Abstract
Some plant species colonize mining-contaminated soils. They are adapted to harsh growth conditions and show high native phytoremediation abilities. For environmental cleanup, these species can be improved by genetic manipulation. Laccases are ligninolytic enzymes that oxidise a broad range of substrates by a radical-catalysed reaction mechanism using oxygen as the electron acceptor. Fungi of the genus Pycnoporus produce laccases with important biotechnological, industrial and environmental applications. Here we describe a successful attempt of Agrobacterium rhizogenes mediated stable transformation of Nicotiana glauca, a species naturally resistant to metal-contaminated soils. The coding region of a Pycnoporus sanguineus laccase gene was fused with the Nicotiana plumbaginifolia calreticulin apoplast targeting signal and driven by the constitutive cauliflower mosaic virus (CaMV) 35S promoter (2X35S). The obtained transgenic N. glauca callus cells secreted a recombinant fungal laccase into the growth medium and were capable to degrade an anthraquinone dye, Remazol Brilliant Blue R. Under phenol and cadmium stresses, the transgenic calli not only maintained their growth capacity but their relative growth rate was greater compared to callus transformed with empty vector. This work shows that stable expression of a fungal laccase in a plant species resistant to heavy metals presents a successful strategy that potentially can be used to combat combined organic and inorganic contamination.
Key message
A fungal laccase was heterologously expressed in a heavy metal-tolerant plant species. The transgenic callus was capable of growth in medium supplemented with organic and inorganic contaminants.
Similar content being viewed by others
References
Aoki S, Syono K (1999) Synergistic function of rolB, rolC, ORF13 and ORF14 of TL-DNA of Agrobacterium rhizogenes in hairy root induction in Nicotiana tabacum. Plant Cell Physiol 40:252–256. https://doi.org/10.1093/oxfordjournals.pcp.a029535
Ayadi R, Trémouillaux-Guiller J (2003) Root formation from transgenic calli of Ginkgo biloba. Tree Physiol 23:713–718. https://doi.org/10.1093/treephys/23.10.713
Balcázar-López E, Méndez-Lorenzo LH, Batista-García RA, Esquivel-Naranjo U, Ayala M, Kumar VV, Savary O, Cabana H, Herrera-Estrella A, Folch-Mallol JL (2016) Xenobiotic compounds degradation by heterologous expression of a Trametes sanguineus laccase in Trichoderma atroviride. PLoS ONE 11(2):e0147997. https://doi.org/10.1371/journal.pone.0147997
Baldrian P (2006) Fungal laccases–occurrence and properties. FEMS Microbiol Rev 30:215–242. https://doi.org/10.1111/j.1574-4976.2005.00010.x
Baldrian P, Gabriel J (1997) Effect of heavy metals on the growth of selected wood-rotting basidiomycetes. Folia Microbiol 42:521–523
Balen B, Leljak-Levanic D, Mihaijević S, Jelenić S, Jelaska S (2004) Formation of embryogenic callus in hairy roots of pumpkin (Cucurbita pepo L.). Vitro Cell Dev Biol-Plant 40:182–187. https://doi.org/10.1079/IVP2003516
Barazani O, Sathiyamoorthy P, Manandhar U, Vulkan R, Golan-Goldhirsh A (2004) Heavy metal accumulation by Nicotiana glauca Graham in a solid waste disposal site. Chemosphere 54:867–872. https://doi.org/10.1016/j.chemosphere.2003.10.005
Benchabane M, Goulet C, Rivard D, Faye L, Gomord V, Michaud D (2008) Preventing unintended proteolysis in plant protein biofactories. Plant Biotechnol J 6:633–648. https://doi.org/10.1111/j.1467-7652.2008.00344.x
Borisjuk N, Sitailo L, Adler K, Malysheva L, Tewes A, Borisjuk L, Manteuffel R (1998) Calreticulin expression in plant cells: developmental regulation, tissue specificity and intracellular distribution. Planta 206:504–514. https://doi.org/10.1007/s004250050427
Borisjuk NV, Borisjuk LG, Logendra S, Petersen F, Gleba Y, Raskin I (1999) Production of recombinant proteins in plant root exudates. Nat Biotechnol 17:466–469. https://doi.org/10.1038/8643
Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157:42–48. https://doi.org/10.1016/j.envpol.2008.07.028
Capone I, Spanò L, Cardarelli M, Bellincampi D, Petit A, Costantino P (1989) Induction and growth properties of carrot roots with different complements of Agrobacterium rhizogenes T-DNA. Plant Mol Biol 13:43–52. https://doi.org/10.1007/BF00027334
Cerniglia CE, Sutherland JB (2010) Degradation of polycyclic aromatic hydrocarbons by fungi. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 2079–2110. https://doi.org/10.1007/978-3-540-77587-4_151
Chakrabarty R, Banerjee R, Chung SM, Farman M, Citovsky V, Hogenhout SA, Tzfira T, Goodin M (2007) pSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana-virus interactions. Mol Plant Microbe Interact 20:740–750. https://doi.org/10.1094/MPMI-20-7-0740
Choi PS, Kim YD, Choi KM, Chung HJ, Choi DW, Liu JR (2004) Plant regeneration from hairy-root cultures transformed by infection with Agrobacterium rhizogenes in Catharanthus roseus. Plant Cell Rep 22:828–831. https://doi.org/10.1007/s00299-004-0765-3
Christey MC, Braun RH (2005) Production of hairy root cultures and transgenic plants by Agrobacterium rhizogenes-mediated transformation. In: Peña L (ed) Transgenic plants: methods and protocols. Methods in molecular biology. Humana Press, New Jersey, pp 47–60. https://doi.org/10.1385/1-59259-827-7:047
Chroma L, Macek T, Demnerova K, Macková M (2002) Decolorization of RBBR by plant cells and correlation with the transformation of PCBs. Chemosphere 49:739–748. https://doi.org/10.1016/S0045-6535(02)00397-1
Curt MD, Fernández J (1990) Production of Nicotiana glauca R.C. Graham aerial biomass in relation to irrigation regime. Biomass 23:103–115. https://doi.org/10.1016/0144-4565(90)90029-J
de Araujo BS, Dec J, Bollag JM, Pletsch M (2006) Uptake and transformation of phenol and chlorophenols by hairy root cultures of Daucus carota, Ipomoea batatas and Solanum aviculare. Chemosphere 63:642–651. https://doi.org/10.1016/j.chemosphere.2005.08.005
De Loose M, Gheysen G, Tiré C, Gielen J, Villarroel R, Genetello C, Van Montagu M, Depicker A, Inzé D (1991) The extensin signal peptide allows secretion of a heterologous protein from protoplasts. Gene 99:95–100. https://doi.org/10.1016/0378-1119(91)90038-D
de Ruijter JC, Koskela EV, Nandania J, Frey AD, Velagapudi V (2018) Understanding the metabolic burden of recombinant antibody production in Saccharomyces cerevisiae using a quantitative metabolomics approach. Yeast 35:331–341. https://doi.org/10.1002/yea.3298
Denecke J, Botterman J, Deblaere R (1990) Protein secretion in plant cells can occur via a default pathway. Plant Cell 2:51–59. https://doi.org/10.2307/3869050
Doty SL, Shang TQ, Wilson AM, Tangen J, Westergreen AD, Newman LA, Strand SE, Gordon MP (2000) Enhanced metabolism of halogenated hydrocarbons in transgenic plants containing mammalian cytochrome P450 2E1. Proc Natl Acad Sci USA 97:6287–6291. https://doi.org/10.1073/pnas.97.12.6287
Dubrovskaya E, Pozdnyakova N, Golubev S, Muratova A, Grinev V, Bondarenkova A, Turkovskaya O (2017) Peroxidases from root exudates of Medicago sativa and Sorghum bicolor: catalytic properties and involvement in PAH degradation. Chemosphere 169:224–232. https://doi.org/10.1016/j.chemosphere.2016.11.027
Eggert C, Temp U, Dean JFD, Eriksson KEL (1996) A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase. FEBS Lett 391:144–148. https://doi.org/10.1016/0014-5793(96)00719-3
Enstone DE, Peterson CA, Ma F (2002) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351. https://doi.org/10.1007/s00344-003-0002-2
Fewson CA (1988) Biodegradation of xenobiotic and other persistent compounds: the causes of recalcitrance. Trends Biotechnol 6:148–153. https://doi.org/10.1016/0167-7799(88)90084-4
Frasconi M, Favero G, Boer H, Koivula A, Mazzei F (2010) Kinetic and biochemical properties of high and low redox potential laccases from fungal and plant origin. Biochim Biophys Acta 1804:899–908. https://doi.org/10.1016/j.bbapap.2009.12.018
Gaume A, Komarnytsky S, Borisjuk N, Raskin I (2003) Rhizosecretion of recombinant proteins from plant hairy roots. Plant Cell Rep 21:1188–1193. https://doi.org/10.1007/s00299-003-0660-3
Geldner N (2013) The endodermis. Annu Rev Plant Biol 64:531–558. https://doi.org/10.1146/annurev-arplant-050312-120050
Glick BR (1995) Metabolic load and heterologous gene expression. Biotechnol Adv 13:247–261. https://doi.org/10.1016/0734-9750(95)00004-A
Gratão PL, Pompeu GB, Capaldi FR, Vitorello VA, Lea PJ, Azevedo RA (2008) Antioxidant response of Nicotiana tabacum cv. Bright Yellow 2 cells to cadmium and nickel stress. Plant Cell Tiss Organ Cult 94:73–83. https://doi.org/10.1007/s11240-008-9389-6
Gurusamy PD, Schäfer H, Ramamoorthy S, Wink M (2017) Biologically active recombinant human erythropoietin expressed in hairy root cultures and regenerated plantlets of Nicotiana tabacum L. PLoS ONE 12(8):e0182367. https://doi.org/10.1371/journal.pone.0182367
Harkin JM, Obst JR (1973) Syringaldazine, an effective reagent for detecting laccase and peroxidase in fungi. Experientia 29:381–387. https://doi.org/10.1007/BF01926734
He J, Li H, Ma C, Zhang Y, Polle A, Rennenberg H, Cheng X, Luo Z-B (2015) Overexpression of bacterial γ-glutamylcysteine synthetase mediates changes in cadmium influx, allocation and detoxification in poplar. New Phytol 205:240–254. https://doi.org/10.1111/nph.13013
Heckman KL, Pease LR (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc 2:924–932. https://doi.org/10.1038/nprot.2007.132
Hunt R (1982) Plant growth curves: a functional approach to plant growth analysis. Edward Arnold, London
Iskander FY, Vega-Carrillo HR, Manzanares EA (1994) Determination of mercury and other elements in La Zacatecana Dam sediment in Mexico. Sci Total Environ 148:43–48. https://doi.org/10.1016/0048-9697(94)90372-7
Iturriaga G, Jefferson RA, Bevan MW (1989) Endoplasmic reticulum targeting and glycosylation of hybrid proteins in transgenic tobacco. Plant Cell 1:381–390. https://doi.org/10.1105/tpc.1.3.381
James CA, Strand SE (2009) Phytoremediation of small organic contaminants using transgenic plants. Curr Opin Biotechnol 20:237–241. https://doi.org/10.1016/j.copbio.2009.02.014
Jin H, Jia JF, Hao JG (2003) Protoplasts from Agrobacterium rhizogenes-transformed cell line of Medicago sativa L. regenerated to hairy roots. Vitro Cell Dev Biol. Plant 39:208–211. https://doi.org/10.1079/IVP2002367
Klose H, Günl M, Usadel B, Fischer R, Commandeur U (2013) Ethanol inducible expression of a mesophilic cellulase avoids adverse effects on plant development. Biotechnol Biofuels 6:53. https://doi.org/10.1186/1754-6834-6-53
Komarnytsky S, Borisjuk N, Yakoby N, Garvey A, Raskin I (2006) Cosecretion of protease inhibitor stabilizes antibodies produced by plant roots. Plant Physiol 141:1185–1193. https://doi.org/10.1104/pp.105.074419
Liu H, Zhao H, Wu L, Liu A, Zhao FJ, Xu W (2017) Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol 215:687–698. https://doi.org/10.1111/nph.14622
Lomascolo A, Uzan-Boukhris E, Herpoël-Gimbert I, Sigoillot JC, Lesage-Meessen L (2011) Peculiarities of Pycnoporus species for applications in biotechnology. Appl Microbiol Biotechnol 92:1129–1149. https://doi.org/10.1007/s00253-011-3596-5
Lu L, Zhao M, Zhang BB, Yu SY, Bian XJ, Wang W, Yan W (2007) Purification and characterization of laccase from Pycnoporus sanguineus and decolorization of an anthraquinone dye by the enzyme. Appl Microbiol Biotechnol 74:1232–1239. https://doi.org/10.1007/s00253-006-0767-x
Lund P, Lee RY, Dunsmuir P (1989) Bacterial chitinase is modified and secreted in transgenic tobacco. Plant Physiol 91:130–135. https://doi.org/10.1104/pp.91.1.130
Mariani P, Navazio L, Zuppini A (2003) Calreticulin and the endoplasmic reticulum in plant cell biology. In: Eggleton P, Michalak M (eds) Calreticulin. Molecular biology intelligence unit. Springer, Boston, pp 94–104
Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60:551–565. https://doi.org/10.1016/S0031-9422(02)00171-1
Mei WY, Wang JB, Luo D, Jia JF (2001) Regeneration of plants from callus cultures of roots induced by Agrobacterium rhizogenes on Alhagi pseudoalhagi. Cell Res 11:279–284. https://doi.org/10.1038/sj.cr.7290097
Migocka M, Kosieradzka A, Papierniak A, Maciaszczyk-Dziubinska E, Posyniak E, Garbiec A, Filleur S (2015) Two metal-tolerance proteins, MTP1 and MTP4, are involved in Zn homeostasis and Cd sequestration in cucumber cells. J Exp Bot 66:1001–1015. https://doi.org/10.1093/jxb/eru459
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plantarum 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nakagawa Y, Sakamoto Y, Kikuchi S, Sato T, Yano A (2010) A chimeric laccase with hybrid properties of the parental Lentinula edodes laccases. Microbiol Res 165:392–401. https://doi.org/10.1016/j.micres.2009.08.006
Nanasato Y, Namiki S, Oshima M, Moriuchi R, Konagaya K, Seike N, Otani T, Nagata Y, Tsuda M, Tabei Y (2016) Biodegradation of γ-hexachlorocyclohexane by transgenic hairy root cultures of Cucurbita moschata that accumulate recombinant bacterial LinA. Plant Cell Rep 35:1963–1974. https://doi.org/10.1007/s00299-016-2011-1
Nordberg GF, Bernard A, Diamond GL, Duffus JH, Illing P, Nordberg M, Bergdahl IA, Jin T, Skerfving S (2018) Risk assessment of effects of cadmium on human health (IUPAC Technical Report). Pure Appl Chem 90:755–808. https://doi.org/10.1515/pac-2016-0910
Ohara A, Akasaka Y, Daimon H, Mii M (2000) Plant regeneration from hairy roots induced by infection with Agrobacterium rhizogenes in Crotalaria juncea L. Plant Cell Rep 19:563–568. https://doi.org/10.1007/s002990050774
Oinonen P, Zhang L, Lawoko M, Henriksson G (2015) On the formation of lignin polysaccharide networks in Norway spruce. Phytochemistry 111:177–184. https://doi.org/10.1016/j.phytochem.2014.10.027
Persans MW, Nieman K, Salt DE (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc Natl Acad Sci USA 98:9995–10000. https://doi.org/10.1073/pnas.171039798
Ponstein AS, Verwoerd TC, Pen J (1996) Production of enzymes for industrial use. Ann NY Acad Sci 792:91–98. https://doi.org/10.1111/j.1749-6632.1996.tb32495.x
Poschenrieder C, Cabot C, Martos S, Gallego B, Barceló J (2013) Do toxic ions induce hormesis in plants? Plant Sci 212:15–25. https://doi.org/10.1016/j.plantsci.2013.07.012
Ramalingam B, Sana B, Seayad J, Ghadessy FJ, Sullivan MB (2017) Towards understanding of laccase-catalysed oxidative oligomerisation of dimeric lignin model compounds. RSC Adv 7:11951–11958. https://doi.org/10.1039/C6RA26975C
Ramírez-Cavazos LI, Junghanns C, Ornelas-Soto N, Cárdenas-Chávez DL, Hernández-Luna C, Demarche P, Enaud E, García-Morales R, Agathos N, Parra R (2014) Purification and characterization of two thermostable laccases from Pycnoporus sanguineus and potential role in degradation of endocrine disrupting chemicals. J Mol Catal B Enzym 108:32–42. https://doi.org/10.1016/j.molcatb.2014.06.006
Ranocha P, McDougall G, Hawkins S, Sterjiades R, Borderies G, Stewart D, Cabanes-Macheteau M, Boudet AM, Goffner D (1999) Biochemical characterization, molecular cloning and expression of laccases—a divergent gene family—in poplar. Eur J Biochem 259:485–495. https://doi.org/10.1046/j.1432-1327.1999.00061.x
Ranocha P, Chabannes M, Chamayou S, Danoun S, Jauneau A, Boudet AM, Goffner D (2002) Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiol 129:145–155. https://doi.org/10.1104/pp.010988
Rieger PG, Meier HM, Gerle M, Vogt U, Groth T, Knackmuss HJ (2002) Xenobiotics in the environment: present and future strategies to obviate the problem of biological persistence. J Biotechnol 94:101–123. https://doi.org/10.1016/S0168-1656(01)00422-9
Rodgers CJ, Blanford CF, Giddens SR, Skamnioti P, Armstrong FA, Gurr SJ (2010) Designer laccases: a vogue for high-potential fungal enzymes? Trends Biotechnol 28:63–72. https://doi.org/10.1016/j.tibtech.2009.11.001
Sakamoto Y, Nakade K, Yano A, Nakagawa Y, Hirano T, Irie T, Watanabe H, Nagai M, Sato T (2008) Heterologous expression of lcc1 from Lentinula edodes in tobacco BY-2 cells results in the production an active, secreted form of fungal laccase. Appl Microbiol Biotechnol 79:971–980. https://doi.org/10.1007/s00253-008-1507-1
Salas-Luévano MA, Mauricio-Castillo JA, González-Rivera ML, Vega-Carrillo HR, Salas-Muñoz S (2017) Accumulation and phytostabilization of As, Pb and Cd in plants growing inside mine tailings reforested in Zacatecas. México. Environ Earth Sci 76:806. https://doi.org/10.1007/s12665-017-7139-y
San Miguel A, Schröder P, Harpaintner R, Gaude T, Ravanel P, Raveton M (2013) Response of phase II detoxification enzymes in Phragmites australis plants exposed to organochlorines. Environ Sci Pollut Res 20:3464–3471. https://doi.org/10.1007/s11356-012-1301-6
Santos-Jallath J, Castro-Rodríguez A, Huezo-Casillas J, Torres-Bustillos L (2012) Arsenic and heavy metals in native plants at tailings impoundments in Queretaro, Mexico. Phys Chem Earth 37–39:10–17. https://doi.org/10.1016/j.pce.2011.12.002
Santos-Santos E, Yarto-Ramírez M, Gavilán-García I, Castro-Díaz J, Gavilán-García A, Rosiles R, Suárez S, López-Villegas T (2006) Analysis of arsenic, lead and mercury in farming areas with mining contaminated soils at Zacatecas, Mexico. J Mex Chem Soc 50:57–63
Schuetz M, Benske A, Smith RA, Watanabe Y, Tobimatsu Y, Ralph J, Demura T, Ellis B, Samuels AL (2014) Laccases direct lignification in the discrete secondary cell wall domains of protoxylem. Plant Physiol 166:798–807. https://doi.org/10.1104/pp.114.245597
Shanmugaraj BM, Malla A, Ramalingam S (2019) Cadmium stress and toxicity in plants: an overview. In: Hasanuzzaman M, Prasad MNV, Fujita M (eds) Cadmium toxicity and tolerance in plants from physiology to remediation. Academic Press, Cambridge, pp 1–17. https://doi.org/10.1016/B978-0-12-814864-8.00001-2
Shapir N, Mongodin EF, Sadowsky MJ, Daugherty SC, Nelson KE, Wackett LP (2007) Evolution of catabolic pathways: genomic insights into microbial s-triazine metabolism. J Bacteriol 189:674–682. https://doi.org/10.1128/JB.01257-06
Shingu Y, Kudo T, Ohsato S, Kimura M, Ono Y, Yamaguchi I, Hamamoto H (2005) Characterization of genes encoding metal tolerance proteins isolated from Nicotiana glauca and Nicotiana tabacum. Biochem Biophys Res Commun 331:675–680. https://doi.org/10.1016/j.bbrc.2005.04.010
Sonoki T, Kajita S, Ikeda S, Uesugi M, Tatsumi K, Katayama Y, Iimura Y (2005) Transgenic tobacco expressing fungal laccase promotes the detoxification of environmental pollutants. Appl Microbiol Biotechnol 67:138–142. https://doi.org/10.1007/s00253-004-1770-8
Spiess T, Desiere F, Fischer P, Spain JC, Knackmuss HJ, Lenke H (1998) A new 4-nitrotoluene degradation pathway in a Mycobacterium strain. Appl Environ Microbiol 64:446–452
Spina F, Cordero C, Schilirò T, Sgorbini B, Pignata C, Gilli G, Bicchi C, Varese GC (2015) Removal of micropollutants by fungal laccases in model solution and municipal wastewater: evaluation of estrogenic activity and ecotoxicity. J Clean Prod 100:185–194. https://doi.org/10.1016/j.jclepro.2015.03.047
Sudo H, Yamakawa T, Yamazaki M, Aimi N, Saito K (2002) Bioreactor production of camptothecin by hairy root cultures of Ophiorrhiza pumila. Biotechnol Lett 24:359–363. https://doi.org/10.1023/A:1014568904957
Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26. https://doi.org/10.1099/13500872-140-1-19
Uchida E, Ouchi T, Suzuki Y, Yoshida T, Habe H, Yamaguchi I, Omori T, Nojiri H (2005) Secretion of bacterial xenobiotic-degrading enzymes from transgenic plants by an apoplastic expressional system: an applicability for phytoremediation. Environ Sci Technol 39:7671–7677. https://doi.org/10.1021/es0506814
Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci USA 107:16500–16505. https://doi.org/10.1073/pnas.1005396107
Uzan E, Nousiainen P, Balland V, Sipila J, Piumi F, Navarro D, Asther M, Record E, Lomascolo A (2010) High redox potential laccases from the lignolytic fungi Pycnoporus coccineus and Pycnoporus sanguineus suitable for white biotechnology: from gene cloning to enzyme characterization and applications. J Appl Microbiol 108:2199–2213. https://doi.org/10.1111/j.1365-2672.2009.04623.x
van Rensburg E, den Haan R, Smith J, van Zyl WH, Görgens JF (2012) The metabolic burden of cellulase expression by recombinant Saccharomyces cerevisiae Y294 in aerobic batch culture. Appl Microbiol Biotechnol 96:197–209. https://doi.org/10.1007/s00253-012-4037-9
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372. https://doi.org/10.1016/j.pbi.2009.05.001
Vite-Vallejo O, Palomares LA, Dantán-González E, Ayala-Castro HG, Martínez-Anaya C, Valderrama B, Folch-Mallol J (2009) The role of N-glycosylation on the enzymatic activity of a Pycnoporus sanguineus laccase. Enzyme Microb Technol 45:233–239. https://doi.org/10.1016/j.enzmictec.2009.05.007
Wang GD, Li QJ, Luo B, Chen XY (2004) Ex planta phytoremediation of trichlorophenol and phenolic allelochemicals via an engineered secretory laccase. Nat Biotechnol 22:893–897. https://doi.org/10.1038/nbt982
Xu F, Shin W, Brown SH, Wahleithner JA, Sundaram UM, Solomon EI (1996) A study of a series of recombinant fungal laccases and bilirubin oxidase that exhibit significant differences in redox potential, substrate specificity and stability. Biochim Biophys Acta 1292:303–311. https://doi.org/10.1016/0167-4838(95)00210-3
Xu J, Tan L, Goodrum KJ, Kieliszewski MJ (2007) High-yields and extended serum half-life of human interferon α2b expressed in tobacco cells as arabinogalactan-protein fusions. Biotechnol Bioeng 97:997–1008. https://doi.org/10.1002/bit.21407
Xu J, Su ZH, Chen C, Han HJ, Zhu B, Fu XY, Zhao W, Jin XF, Wu AZ, Yao QH (2012) Stress responses to phenol in Arabidopsis and transcriptional changes revealed by microarray analysis. Planta 235:399–410. https://doi.org/10.1007/s00425-011-1498-5
Yuan L, Yang S, Liu B, Zhang M, Wu K (2012) Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell Rep 31:67–79. https://doi.org/10.1007/s00299-011-1140-9
Zdarta J, Antecka K, Frankowski R, Zgoła-Grześkowiak A, Ehrlich H, Jesionowski T (2018) The effect of operational parameters on the biodegradation of bisphenols by Trametes versicolor laccase immobilized on Hippospongia communis spongin scaffolds. Sci Total Environ 615:784–795. https://doi.org/10.1016/j.scitotenv.2017.09.213
Acknowledgements
We gratefully acknowledge D. Lagunas-Gómez, H.H. Torres-Martínez and S. Napsucialy-Mendivil from the Instituto de Biotecnología (IBt) of the Universidad Nacional Autónoma de México (UNAM) for technical assistance. We also acknowledge the technical help of the staff of the Core Facility of Oligonucleotide Synthesis and DNA Sequencing of the IBt, UNAM. R. De-Jesús-García was supported by a Ph.D. fellowship from Consejo Nacional de Ciencia y Tecnología (CONACyT). We extend special thanks to R. Vázquez-Duhalt for his participation in coordination of the Ph.D. project of R. De-Jesús-García. This work was partially supported by Dirección General de Asuntos del Personal Académico (DGAPA)—Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT)—UNAM (grants IN205315 and IN200818).
Author information
Authors and Affiliations
Contributions
RDJG and JGD designed the research. JGD and JLFM provided resources and conceptualised the research. RDJG performed all the experiments, RDJG and JGD analised the data. RDJG drafted and together with JGD wrote the final version of the manuscript. All authors read and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Goetz Hensel.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
De-Jesús-García, R., Folch-Mallol, J.L. & Dubrovsky, J.G. Transgenic callus of Nicotiana glauca stably expressing a fungal laccase maintains its growth in presence of organic contaminants. Plant Cell Tiss Organ Cult 138, 311–324 (2019). https://doi.org/10.1007/s11240-019-01626-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-019-01626-2