds) Comprehensive natural products chemistry, vol 3. Elsevier, Oxford, UK, pp 617–745
Liu L, Dean JFD, Friedman WE, Eriksson K-EL (1994) A laccase-like phenoloxidase is correlated with lignin biosynthesis in Zinnia elegans stem tissues. Plant J 6:213–224
Lu C, Tej SS, Luo S, Haudenschild CD, Meyers BC, Green PJ (2005) Elucidation of the small RNA component of the transcriptome. Science 309:1567–1569
Madzak C, Mimmi MC, Caminade E, Brault A, Baumberger S, Briozzo P, Mougin C, Jolivalt C (2006) Shifting the optimal pH of activity for a laccase from the fungus Trametes versicolor by structure-based mutagenesis. Protein Eng Des Sel 19:77–84
Mattinen M-L, Kruus K, Buchert J, Nielsen JH, Andersen HJ, Steffensen CL (2005) Laccase-catalyzed polymerization of tyrosine-containing peptides. FEBS J 272:3640–3650
Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60:551–565
McCaig BC, Meagher RB, Dean JFD (2005) Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana. Planta 221:619–636
McDougall GJ (2000) A comparison of proteins from the developing xylem of compression and non-compression wood of branches of Sitka spruce (Picea sitchensis) reveals a differentially expressed laccase. J Exp Bot 51:1395–1401
Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006
Nakamura T (1958) Purification and physico-chemical properties of laccase. Biochim Biophys Acta 30:44–52
Nakatsubo T, Mizutani M, Suzuki S, Hattori T, Umezawa T (2008) Characterization of Arabidopsis thaliana pinoresinol reductase, a new type of enzyme involved in lignan biosynthesis. J Biol Chem 283:15550–15557
Niemetz R, Gross GG (2003) Oxidation of pentagalloylglucose to the ellagitannin, tellimagrandin II, by a phenol oxidase from Tellima grandiflora leaves. Phytochemistry 62:301–306
Niemetz R, Schilling G, Gross GG (2003) Biosynthesis of the dimeric ellagitannin, cornusiin E, in Tellima grandiflora. Phytochemistry 64:109–114
Nitta K, Kataoka K, Sakurai T (2002) Primary structure of a Japanese lacquer tree laccase as a prototype enzyme of multicopper oxidases. J Inorg Biochem 91:125–131
O’Connor TR, Dyreson C, Wyrick JJ (2005) Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences. Bioinformatics 21:4411–4413
Patten AM, Jourdes M, Cardenas CL, Laskar DD, Nakazawa Y, Chung BY, Franceschi VR, Davin LB, Lewis NG (2010) Probing native lignin macromolecular configuration in Arabidopsis thaliana in specific cell wall types: further insights into limited substrate degeneracy and assembly of the lignins of ref8, fah 1-2 and C4H:F5H lines. Mol Biosyst 6:499–515
Persson S, Wei H, Milne J, Page GP, Somerville CR (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102:8633–8638
Pickel B, Constantin M-A, Pfannstiel J, Conrad J, Beifuss U, Schaller A (2010) An enantiocomplementary dirigent protein for the enantioselective laccase-catalyzed oxidative coupling of phenols. Angew Chem Int Ed Engl 49:202–204
Pilot G, Stransky H, Bushey DF, Pratelli R, Ludewig U, Wingate VPM, Frommer WB (2004) Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from hydathodes of Arabidopsis leaves. Plant Cell 16:1827–1840
Piontek K, Antorini M, Choinowski T (2002) Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-Å resolution containing a full complement of coppers. J Biol Chem 277:37663–37669
Pourcel L, Routaboul J-M, Kerhoas L, Caboche M, Lepiniec L, 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
Raes J, Rohde A, Christensen JH, Van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071
Ranocha P, McDougall G, Hawkins S, Sterjiades R, Borderies G, Stewart D, Cabanes-Macheteau M, Boudet A-M, Goffner D (1999) Biochemical characterization, molecular cloning and expression of laccases—a divergent gene family—in poplar. Eur J Biochem 259:485–495
Ranocha P, Chabannes M, Chamayou S, Danoun S, Jauneau A, Boudet A-M, Goffner D (2002) Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiol 129:145–155
Reinhammar B (1970) Purification and properties of laccase and stellacyanin from Rhus vernicifera. Biochim Biophys Acta 205:35–47
Reinhammar B, Malmstroem BG (1981) “Blue” copper-containing oxidases. In: Spiro TG (ed) Copper proteins, vol 3. Wiley, New York, NY, pp 109–149
Richardson A, Duncan J, McDougall GJ (2000) Oxidase activity in lignifying xylem of a taxonomically diverse range of trees: identification of a conifer laccase. Tree Physiol 20:1039–1047
Saloheimo M, Niku-Paavola M-L, Knowles JKC (1991) Isolation and structural analysis of the laccase gene from the lignin-degrading fungus Phlebia radiata. J Gen Microbiol 137:1537–1544
Sato Y, Bao W, Sederoff R, Whetten R (2001) Molecular cloning and expression of eight laccase cDNAs in loblolly pine (Pinus taeda). J Plant Res 114:147–155
Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357
Sibout R, Eudes A, Mouille G, Pollet B, Lapierre C, Jouanin L, 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
Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9:355–365
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767
Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem Rev 96:2563–2605
Sterjiades R, Dean JFD, Eriksson K-EL (1992) Laccase from sycamore maple (Acer pseudoplatanus) polymerizes monolignols. Plant Physiol 99:1162–1168
Stewart CN Jr, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechnology 14:748–750
Takahama U (1995) Oxidation of hydroxycinnamic acid and hydroxycinnamyl alcohol derivatives by laccase and peroxidase. Interactions among p-hydroxyphenyl, guaiacyl and syringyl groups during the oxidation reactions. Physiol Plant 93:61–68
Taylor AB, Stoj CS, Ziegler L, Kosman DJ, Hart PJ (2005) The copper-iron connection in biology: structure of the metallo-oxidase Fet3p. Proc Natl Acad Sci USA 102:15459–15464
Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The Botany Array Resource: e-northerns, expression angling, and promoter analyses. Plant J 43:153–163
Tsugeki R, Fedoroff NV (1999) Genetic ablation of root cap cells in Arabidopsis. Proc Natl Acad Sci USA 96:12941–12946
Ulmasov T, Hagen G, Guilfoyle TJ (1999) Dimerization and DNA binding of auxin response factors. Plant J 19:309–319
Vassão DG, Kim K-W, Davin LB, Lewis NG (2010) Lignans (neolignans) and allyl/propenyl phenols: biogenesis, structural biology, and biological/human health considerations. In: Townsend C, Ebizuka Y (eds) Comprehensive natural products chemistry II. Elsevier, Oxford, UK, vol 1: structural diversity I, pp 815–928
Wang G-D, Li Q-J, Luo B, Chen X-Y (2004) Ex planta phytoremediation of trichlorophenol and phenolic allelochemicals via an engineered secretory laccase. Nat Biotechnol 22:893–897
Wang X-J, Gaasterland T, Chua N-H (2005) Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana. Genome Biol 6:R30. doi:10.1186/gb-2005-6-4-r30
Western TL, Skinner DJ, Haughn GW (2000) Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiol 122:345–355
Weymouth N, Dean JFD, Eriksson K-EL, Morrison WH III, Himmelsbach DS, Hartley RD (1993) Synthesis and spectroscopic characterization of p-hydroxyphenyl, guaiacyl and syringyl lignin polymer models (DHPs). Nordic Pulp & Paper Research Journal 8:344–349, 383
Yoshida H (1883) Chemistry of lacquer (urushi). Part I. J Chem Soc 472–486
Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE (2007) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5:e129. doi:10.1371/journal.pbio.0050129
Zhou J, Lee C, Zhong R, Ye Z-H (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266
Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69
Acknowledgments
This research was supported in part by the National Science Foundation (MCB-0117260, Arabidopsis 2010), the United States Department of Energy (DE-FG-0397ER20259) and the G. Thomas and Anita Hargrove Center for Plant Genomic Research. The authors would also like to thank late Vincent R. Franceschi for his valuable advice and insights during this study and Julia Gothard-Szamosfalvi for growing/maintaining plants in the greenhouse facilities.
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Turlapati, P.V., Kim, KW., Davin, L.B. et al. The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s). Planta 233, 439–470 (2011). https://doi.org/10.1007/s00425-010-1298-3
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DOI: https://doi.org/10.1007/s00425-010-1298-3