Transcriptomic Analysis Reveals the Roles of Detoxification Systems in Response to Mercury in Chromera velia

. 2019 Oct 24 ; 9 (11) : . [epub] 20191024

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31653042

Heavy metal pollution is an increasing global concern. Among heavy metals, mercury (Hg) is especially dangerous because of its massive release into the environment and high toxicity, especially for aquatic organisms. The molecular response mechanisms of algae to Hg exposure are mostly unknown. Here, we combine physiological, biochemical, and transcriptomic analysis to provide, for the first time, a comprehensive view on the pathways activated in Chromera velia in response to toxic levels of Hg. Production of hydrogen peroxide and superoxide anion, two reactive oxygen species (ROS), showed opposite patterns in response to Hg2+ while reactive nitrogen species (RNS) levels did not change. A deep RNA sequencing analysis generated a total of 307,738,790 high-quality reads assembled in 122,874 transcripts, representing 89,853 unigenes successfully annotated in databases. Detailed analysis of the differently expressed genes corroborates the biochemical results observed in ROS production and suggests novel putative molecular mechanisms in the algal response to Hg2+. Moreover, we indicated that important transcription factor (TF) families associated with stress responses differentially expressed in C. velia cultures under Hg stress. Our study presents the first in-depth transcriptomic analysis of C. velia, focusing on the expression of genes involved in different detoxification defense systems in response to heavy metal stress.

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Harada M. Minamata Disease: Methylmercury Poisoning in Japan Caused by Environmental Pollution. Crit. Rev. Toxicol. 1995;25:1–24. doi: 10.3109/10408449509089885. PubMed DOI

Lamborg C.H., Hammerschmidt C.R., Bowman K.L., Swarr G.J., Munson K.M., Ohnemus D.C., Lam P.J., Heimbürger L.-E., Rijkenberg M.J.A., Saito M.A. A global ocean inventory of anthropogenic mercury based on water column measurements. Nature. 2014;512:65–68. doi: 10.1038/nature13563. PubMed DOI

Cho U.H., Park J.O. Mercury-induced oxidative stress in tomato seedlings. Plant Sci. 2000;156:1–9. doi: 10.1016/S0168-9452(00)00227-2. PubMed DOI

Israr M., Sahi S., Datta R., Sarkar D. Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere. 2006;65:591–598. doi: 10.1016/j.chemosphere.2006.02.016. PubMed DOI

Lomonte C., Doronila A.I., Gregory D., Baker A.J.M., Kolev S.D. Phytotoxicity of biosolids and screening of selected plant species with potential for mercury phytoextraction. J. Hazard. Mater. 2010;173:494–501. doi: 10.1016/j.jhazmat.2009.08.112. PubMed DOI

Beauvais-Flück R., Slaveykova V., Cosio C. Molecular Effects of Inorganic and Methyl Mercury in Aquatic Primary Producers: Comparing Impact to a Macrophyte and a Green Microalga in Controlled Conditions. Geosciences. 2018;8:393. doi: 10.3390/geosciences8110393. DOI

Bodaly R.A., Jansen W.A., Majewski A.R., Fudge R.J.P., Strange N.E., Derksen A.J., Green D.J. Postimpoundment time course of increased mercury concentrations in fish in hydroelectric reservoirs of northern Manitoba, Canada. Arch. Environ. Contam. Toxicol. 2007;53:379–389. doi: 10.1007/s00244-006-0113-4. PubMed DOI

Elbaz A., Wei Y.Y., Meng Q., Zheng Q., Yang Z.M. Mercury-induced oxidative stress and impact on antioxidant enzymes in Chlamydomonas reinhardtii. Ecotoxicology. 2010;19:1285–1293. doi: 10.1007/s10646-010-0514-z. PubMed DOI

Kamal M., Ghaly A.E., Mahmoud N., CoteCôté R. Phytoaccumulation of heavy metals by aquatic plants. Environ. Int. 2004;29:1029–1039. doi: 10.1016/S0160-4120(03)00091-6. PubMed DOI

Narula P., Mahajan A., Gurnani C., Kumar V., Mukhija S. Microalgae as an indispensable tool against heavy metals toxicity to plants: A review. Int. J. Pharm. Sci. Rev. Res. 2015;31:86–93.

He S., Yang X., He Z., Baligar V.C. Morphological and Physiological Responses of Plants to Cadmium Toxicity: A Review. Pedosphere. 2017;27:421–438. doi: 10.1016/S1002-0160(17)60339-4. DOI

Azevedo R., Rodriguez E. Phytotoxicity of Mercury in Plants: A Review. J. Bot. 2012;2012:1–6. doi: 10.1155/2012/848614. DOI

Chen J., Yang Z.M. Mercury toxicity, molecular response and tolerance in higher plants. BioMetals. 2012;25:847–857. doi: 10.1007/s10534-012-9560-8. PubMed DOI

Apel K., Hirt H. Reactive Oxygen Species: Metabolism, Oxidative Stress, and Signal Transduction. Annu. Rev. Plant Biol. 2004;55:373–399. doi: 10.1146/annurev.arplant.55.031903.141701. PubMed DOI

Gupta D.K., Pena L.B., Romero-Puertas M.C., Hernández A., Inouhe M., Sandalio L.M. NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity. Plant Cell Environ. 2017;40:509–526. doi: 10.1111/pce.12711. PubMed DOI

Del Río L.A. ROS and RNS in plant physiology: An overview. J. Exp. Bot. 2015;66:2827–2837. doi: 10.1093/jxb/erv099. PubMed DOI

Martins L.L., Mourato M.P., Cardoso A.I., Pinto A.P., Mota A.M., Maria M.L., de Varennes A., de Lurdes S., Gonçalves M., de Varennes A. Oxidative stress induced by cadmium in Nicotiana tabacum L.: Effects on growth parameters, oxidative damage and antioxidant responses in different plant parts. Acta Physiol. Plant. 2011;33:1375–1383. doi: 10.1007/s11738-010-0671-y. DOI

Sytar O., Kumar A., Latowski D., Kuczynska P., Strzałka K., Prasad M.N.V. Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol. Plant. 2013;35:985–999. doi: 10.1007/s11738-012-1169-6. DOI

Gupta D.K., Palma J.M., Corpas F.J. Reactive Oxygen Species and Oxidative Damage in Plants under Stress. Springer International Publishing; Cham, Switzerland: 2015.

De Michele R., Vurro E., Rigo C., Costa A., Elviri L., Di Valentin M., Careri M., Zottini M., Sanita di Toppi L., Lo Schiavo F. Nitric Oxide Is Involved in Cadmium-Induced Programmed Cell Death in Arabidopsis Suspension Cultures. Plant Physiol. 2009;150:217–228. doi: 10.1104/pp.108.133397. PubMed DOI PMC

Chen J., Shiyab S., Han F.X., Monts D.L., Waggoner C.A., Yang Z., Su Y. Bioaccumulation and physiological effects of mercury in Pteris vittata and Nephrolepis exaltata. Ecotoxicology. 2009;18:110. doi: 10.1007/s10646-008-0264-3. PubMed DOI

Ortega-Villasante C., Rellán-Álvarez R., Del Campo F.F., Carpena-Ruiz R.O., Hernández L.E. Cellular damage induced by cadmium and mercury in Medicago sativa. J. Exp. Bot. 2005;56:2239–2251. doi: 10.1093/jxb/eri223. PubMed DOI

Ortega-Villasante C., Hernández L.E., Rellán-Álvarez R., Del Campo F.F., Carpena-Ruiz R.O. Rapid alteration of cellular redox homeostasis upon exposure to cadmium and mercury in alfalfa seedlings. New Phytol. 2007;176:96–107. doi: 10.1111/j.1469-8137.2007.02162.x. PubMed DOI

Zhou Z.S., Wang S.J., Yang Z.M. Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere. 2008;70:1500–1509. doi: 10.1016/j.chemosphere.2007.08.028. PubMed DOI

Zhou Z.S., Huang S.Q., Guo K., Mehta S.K., Zhang P.C., Yang Z.M. Metabolic adaptations to mercury-induced oxidative stress in roots of Medicago sativa L. J. Inorg. Biochem. 2007;101:1–9. doi: 10.1016/j.jinorgbio.2006.05.011. PubMed DOI

Kováčik J., Rotková G., Bujdoš M., Babula P., Peterková V., Matúš P. Ascorbic acid protects Coccomyxa subellipsoidea against metal toxicity through modulation of ROS/NO balance and metal uptake. J. Hazard. Mater. 2017;339:200–207. doi: 10.1016/j.jhazmat.2017.06.035. PubMed DOI

Rellán-Álvarez R., Ortega-Villasante C., Álvarez-Fernández A., del Campo F.F., Hernández L.E. Stress Responses of Zea mays to Cadmium and Mercury. Plant Soil. 2006;279:41–50. doi: 10.1007/s11104-005-3900-1. DOI

DellaGreca M., Pinto G., Pollio A., Previtera L., Temussi F. Biotransformation of sinapic acid by the green algae Stichococcus bacillaris 155LTAP and Ankistrodesmus braunii C202.7a. Tetrahedron Lett. 2003;44:2779–2780. doi: 10.1016/S0040-4039(03)00458-1. DOI

Kirso U., Irha N. Role of algae in fate of carcinogenic polycyclic aromatic hydrocarbons in the aquatic environment. Ecotoxicol. Environ. Saf. 1998;41:83–89. doi: 10.1006/eesa.1998.1671. PubMed DOI

Pflugmacher S., Wiencke C., Sandermann H. Activity of phase I and phase II detoxication enzymes in Antarctic and Arctic macroalgae. Mar. Environ. Res. 1999;48:23–36. doi: 10.1016/S0141-1136(99)00030-6. DOI

Thies F., Grimme L.H. In vivo O-dealkylation of resorufin and coumarin ethers by the green alga Chlorella fusca analysed by a rapid and sensitive high-performance liquid chromatographic assay. J. Chromatogr. A. 1994;684:168–173. doi: 10.1016/S0021-9673(94)89143-5. DOI

Warshawsky D., Cody T., Radike M., Reilman R., Schumann B., LaDow K., Schneider J. Biotransformation of benzo[a]pyrene and other polycyclic aromatic hydrocarbons and heterocyclic analogs by several green algae and other algal species under gold and white light. Chem. Biol. Interact. 1995;97:131–148. doi: 10.1016/0009-2797(95)03610-X. PubMed DOI

Barque J.P., Abahamid A., Flinois J.P., Beaune P., Bonaly J. Constitutive overexpression of immunoidentical forms of PCP-induced Euglena gracilis CYP-450. Biochem. Biophys. Res. Commun. 2002;298:277–281. doi: 10.1016/S0006-291X(02)02439-7. PubMed DOI

Pflugmacher S., Sandermann H. Cytochrome P450 Monooxygenases for Fatty Acids and Xenobiotics in Marine Macroalgae. Plant Physiol. 1998;117:123–128. doi: 10.1104/pp.117.1.123. PubMed DOI PMC

Thies F., Backhaus T., Bossmann B., Grimme L.H. Xenobiotic Biotransformation in Unicellular Green Algae (Involvement of Cytochrome P450 in the Activation and Selectivity of the Pyridazinone Pro-Herbicide Metflurazon) Plant Physiol. 1996;112:361–370. doi: 10.1104/pp.112.1.361. PubMed DOI PMC

Zangar R.C., Davydov D.R., Verma S. Mechanisms that regulate production of reactive oxygen species by cytochrome P450. Toxicol. Appl. Pharmacol. 2004;199:316–331. doi: 10.1016/j.taap.2004.01.018. PubMed DOI

Pflugmacher S., Schröder P., Sandermann H. Taxonomic distribution of plant glutathione S-transferases acting on xenobiotics. Phytochemistry. 2000;54:267–273. doi: 10.1016/S0031-9422(00)00116-3. PubMed DOI

Reilman R., Keenan T.H., Cody T.E., Radike M.J., Warshawsky D. Conjugation of benzo[a]pyrene metabolites by freshwater green alga Selenastrum capricornutum. Chem. Biol. Interact. 1990;74:93–105. PubMed

Sandermann H. Molecular ecotoxicology of plants. Trends Plant Sci. 2004;9:406–413. doi: 10.1016/j.tplants.2004.06.001. PubMed DOI

Avery S.V., Codd G.A., Gadd G.M. Characterisation of caesium transport in the microalga Chlorella salina. Biochem. Soc. Trans. 1995;23:468S. doi: 10.1042/bst023468s. PubMed DOI

Avilés C., Torres-Márquez M.E., Mendoza-Cózatl D., Moreno-Sánchez R. Time-course development of the Cd2+ hyper-accumulating phenotype in Euglena gracilis. Arch. Microbiol. 2005;184:83–92. doi: 10.1007/s00203-005-0013-4. PubMed DOI

Jabusch T.W., Swackhamer D.L. Subcellular accumulation of polychlorinated biphenyls in the green alga Chlamydomonas reinhardtii. Environ. Toxicol. Chem. 2004;23:2823–2830. doi: 10.1897/03-431.1. PubMed DOI

Smital T., Sauerborn R., Hackenberger B.K. Inducibility of the P-glycoprotein transport activity in the marine mussel Mytilus galloprovincialis and the freshwater mussel Dreissena polymorpha. Aquat. Toxicol. 2003;65:443–465. doi: 10.1016/S0166-445X(03)00175-9. PubMed DOI

Torres M.A., Barros M.P., Campos S.C.G., Pinto E., Rajamani S., Sayre R.T., Colepicolo P. Biochemical biomarkers in algae and marine pollution: A review. Ecotoxicol. Environ. Saf. 2008;71:1–15. doi: 10.1016/j.ecoenv.2008.05.009. PubMed DOI

You J., Chan Z. ROS Regulation during Abiotic Stress Responses in Crop Plants. Front. Plant Sci. 2015;6:1092. doi: 10.3389/fpls.2015.01092. PubMed DOI PMC

Jalmi S.K., Bhagat P.K., Verma D., Noryang S., Tayyeba S., Singh K., Sharma D., Sinha A.K. Traversing the Links between Heavy Metal Stress and Plant Signaling. Front. Plant Sci. 2018;9:12. doi: 10.3389/fpls.2018.00012. PubMed DOI PMC

Wang Y., Gao C., Liang Y., Wang C., Yang C., Liu G. A novel bZIP gene from Tamarix hispida mediates physiological responses to salt stress in tobacco plants. J. Plant Physiol. 2010;167:222–230. doi: 10.1016/j.jplph.2009.09.008. PubMed DOI

Hong C., Cheng D., Zhang G., Zhu D., Chen Y., Tan M. The role of ZmWRKY4 in regulating maize antioxidant defense under cadmium stress. Biochem. Biophys. Res. Commun. 2017;482:1504–1510. doi: 10.1016/j.bbrc.2016.12.064. PubMed DOI

Moore R.B., Oborník M., Janouškovec J., Chrudimský T., Vancová M., Green D.H., Wright S.W., Davies N.W., Bolch C.J.S., Heimann K., et al. A photosynthetic alveolate closely related to apicomplexan parasites. Nature. 2008;451:959–963. doi: 10.1038/nature06635. PubMed DOI

Oborník M., Vancová M., Lai D.H., Janouškovec J., Keeling P.J., Lukeš J. Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of apicomplexa, Chromera velia. Protist. 2011;162:115–130. doi: 10.1016/j.protis.2010.02.004. PubMed DOI

Vazač J., Füssy Z., Hladová I., Killi S., Oborník M. Ploidy and Number of Chromosomes in the Alveolate Alga Chromera velia. Protist. 2018;169:53–63. doi: 10.1016/j.protis.2017.12.001. PubMed DOI

Kotabová E., Jarešová J., Kaňa R., Sobotka R., Bína D., Prášil O. Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems. Biochim. Biophys. Acta Bioenerg. 2014;1837:734–743. doi: 10.1016/j.bbabio.2014.01.012. PubMed DOI

Mann M., Hoppenz P., Jakob T., Weisheit W., Mittag M., Wilhelm C., Goss R. Unusual features of the high light acclimation of Chromera velia. Photosynth. Res. 2014;122:159–169. doi: 10.1007/s11120-014-0019-3. PubMed DOI

Quigg A., Kotabová E., Jarešová J., Kaňa R., Šetlík J., Šedivá B., Komárek O., Prášil O. Photosynthesis in Chromera velia Represents a Simple System with High Efficiency. PLoS ONE. 2012;7:e47036. doi: 10.1371/journal.pone.0047036. PubMed DOI PMC

Sobotka R., Esson H.J., Koník P., Trsková E., Moravcová L., Horák A., Dufková P., Oborník M. Extensive gain and loss of photosystem I subunits in chromerid algae, photosynthetic relatives of apicomplexans. Sci. Rep. 2017;7:13214. doi: 10.1038/s41598-017-13575-x. PubMed DOI PMC

Liu M.M., Xing Y.M., Zhang D.W., Guo S.X. Transcriptome analysis of genes involved in defence response in Polyporus umbellatus with Armillaria mellea infection. Sci. Rep. 2015;5:16075. doi: 10.1038/srep16075. PubMed DOI PMC

Dittami S.M., Scornet D., Petit J.-L.L., Ségurens B., Da Silva C., Corre E., Dondrup M., Glatting K.-H.H., König R., Sterck L., et al. Global expression analysis of the brown alga Ectocarpus siliculosus (Phaeophyceae) reveals large-scale reprogramming of the transcriptome in response to abiotic stress. Genome Biol. 2009;10:R66. doi: 10.1186/gb-2009-10-6-r66. PubMed DOI PMC

Holzinger A., Pichrtová M. Abiotic Stress Tolerance of Charophyte Green Algae: New Challenges for Omics Techniques. Front. Plant Sci. 2016;7:678. doi: 10.3389/fpls.2016.00678. PubMed DOI PMC

Khraiwesh B., Qudeimat E., Thimma M., Chaiboonchoe A., Jijakli K., Alzahmi A., Arnoux M., Salehi-Ashtiani K. Genome-wide expression analysis offers new insights into the origin and evolution of Physcomitrella patens stress response. Sci. Rep. 2015;5:17434. doi: 10.1038/srep17434. PubMed DOI PMC

Matthijs M., Fabris M., Broos S., Vyverman W., Goossens A. Profiling of the Early Nitrogen Stress Response in the Diatom Phaeodactylum tricornutum Reveals a Novel Family of RING-Domain Transcription Factors. Plant Physiol. 2016;170:489–498. doi: 10.1104/pp.15.01300. PubMed DOI PMC

De Michele R., Formentin E., Todesco M., Toppo S., Carimi F., Zottini M., Barizza E., Ferrarini A., Delledonne M., Fontana P., et al. Transcriptome analysis of Medicago truncatula leaf senescence: Similarities and differences in metabolic and transcriptional regulations as compared with Arabidopsis, nodule senescence and nitric oxide signalling. New Phytol. 2009;181:563–575. doi: 10.1111/j.1469-8137.2008.02684.x. PubMed DOI

Wintermans J.F.G.M., De Mots A. Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochim. Biophys. Acta Biophys. Incl. Photosynth. 1965;109:448–453. doi: 10.1016/0926-6585(65)90170-6. PubMed DOI

Chen X., Zhong Z., Xu Z., Chen L., Wang Y. 2′,7′-Dichlorodihydrofluorescein as a fluorescent probe for reactive oxygen species measurement: Forty years of application and controversy. Free Radic. Res. 2010;44:587–604. doi: 10.3109/10715761003709802. PubMed DOI

Nazarewicz R.R., Bikineyeva A., Dikalov S.I. Rapid and Specific Measurements of Superoxide Using Fluorescence Spectroscopy. J. Biomol. Screen. 2013;18:498–503. doi: 10.1177/1087057112468765. PubMed DOI PMC

Kojima H., Urano Y., Kikuchi K., Higuchi T., Hirata Y., Nagano T. Fluorescent Indicators for Imaging Nitric Oxide Production. Angew. Chem. Int. Ed. 1999;38:3209–3212. doi: 10.1002/(SICI)1521-3773(19991102)38:21<3209::AID-ANIE3209>3.0.CO;2-6. PubMed DOI

Setsukinai K., Urano Y., Kakinuma K., Majima H.J., Nagano T. Development of Novel Fluorescence Probes That Can Reliably Detect Reactive Oxygen Species and Distinguish Specific Species. J. Biol. Chem. 2003;278:3170–3175. doi: 10.1074/jbc.M209264200. PubMed DOI

Bellincampi D., Dipierro N., Salvi G., Cervone F., De Lorenzo G. Extracellular H(2)O(2) induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol. 2000;122:1379–1386. doi: 10.1104/pp.122.4.1379. PubMed DOI PMC

Hu L., Li H., Chen L., Lou Y., Amombo E., Fu J. RNA-seq for gene identification and transcript profiling in relation to root growth of bermudagrass (Cynodon dactylon) under salinity stress. BMC Genom. 2015;16:575. doi: 10.1186/s12864-015-1799-3. PubMed DOI PMC

Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q., et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011;299:644. doi: 10.1038/nbt.1883. PubMed DOI PMC

Bryant D.M., Johnson K., DiTommaso T., Tickle T., Couger M.B., Payzin-Dogru D., Lee T.J., Leigh N.D., Kuo T.-H., Davis F.G., et al. A Tissue-Mapped Axolotl De Novo Transcriptome Enables Identification of Limb Regeneration Factors. Cell Rep. 2017;18:762–776. doi: 10.1016/j.celrep.2016.12.063. PubMed DOI PMC

Supek F., Bošnjak M., Škunca N., Šmuc T. REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms. PLoS ONE. 2011;6:e21800. doi: 10.1371/journal.pone.0021800. PubMed DOI PMC

Li B., Dewey C.N. RSEM: Accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinfor. 2014;12:323 PubMed PMC

McCarthy D.J., Chen Y., Smyth G.K. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 2012;40:4288–4297. doi: 10.1093/nar/gks042. PubMed DOI PMC

Boratyn G.M., Schäffer A.A., Agarwala R., Altschul S.F., Lipman D.J., Madden T.L. Domain enhanced lookup time accelerated BLAST. Biol. Direct. 2012;7:12. doi: 10.1186/1745-6150-7-12. PubMed DOI PMC

Woo Y.H., Ansari H., Otto T.D., Linger C.M.K., Olisko M.K., Michálek J., Saxena A., Shanmugam D., Tayyrov A., Veluchamy A., et al. Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. Elife. 2015;4:1–41. doi: 10.7554/eLife.06974. PubMed DOI PMC

Nordberg H., Cantor M., Dusheyko S., Hua S., Poliakov A., Shabalov I., Smirnova T., Grigoriev I.V., Dubchak I. The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res. 2014;42:D26–D31. doi: 10.1093/nar/gkt1069. PubMed DOI PMC

Bendtsen J.D., Nielsen H., Von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004;340:783–795. doi: 10.1016/j.jmb.2004.05.028. PubMed DOI

Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods. 2011;8:785–786. doi: 10.1038/nmeth.1701. PubMed DOI

Gruber A., Rocap G., Kroth P.G., Armbrust E.V., Mock T. Plastid proteome prediction for diatoms and other algae with secondary plastids of the red lineage. Plant J. 2015;81:519–528. doi: 10.1111/tpj.12734. PubMed DOI PMC

Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007;2:953–971. doi: 10.1038/nprot.2007.131. PubMed DOI

Bannai H., Tamada Y., Maruyama O., Nakai K., Miyano S. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics. 2002;18:298–305. doi: 10.1093/bioinformatics/18.2.298. PubMed DOI

Horton P., Park K.J., Obayashi T., Fujita N., Harada H., Adams-Collier C.J., Nakai K. WoLF PSORT: Protein localization predictor. Nucleic Acids Res. 2007;35:W585–W587. doi: 10.1093/nar/gkm259. PubMed DOI PMC

Claros M.G., Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 1996;241:779–786. doi: 10.1111/j.1432-1033.1996.00779.x. PubMed DOI

Almagro Armenteros J.J., Sønderby C.K., Sønderby S.K., Nielsen H., Winther O. DeepLoc: Prediction of protein subcellular localization using deep learning. Bioinformatics. 2017;33:3387–3395. doi: 10.1093/bioinformatics/btx431. PubMed DOI

Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

de Juan D., Pazos F., Valencia A., Evaluation P.M., Rehbein P., Schwalbe H., Jones D.T., Buchan D.W.A., Cozzetto D., Pontil M., et al. ProtTest: Selection of best-fit models of protein evolution. Bioinformatics. 2015;21:2104–2105. PubMed

Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Nguyen L.-T., Schmidt H.A., von Haeseler A., Minh B.Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Mol. Biol. Evol. 2015;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC

Nowicka B., Pluciński B., Kuczyńska P., Kruk J. Physiological characterization of Chlamydomonas reinhardtii acclimated to chronic stress induced by Ag, Cd, Cr, Cu and Hg ions. Ecotoxicol. Environ. Saf. 2016;130:133–145. doi: 10.1016/j.ecoenv.2016.04.010. PubMed DOI

Cargnelutti D., Tabaldi L.A., Spanevello R.M., de Oliveira Jucoski G., Battisti V., Redin M., Linares C.E.B., Dressler V.L., de Moraes Flores É.M., Nicoloso F.T., et al. Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere. 2006;65:999–1006. doi: 10.1016/j.chemosphere.2006.03.037. PubMed DOI

Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden markov model: Application to complete genomes11Edited by F. Cohen. J. Mol. Biol. 2001;305:567–580. doi: 10.1006/jmbi.2000.4315. PubMed DOI

Pinto E., Sigaud-kutner T.C.S., Leitao M.A.S., Okamoto O.K., Morse D., Colepicolo P. HEAVY METAL-INDUCED OXIDATIVE STRESS IN ALGAE1. J. Phycol. 2003;39:1008–1018. doi: 10.1111/j.0022-3646.2003.02-193.x. DOI

Sabatini S.E., Juárez Á.B., Eppis M.R., Bianchi L., Luquet C.M., de Molina M.D.C.R. Oxidative stress and antioxidant defenses in two green microalgae exposed to copper. Ecotoxicol. Environ. Saf. 2009;72:1200–1206. doi: 10.1016/j.ecoenv.2009.01.003. PubMed DOI

Guo J.T., Weatherby K., Carter D., Šlapeta J. Effect of nutrient concentration and salinity on immotile-motile transformation of Chromera velia. J. Eukaryot. Microbiol. 2010;57:444–446. doi: 10.1111/j.1550-7408.2010.00495.x. PubMed DOI

Kabeláčová K. The Fitness of Three Strains of the Alga Chromera velia—Salinity and pH. University of South Bohemia; Budejovice, Ceske: 2018.

Perez-Perez M.E., Lemaire S.D., Crespo J.L. Reactive Oxygen Species and Autophagy in Plants and Algae. Plant Physiol. 2012;160:156–164. doi: 10.1104/pp.112.199992. PubMed DOI PMC

Shanura Fernando I.P., Asanka Sanjeewa K.K., Samarakoon K.W., Lee W.W., Kim H.S., Kim E.A., Gunasekara U.K., Abeytunga D.T.U., Nanayakkara C., De Silva E.D., et al. FTIR characterization and antioxidant activity of water soluble crude polysaccharides of Sri Lankan marine algae. Algae. 2017;32:75–86. doi: 10.4490/algae.2017.32.12.1. DOI

Fan Y., Bose J., Zhou M., Shabala S. ROS Production, Scavenging, and Signaling under Salinity Stress. In: Wani S.H., Hossain M.A., editors. Managing Salt Tolerance in Plants. CRC Press; Boca Raton, FL, USA: 2015.

Gratão P.L., Monteiro C.C., Tezotto T., Carvalho R.F., Alves L.R., Peters L.P., Azevedo R.A. Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants. BioMetals. 2015;28:803–816. doi: 10.1007/s10534-015-9867-3. PubMed DOI

Shahabivand S., Zare Maivan H., Mahmoudi E., Soltani B.M., Sharifi M., Aliloo A.A. Antioxidant activity and gene expression associated with cadmium toxicity in wheat affected by mycorrhizal fungus. Zemdirb. Agric. 2016;103:53–60. doi: 10.13080/z-a.2016.103.007. DOI

Cassier-Chauvat C., Chauvat F. Responses to oxidative and heavy metal stresses in cyanobacteria: Recent advances. Int. J. Mol. Sci. 2015;16:871–886. doi: 10.3390/ijms16010871. PubMed DOI PMC

Narainsamy K., Marteyn B., Sakr S., Cassier-Chauvat C., Chauvat F. Genomics of the Pleïotropic Glutathione System in Cyanobacteria. Adv. Bot. Res. 2013;65:157–188.

Ken C.F., Hsiung T.M., Huang Z.X., Juang R.H., Lin C.T. Characterization of Fe/Mn-superoxide dismutase from diatom Thallassiosira weissflogii: Cloning, expression, and property. J. Agric. Food Chem. 2005;53:1470–1474. doi: 10.1021/jf048269f. PubMed DOI

Fridovich I. Superoxide anion radical (O 2), superoxide dismutases, and related matters. J. Biol. Chem. 1997;272:18515–18517. doi: 10.1074/jbc.272.30.18515. PubMed DOI

Okamoto O.K., Robertson D.L., Fagan T.F., Hastings J.W., Colepicolo P. Different Regulatory Mechanisms Modulate the Expression of a Dinoflagellate Iron-Superoxide Dismutase. J. Biol. Chem. 2001;276:19989–19993. doi: 10.1074/jbc.M101169200. PubMed DOI

Barros M.P., Pinto E., Sigaud-Kutner T.C.S., Cardozo K.H.M., Colepicolo P. Rhythmicity and oxidative/nitrosative stress in algae. Biol. Rhythm Res. 2005;36:67–82. doi: 10.1080/09291010400028666. DOI

Murthy K.N.C., Vanitha A., Rajesha J., Swamy M.M., Sowmya P.R., Ravishankar G.A. In vivo antioxidant activity of carotenoids from Dunaliella salina—A green microalga. Life Sci. 2005;76:1381–1390. doi: 10.1016/j.lfs.2004.10.015. PubMed DOI

Tripathi B.N., Mehta S.K., Amar A., Gaur J.P. Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu2+ and Zn2+ Chemosphere. 2006;62:538–544. doi: 10.1016/j.chemosphere.2005.06.031. PubMed DOI

Yamada Y., Fujiwara T., Sato T., Igarashi N., Tanaka N. The 2.0 å crystal structure of catalase-peroxidase from haloarcula marismortui. Nat. Struct. Biol. 2002;9:691. doi: 10.1038/nsb834. PubMed DOI

Welinder K.G. Superfamily of plant, fungal and bacterial peroxidases. Curr. Opin. Struct. Biol. 1992;2:388–393. doi: 10.1016/0959-440X(92)90230-5. DOI

Passardi F., Bakalovic N., Teixeira F.K., Margis-Pinheiro M., Penel C., Dunand C. Prokaryotic origins of the non-animal peroxidase superfamily and organelle-mediated transmission to eukaryotes. Genomics. 2007;89:567–579. doi: 10.1016/j.ygeno.2007.01.006. PubMed DOI

Klotz M.G., Loewen P.C. The molecular evolution of catalatic hydroperoxidases: Evidence for multiple lateral transfer of genes between prokaryota and from bacteria into eukaryota. Mol. Biol. Evol. 2003;20:1098–1112. doi: 10.1093/molbev/msg129. PubMed DOI

Yu R., Tang Y., Liu C., Du X., Miao C., Shi G. Comparative transcriptomic analysis reveals the roles of ROS scavenging genes in response to cadmium in two pak choi cultivars. Sci. Rep. 2017;7:9217. doi: 10.1038/s41598-017-09838-2. PubMed DOI PMC

Zang X., Geng X., Wang F., Liu Z., Zhang L., Zhao Y., Tian X., Ni Z., Yao Y., Xin M., et al. Overexpression of wheat ferritin gene TaFER-5B enhances tolerance to heat stress and other abiotic stresses associated with the ROS scavenging. BMC Plant Biol. 2017;17:14. doi: 10.1186/s12870-016-0958-2. PubMed DOI PMC

Zok A., Oláh R., Hideg É., Horváth V.G., Kós P.B., Majer P., Váradi G., Szegedi E. Effect of Medicago sativa ferritin gene on stress tolerance in transgenic grapevine. Plant Cell. Tissue Organ Cult. 2010;100:339–344. doi: 10.1007/s11240-009-9641-8. DOI

Hannemann F., Bichet A., Ewen K.M., Bernhardt R. Cytochrome P450 systems-biological variations of electron transport chains. Biochim. Biophys. Acta Gen. Subj. 2007;1770:330–344. doi: 10.1016/j.bbagen.2006.07.017. PubMed DOI

Kelly S.L., Kelly D.E. Microbial cytochromes P450: Biodiversity and biotechnology. Where do cytochromes P450 come from, what do they do and what can they do for us? Philos. Trans. R. Soc. B Biol. Sci. 2013;368:20120476. doi: 10.1098/rstb.2012.0476. PubMed DOI PMC

Schenkman J.B., Jansson I. The many roles of cytochrome b5. Pharmacol. Ther. 2003;97:139–152. doi: 10.1016/S0163-7258(02)00327-3. PubMed DOI

Kandel S.E., Lampe J.N. Role of Protein–Protein Interactions in Cytochrome P450-Mediated Drug Metabolism and Toxicity. Chem. Res. Toxicol. 2014;27:1474–1486. doi: 10.1021/tx500203s. PubMed DOI PMC

Jamakhandi A.P., Kuzmic P., Sanders D.E., Miller G.P. Global Analysis of Protein−Protein Interactions Reveals Multiple CYP2E1−Reductase Complexes †. Biochemistry. 2007;46:10192–10201. doi: 10.1021/bi7003476. PubMed DOI PMC

Lane T.S., Rempe C.S., Davitt J., Staton M.E., Peng Y., Soltis D.E., Melkonian M., Deyholos M., Leebens-Mack J.H., Chase M., et al. Diversity of ABC transporter genes across the plant kingdom and their potential utility in biotechnology. BMC Biotechnol. 2016;16:47. doi: 10.1186/s12896-016-0277-6. PubMed DOI PMC

Ben Chekroun K., Baghour M. The role of algae in phytoremediation of heavy metals: A review. J. Mater. Environ. Sci. 2013;4:873–880.

Hossain M.A., Piyatida P., da Silva J.A.T., Fujita M. Molecular Mechanism of Heavy Metal Toxicity and Tolerance in Plants: Central Role of Glutathione in Detoxification of Reactive Oxygen Species and Methylglyoxal and in Heavy Metal Chelation. J. Bot. 2012;2012:37. doi: 10.1155/2012/872875. DOI

Yamuna A., Kabila V., Geraldine P. Expression of heat shock protein 70 in freshwater prawn Macrobrachium malcolmsonii (H. Milne Edwards) following exposure to Hg and Cu. Indian J. Exp. Biol. 2000;38:921–925. PubMed

Wei Y.Y., Zheng Q., Liu Z.P., Yang Z.M. Regulation of tolerance of chlamydomonas reinhardtii to heavy metal toxicity by heme oxygenase-1 and carbon monoxide. Plant Cell Physiol. 2011;52:1665–1675. doi: 10.1093/pcp/pcr102. PubMed DOI

Sanità Di Toppi L., Prasad M.N.V., Ottonello S. Metal Chelating Peptides and Proteins in Plants. In: Prasad M.N.V., editor. Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants. Springer; Dordrecht, The Netherlands: 2002. pp. 59–93.

Zémocký M. Phylogenetic relationships in class I of the superfamily of bacterial, fungal, and plant peroxidases. Eur. J. Biochem. 2004;271:3297–3309. doi: 10.1111/j.1432-1033.2004.04262.x. PubMed DOI

Theologis A., Ecker J.R., Palm C.J., Federspiel N.A., Kaul S., White O., Alonso J., Altafi H., Araujo R., Bowman C.L., et al. Sequence and analysis of chromosome 1 of the plant Arabidopsis thaliana. Nature. 2000;408:816–820. doi: 10.1038/35048500. PubMed DOI

Wu H., Chen C., Du J., Liu H., Cui Y., Zhang Y., He Y., Wang Y., Chu C., Feng Z., et al. Co-Overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis-Enhanced Cadmium Tolerance via Increased Cadmium Sequestration in Roots and Improved Iron Homeostasis of Shoots 1. Plant Physiol. 2012;158:790–800. doi: 10.1104/pp.111.190983. PubMed DOI PMC

Yang G., Wang C., Wang Y., Guo Y., Zhao Y., Yang C., Gao C. Overexpression of ThVHAc1 and its potential upstream regulator, ThWRKY7, improved plant tolerance of Cadmium stress. Sci. Rep. 2016;6:18752. doi: 10.1038/srep18752. PubMed DOI PMC

Zhang H., Li A., Zhang Z., Huang Z., Lu P., Zhang D., Liu X., Zhang Z.F., Huang R. Ethylene Response Factor TERF1, Regulated by ETHYLENE-INSENSITIVE3-like Factors, Functions in Reactive Oxygen Species (ROS) Scavenging in Tobacco (Nicotiana tabacum L.) Sci. Rep. 2016;6:29948. doi: 10.1038/srep29948. PubMed DOI PMC

Yadav N.R., Taunk J., Rani A., Aneja B., Yadav R.C. Role of Transcription Factors in Abiotic Stress Tolerance in Crop Plants. In: Tuteja N., Gill S.S., editors. Climate Change and Plant Abiotic Stress Tolerance. Wiley-VCH GmbH & Co. KGaA; Weinheim, Germany: 2013. pp. 605–640.

Moustafa A., Beszteri B., Maier U.G., Bowler C., Valentin K., Bhattacharya D. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science. 2009;324:1724–1726. doi: 10.1126/science.1172983. PubMed DOI

Thiriet-Rupert S., Carrier G., Chénais B., Trottier C., Bougaran G., Cadoret J.P., Schoefs B., Saint-Jean B. Transcription factors in microalgae: Genome-wide prediction and comparative analysis. BMC Genom. 2016;17:282. doi: 10.1186/s12864-016-2610-9. PubMed DOI PMC

Ritter A., Dittami S.M., Goulitquer S., Correa J.A., Boyen C., Potin P., Tonon T. Transcriptomic and metabolomic analysis of copper stress acclimation in Ectocarpus siliculosus highlights signaling and tolerance mechanisms in brown algae. BMC Plant Biol. 2014;14:116. doi: 10.1186/1471-2229-14-116. PubMed DOI PMC

Lu D., Wang T., Persson S., Mueller-Roeber B., Schippers J.H.M. Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nat. Commun. 2014;5:3767. doi: 10.1038/ncomms4767. PubMed DOI PMC

Fan S., Dong L., Han D., Zhang F., Wu J., Jiang L., Cheng Q., Li R., Lu W., Meng F., et al. GmWRKY31 and GmHDL56 Enhances Resistance to Phytophthora sojae by Regulating Defense-Related Gene Expression in Soybean. Front. Plant Sci. 2017;8:781. doi: 10.3389/fpls.2017.00781. PubMed DOI PMC

Sewelam N., Kazan K., Thomas-Hall S.R., Kidd B.N., Manners J.M., Schenk P.M. Ethylene Response Factor 6 Is a Regulator of Reactive Oxygen Species Signaling in Arabidopsis. PLoS ONE. 2013;8:e70289. doi: 10.1371/journal.pone.0070289. PubMed DOI PMC

Chen J., Yang L., Yan X., Liu Y., Wang R., Fan T., Ren Y., Tang X., Xiao F., Liu Y., et al. Zinc-Finger Transcription Factor ZAT6 Positively Regulates Cadmium Tolerance through Glutathione-dependent Pathway in Arabidopsis. Plant Physiol. 2016;171:707–719. doi: 10.1104/pp.15.01882. PubMed DOI PMC

Li X.D., Zhuang K.Y., Liu Z.M., Yang D.Y., Ma N.N., Meng Q.W. Overexpression of a novel NAC-type tomato transcription factor, SlNAM1, enhances the chilling stress tolerance of transgenic tobacco. J. Plant Physiol. 2016;204:54–65. doi: 10.1016/j.jplph.2016.06.024. PubMed DOI

Xue G.P., Way H.M., Richardson T., Drenth J., Joyce P.A., McIntyre C.L. Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol. Plant. 2011;4:697–712. doi: 10.1093/mp/ssr013. PubMed DOI

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