Transcriptomic Analysis Reveals the Roles of Detoxification Systems in Response to Mercury in Chromera velia
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31653042
PubMed Central
PMC6920818
DOI
10.3390/biom9110647
PII: biom9110647
Knihovny.cz E-zdroje
- Klíčová slova
- antioxidant enzymes, chromerids, heavy metal, phylogenies, reactive nitrogen species, reactive oxygen species, transcriptome, xenobiotics,
- MeSH
- Alveolata účinky léků genetika růst a vývoj metabolismus MeSH
- chemické látky znečišťující vodu toxicita MeSH
- chlorofyl metabolismus MeSH
- peroxid vodíku metabolismus MeSH
- reaktivní formy dusíku metabolismus MeSH
- reaktivní formy kyslíku metabolismus MeSH
- rtuť toxicita MeSH
- transkriptom účinky léků MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- chemické látky znečišťující vodu MeSH
- chlorofyl MeSH
- peroxid vodíku MeSH
- reaktivní formy dusíku MeSH
- reaktivní formy kyslíku MeSH
- rtuť MeSH
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.
Faculty of Science University of South Bohemia 37005 České Budějovice Czech Republic
Genetic Department Faculty of Agriculture Ain Shams University Cairo 11241 Egypt
Institute of Biosciences and Bioresources of Italy 90129 Palermo Italy
Zobrazit více v PubMed
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