Abstract
Phytophthora spp. is a primary pathogen in oomycete, causing economically and environmentally devastating epidemics of plants. Laccases have been found in all domains of life but have not been reported in oomycte. In this paper, laccase genes of Phytophthora spp. were identified in three genomes (Phytophthora capsici, Phytophthora sojae and Phytophthora ramorum). 18 laccase genes were identified in total, including four in P. capsici genome, six in P. sojae genome and eight in P. ramorum genome. Most of the predicted gene models shared typical fungal laccase character, possessing three conserved positions with one cysteine and ten histidine residues at these positions. Phylogenetic analysis illustrated that laccases from Phytophthora clustered into four clades, while fungal laccases clustered together. The results provided the theoretical ground for new hypotheses about the roles laccases in oomycetes and may guide the future research of these enzymes.
Similar content being viewed by others
References
Ausec L, Zakrzewski M, Goesmann A, Schluter A, Mandic-Mulec I (2011) Bioinformatic analysis reveals high diversity of bacterial genes for laccase-like enzymes. PLoS ONE 6:e25724. doi:10.1371/journal.pone.0025724
Baldrian P (2005) Fungal laccases-occurrence and properties. FEMS Microbiol Rev 30:215–242. doi:10.1111/j.1574-4976.2005.00010.x
Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795. doi:10.1016/j.jmb.2004.05.028
Bertrand T, Jolivalt C, Briozzo P, Caminade E, Joly N, Madzak C et al (2002) Crystal structure of a four-copper laccase complexed with an arylamine: insights into substrate recognition and correlation with kinetics. Biochemistry 41:7325–7333. doi:10.1021/bi0201318
Cañero DC, Roncero MIG (2008) Functional analysis of laccase genes from Fusarium oxysporum. Phytopathology 98:509–518. doi:10.1094/PHYTO-98-5-0509
Cavalier-Smith T, Chao EE (2006) Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J Mol Evol 62:388–420. doi:10.1007/s00239-004-0353-8
Chung HJ, Kwon BR, Kim JM, Park SM, Park JK, Cha BJ et al (2008) A tannic acid-inducible and hypoviral-regulated laccase3 contributes to the virulence of the chestnut blight fungus Cryphonectria parasitica. Mol Plant-Microbe Interact 21:1582–1589. doi:10.1094/MPMI-21-12-1582
Claus H (2004) Laccases: structure, reactions, distribution. Micron 35:93–96. doi:10.1016/j.micron.2003.10.029
Eggert C, Temp U, Eriksson KE (1997) Laccase is essential for lignin degradation by the white-rot fungus Pycnoporus cinnabarinus. FEBS Lett 407:89–92. doi:10.1016/S0014-5793(97)00301-3
Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. APS Press, USA
Fan F, Zhuo R, Sun S, Jiang M, Zhang X, Yang Y (2011) Cloning and functional analysis of a new laccase gene from Trametes sp. 48424 which had the high yield of laccase and strong ability for decolorizing different dyes. Bioresour Technol 102:3126–3137. doi:10.1016/j.biortech.2010.10.079
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Gupta N, Lee NS, Farinas ET (2010) Laboratory evolution of laccase for substrate specificity. J Mol Catal B Enzym 62:230–234. doi:10.1016/j.molcatb.2009.10.012
Hoegger PJ, Kilaru S, James TY, Thacker JR, Kues U (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273:2308–2326. doi:10.1111/j.1742-4658.2006.05247.x
Kallio JP, Auer S, Janis J, Andberg M, Kruus K, Rouvinen J et al (2009) Structure-function studies of a Melanocarpus albomyces laccase suggest a pathway for oxidation of phenolic compounds. J Mol Biol 392:895–909. doi:10.1016/j.jmb.2009.06.053
Kallio JP, Gaparetti C, Andberg M, Boer H, Koivula A, Kruus K et al (2011) Crystal structure of an ascomycete fungal laccase from Thielavia arenaria—common structural features of asco-laccases. FEBS J 278:2283–2295. doi:10.1111/j.1742-4658.2011.08146.x
Kim SE, Jae SM, Jung KK, Ran HY, Won SC, Eun NL et al (2010) Monitoring of possible horizontal gene transfer from transgenic potatoes to soil microorganisms in the potato fields and the emergence of variants in Phytophthora infestans. J Microbiol Biotechnol 20:1027–1031. doi:10.4014/jmb.1002.02028
Kumar SVS, Phale PS, Durani S, Wangikar PP (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83:386–394. doi:10.1002/bit.10681
LaFayette PR, Eriksson KE, Dean JFD (1999) Characterization and heterologous expression of laccase cDNA from xylem tissues of yellowpoplar (Liriodendron tulipifera). Plant Mol Biol 40:23–35. doi:10.1023/A:1026437406859
Lamour KH, Hausbeck MK (2004) Phytophthora capsici on vegeTable crops: research progress and management challenges. Plant Dis 88:1292–1303. doi:10.1094/PDIS.2004.88.12.1292
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404
Litvintseva AP, Henson JM (2002) Cloning, characterization, and transcription of three laccase genes from Gaeumannomyces graminis var. tritici, the take-all fungus. Appl Environ Microbiol 68:1305–1311. doi:10.1128/AEM.68.3.1305-1311.2002
Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–W331. doi:10.1093/nar/gkh454
Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH et al (2009) CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res 37:D205–D210. doi:10.1093/nar/gkn845
Matera I, Gullotto A, Tilli S, Ferraroni M, Scozzafava A, Briganti F (2008) Crystal structure of the blue multicopper oxidase from the white-rot fungus Tramete trogii complexed with p-toluate. Inorg Chim Acta 361:4129–4137. doi:10.1016/j.ica.2008.03.091
Morozova OV, Shumakovich GP, Gorbacheva MA, Shleev SV, Yaropolov AI (2007) “Blue” laccases. Biochemistry (Moscow) 72:1136–1150. doi:10.1134/S0006297907100112
Pihet M, Vandeputte P, Tronchin G, Renier G, Saulnier P, Georgeault S et al (2009) Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol 9:177. doi:10.1186/1471-2180-9-177
Ramos JT, Barends S, Verhaert R, de Graaff LH (2011) The Aspergillus niger multicopper oxidase family: analysis and overexpression of laccase-like encoding genes. Microb Cell Fact 10:78. doi:10.1186/1475-2859-10-78
Rigling D, Van Alfen NK (1993) Extra- and intracellular laccases of the chestnut blight fungus, Cryphonectria parasitica. Appl Environ Microbiol 59:3634–3639
Sugareva V, Härtl A, Brock M, Hübner K, Rohde M, Heinekamp T (2006) Characterisation of the laccase-encoding gene abr2 of the dihydroxynaphthalene-like melanin gene cluster of Aspergillus fumigatus. Arch Microbiol 186:345–355. doi:10.1007/s00203-006-0144-2
Temp U, Eggert C (1999) Novel interaction between laccase and cellobiose dehydrogenase during pigment synthesis in the white rot fungus Pycnoporus cinnabarinus. Appl Environ Microbiol 65:389–395
Tsai HF, Wheeler MH, Chang YC, Kwon-Chung KJ (1999) A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J Bacteriol 181:6469–6477
Tyler BM (2001) Genetics and genomics of the oomycete–host interface. Trends Genet 17:611–614. doi:10.1016/S0168-9525(01)02517-3
Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99:15507–15512. doi:10.1046/j.1529-8817.38.s1.8.x
Zhu X, Gibbons J, Garcia-Rivera J, Casadevall A, Williamson PR (2001) Laccase of Cryptococcus neoformans is a cell wall-associated virulence factor. Infect Immun 69:5589–5596. doi:10.1128/IAI.69.9.5589-5596.2001
Zhukhlistova NE, Zhukova YN, Lyashenko AV, Zaitsev VN, Mikhailov AM (2008) Three-dimensional organization of three-domain copper oxidases: a review. Crystallogr Rep 53:92–109. doi:10.1134/S1063774508010124
Acknowledgments
This research was supported by Program of University of Science and Technology of Shanxi province (20121025) and doctoral fund of Yuncheng University (YQ-2011037).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Feng, B., Li, P. Genome-wide identification of laccase gene family in three Phytophthora species. Genetica 140, 477–484 (2012). https://doi.org/10.1007/s10709-012-9696-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-012-9696-z