Cadmium Stress Reprograms ROS/RNS Homeostasis in Phytophthora infestans (Mont.) de Bary
Abstract
:1. Introduction
2. Results
2.1. Cadmium Stress Affects P. infestans in Vitro Growth and Sporulation
2.2. Cadmium Exposure Provokes Reactive Oxygen and Nitrogen Species Formation in P. infestans Structures
2.3. Cadmium Affects the Nitro-Oxidative Pattern of Nucleic Acids and Proteins
2.4. Cadmium Accelerates P. infestans Antioxidative Response
2.5. Moderate Cadmium Stress Amplifies P. infestans Pathogenicity on Potato
3. Discussion
4. Materials and Methods
4.1. Pathogen Culture
4.2. Plant Material
4.3. Assessment of the Area under Disease Progress
4.4. Cadmium Stress, Hyphal Growth, and Sporulation of P. infestans
4.5. Superoxide Radical Production
4.6. Hydrogen Peroxide Accumulation
4.7. Bio-Imaging of Nitric Oxide
4.8. Peroxynitrite Detection
4.9. Protein 3-Nitrotyrosine Assay
4.10. Protein Carbonylation Assay
4.11. RNA Extraction
4.12. DNA Extraction
4.13. 8-NO2-G Quantification
4.14. Total Antioxidative Capacity
4.15. Superoxide Dismutase Activity
4.16. Catalase Activity
4.17. Gene Expression Measurement
4.18. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Abbreviations
CAT | catalase |
Cd | cadmium |
FW | fresh weight |
NO | nitric oxide |
8-NO2-G | 8-nitroguanine |
ONOO¯ | peroxynitrite |
PCO | carbonylated proteins |
RNS | reactive nitrogen species |
ROS | reactive oxygen species |
SOD | superoxide dismutase |
TAC | total antioxidative capacity |
References
- Candelone, J.P.; Hong, S.; Pellone, C.; Boutron, C.F. Post Industrial Revolution changes in large-scale atmospheric pollution of the northern Hemisphere by heavy metals documented in central Greenland snow and ice. J. Geophys. Res. 1995, 100, 16605–16616. [Google Scholar] [CrossRef]
- Maanan, M.; Saddik, M.; Maanan, M.; Chaibi, M.; Assobhei, O.; Zourarah, B. Environmental and ecological risk assessment of heavy metals in sediments of Nador lagoon, Morocco. Ecol. Indic. 2015, 48, 616–626. [Google Scholar] [CrossRef]
- Wu, Q.; Zhou, H.; Tam, N.F.Y.; Tian, Y.; Tan, Y.; Zhou, S.; Li, Q.; Chen, Y.; Leung, J.Y. Contamination, toxicity and speciation of heavy metals in an industrialized urban river: Implications for the dispersal of heavy metals. Mar. Pollut. Bull. 2016, 104, 153–161. [Google Scholar] [CrossRef] [PubMed]
- Gadd, G.M. Interactions of fungi with toxic metals. In The Genus Aspergillus; Powell, K.A., Renwick, A., Peberdy, J.F., Eds.; FEMS Springer: Boston, MA, USA, 1994; p. 69. [Google Scholar]
- Ali, E.H.; Hashem, M. Removal Efficiency of the heavy metals Zn(II), Pb(II) and Cd(II) by Saprolegnia delica and Trichoderma viride at different pH values and temperature degrees. Mycobiology 2007, 35, 135–144. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gallego, S.M.; Pena, L.B.; Barcia, R.A.; Azpilicueta, C.E.; Iannone, M.F.; Rosales, E.P.; Zawoznik, M.S.; Groppa, M.D.; Benavides, M.P. Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ. Exp. Bot. 2012, 83, 33–46. [Google Scholar] [CrossRef]
- Chmielowska-Bąk, J.; Izbiańska, K.; Ekner-Grzyb, A.; Bayar, M.; Deckert, J. Cadmium stress leads to rapid increase in RNA oxidative modifications in soybean seedlings. Front. Plant Sci. 2018, 8, 2219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rodríguez-Serrano, M.; Romero-Puertas, M.C.; Pazmiño, D.M.; Testillano, P.S.; Risueño, M.C.; Del Río, L.A.; Sandalio, L.M. Cellular response of pea plant to cadmium toxicity: Cross talk between reactive oxygen species, nitric oxide and cadmium. Plant Physiol. 2009, 150, 229–243. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bailey-Serres, J.; Mittler, R. The roles of reactive oxygen species in plant cells. Plant Physiol. 2006, 141, 311. [Google Scholar] [CrossRef] [Green Version]
- Finkel, T. Signal transduction by reactive oxygen species. J. Cell Biol. 2011, 194, 7–15. [Google Scholar] [CrossRef] [Green Version]
- Turkan, I. ROS and RNS: Key signalling molecules in plants. J. Exp. Bot. 2018, 69, 3313–3315. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pauly, N.; Pucciariello, C.; Mandon, K.; Innocenti, G.; Jamet, A.; Baudouin, E.; Hérouart, D.; Fredo, P.; Puppo, A. Reactive oxygen and nitrogen species and glutathione: Key players in the legume—Rhizobium symbiosis. J. Exp. Bot. 2006, 57, 1769–1776. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Q.; Zeng, G.; Chen, G.; Yan, M.; Chen, A.; Du, J.; Huang, J.; Yi, B.; Zhou, Y.; He, X.; et al. The effect of heavy metal-induced oxidative stress on the enzymes in white rot fungus Phanerochaete chrysosporium. Appl. Biochem. Biotechnol. 2015, 175, 1281–1293. [Google Scholar] [CrossRef] [PubMed]
- Englender, C.M.; Corden, M.E. Stimulation of mycelial growth of Endothia parasitica by heavy metals. Appl. Microbiol. 1971, 22, 1012–1016. [Google Scholar] [CrossRef] [Green Version]
- Cuero, R.T.; Ouellet, T.J.; Yu, J.; Mogongwa, N. Metal ion enhancement of fungal growth, gene expression and aflatoxin synthesis in Aspergillus flavus: RT-PCR characterization. J. Appl. Microbiol. 2003, 94, 953–961. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abu-Mejdad, N. Response of some fungal species to the effect of copper, magnesium and zinc under the laboratory condition. Eur. J. Exp. Biol. 2013, 3, 535–540. [Google Scholar]
- Mwangi, E.S.K.; Gatebe, E.G.; Ndung’u, M.W. Effect of selected metal ions on the mycelial growth of Sclerotinia sclerotiorum isolated from soybean field in Rongai, Kenya. IJCMR 2014, 2, 116–125. [Google Scholar]
- Baldrian, P. Interactions of heavy metals with white-rot fungi. Enzym. Microb. Technol. 2003, 32, 78–91. [Google Scholar] [CrossRef]
- Golubović-Ćurguz, V.; Tabaković-Tošić, M.; Veselinović, M.; Rajković, S. The influence of the heavy metals on the growth of pathogenic fungi. For. Ideas 2010, 16, 39. [Google Scholar]
- Ouda, S.M. Antifungal activity of silver and copper nanoparticles on two plant pathogens, Alternaria alternata and Botrytis cinerea. Res. J. Microbiol. 2014, 9, 34–42. [Google Scholar] [CrossRef] [Green Version]
- Sazanova, K.; Osmolovskaya, N.; Schiparev, S.; Yakkonen, K.; Kuchaeva, L.; Vlasov, D. Organic acids induce tolerance to zinc- and copper-exposed fungi under various growth conditions. Curr. Microbiol. 2015, 70, 520–527. [Google Scholar] [CrossRef] [PubMed]
- Lazarova, N.; Krumova, E.; Stefanova, T.; Georgieva, N.; Angelova, M. The oxidative stress response of the filamentous yeast Trichosporon cutaneum R57 to copper, cadmium and chromium exposure. Biotechnol. Biotechnol. Equip. 2014, 28, 855–862. [Google Scholar] [CrossRef]
- Lundy, S.D.; Payne, R.J.; Giles, K.R.; Garrill, A. Heavy metals have diferent effects on mycelial morphology of Achlya bisexualis as determined by fractal geometry. FEMS Microbiol. Lett. 2001, 201, 259–263. [Google Scholar] [CrossRef]
- Ali, E.H. Comparative study of the effect of stress by the heavy metals Cd+2, Pb+2, and Zn+2 on morphological characteristics of Saprolegnia Delica Coker and Dictyuchus Carpophorus Zopf. Pol. J. Microbiol. 2007, 56, 257–264. [Google Scholar]
- Liu, P.; Wei, M.; Zhang, J.; Wang, R.; Li, B.; Chen, Q.; Weng, Q. Changes in mycelia growth, sporulation, and virulence of Phytophthora capsici when challenged by heavy metals (Cu2+, Cr2+ and Hg2+) under acid pH stress. Environ. Pollut. 2018, 235, 372–380. [Google Scholar] [CrossRef]
- Resjö, S.; Brus, M.; Ali, A.; Meijer, H.; Sandin, M.; Govers, F.; Levander, F.; Grenville-Briggs, L.; Andreasson, E. Proteomic analysis of Phytophthora infestans reveals the importance of cell wall proteins in pathogenicity. Mol. Cell. Proteomics 2017, 16, 1958–1971. [Google Scholar] [CrossRef] [Green Version]
- Fry, W. Phytophthora infestans: The plant (and R gene) destroyer. Mol. Plant Pathol. 2008, 9, 385–402. [Google Scholar] [CrossRef]
- Forbes, G.A. Using host resistance to manage potato late blight with particular reference to developing countries. Potato Res. 2012, 55, 205–216. [Google Scholar] [CrossRef]
- Qiu, L.; Wang, K.; Long, W.; Wang, K.; Hu, W.; Amable, G.S. A comparative assessment of the influences of human impacts on soil Cd concentrations based on stepwise linear regression, classification and regression tree, and random forest models. PLoS ONE 2016, 11, e0151131. [Google Scholar] [CrossRef] [Green Version]
- Khan, M.A.; Khan, S.; Khan, A.; Alam, M. Soil contamination with cadmium, consequences and remediation using organic amendments. Sci. Total Environ. 2017, 601, 1591–1605. [Google Scholar] [CrossRef] [PubMed]
- Izbiańska, K.; Floryszak-Wieczorek, J.; Gajewska, J.; Gzyl, J.; Jelonek, T.; Arasimowicz-Jelonek, M. Switchable nitroproteome states of Phytophthora infestans biology and pathobiology. Front. Microbiol. 2019, 10, 1516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Castello, P.R.; David, P.S.; McMlure, T.; Crook, Z.; Poyton, R.O. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: Implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab. 2006, 3, 277–287. [Google Scholar] [CrossRef] [Green Version]
- Chiang, K.T.; Switzer, C.H.; Akali, K.O.; Fukudo, J.M. The role of oxygen and reduced oxygen species in nitric-oxide-mediated cytotoxicity: Studies in the yeast Saccharomyces cerevisiae model system. Toxicol. Appl. Pharmacol. 2000, 167, 30–36. [Google Scholar] [CrossRef]
- Domitrovic, T.; Palhano, F.L.; Barja-Fidalgo, C.; DeFreitas, M.; Orlando, M.T.; Fernandes, P.M. Role of nitric oxide in the response of Saccharomyces cerevisiae cells to heat shock and high hydrostatic pressure. FEMS Yeast Res. 2003, 3, 341–346. [Google Scholar] [CrossRef] [Green Version]
- Orłowska, E.; Fiil, A.; Kirk, H.G.; Llorente, B.; Cvitanich, C. Differential gene induction in resistant and susceptible potato cultivars at early stages of infection by Phytophthora infestans. Plant Cell Rep. 2012, 31, 187–203. [Google Scholar] [CrossRef]
- Jaworska, M.; Gorczyca, A. Effect of metal ions on entomopathogenic fungi pathogenicity. Ecol. Chem. Eng. 2004, 11, 327–339. [Google Scholar]
- Bakti, F.; Sasse, C.; Heinekamp, T.; Pócsi, I.; Braus, G.H. Heavy metal-induced expression of PcaA provides cadmium tolerance to Aspergillus fumigatus and supports its virulence in the Galleria mellonella model. Front. Microbiol. 2018, 9, 744. [Google Scholar] [CrossRef]
- Lorenzo-Gutiérrez, D.; Gómez-Gil, L.; Guarro, J.; Roncero, M.I.G.; Fernández-Bravo, A.; Capilla, J.; López-Fernández, L. Role of the Fusarium oxysporum metallothionein Mt1 in resistance to metal toxicity and virulence. Metallomics 2019, 11, 1230–1240. [Google Scholar] [CrossRef]
- Gill, M. Heavy metal stress in plants: A review. Int. J. Adv. Res. 2014, 2, 1043–1055. [Google Scholar]
- Pengkit, A.; Jeon, S.S.; Son, S.J.; Shin, J.H.; Baik, K.Y.; Choi, E.H.; Park, G. Identification and functional analysis of endogenous nitric oxide in a filamentous fungus. Sci. Rep. 2016, 6, 30037. [Google Scholar] [CrossRef] [Green Version]
- Arasimowicz-Jelonek, M.; Floryszak-Wieczorek, J. A physiological perspective on targets of nitration in NO-based signaling networks in plants. J. Exp. Bot. 2019, 70, 4379–4389. [Google Scholar] [CrossRef] [PubMed]
- Hoernes, T.P.; Erlacher, M.D. Translating the epitranscriptome. WIREs RNA 2017, 8, e1375. [Google Scholar] [CrossRef] [Green Version]
- Ilyas, S.; Kim, M.S.; Lee, J.C.; Jabeen, A.; Bhatti, H.N. Bio-reclamation of strategic and energy critical metals from secondary resources. Metals 2017, 7, 207. [Google Scholar] [CrossRef]
- Han, Y.; Zhao, B.; Zhang, M.; Hong, Y.; Han, H.; Cao, X.; Lu, K.; Lin, J.; Fu, Z. Biochemical properties and vaccine effect of recombinant TPx-3 from Schistosoma japonicum. Parasitol. Res. 2017, 116, 1361–1372. [Google Scholar] [CrossRef] [PubMed]
- Ighodaro, O.M.; Akinloye, O.A. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alex. J. Med. 2018, 54, 287–293. [Google Scholar] [CrossRef] [Green Version]
- Chen, A.; Zeng, G.; Chen, G.; Liu, L.; Shang, C.; Hu, X.; Lu, L.; Chen, M.; Zhou, Y.; Zhang, Q. Plasma membrane behavior, oxidative damage, and defense mechanism in Phanerochaete chrysosporium under cadmium stress. Process Biochem. 2014, 49, 589–598. [Google Scholar] [CrossRef]
- Floryszak-Wieczorek, J.; Arasimowicz-Jelonek, M. Contrasting regulation of NO and ROS in potato defense-associated metabolism in response to pathogens of different lifestyles. PLoS ONE 2016, 11, e0163546. [Google Scholar] [CrossRef] [PubMed]
- Warris, A.; Ballou, E.R. Oxidative responses and fungal infection biology. Semin. Cell Dev. Biol. 2019, 89, 34–46. [Google Scholar] [CrossRef]
- Stroiński, A.; Woźny, A.; Floryszak-Wieczorek, J. Effects of cadmium on the host-pathogen system II. Alterations of potato tuber and Phytophthora infestans relations. Biochem. Physiol. Pflanzen. 1990, 186, 229–238. [Google Scholar] [CrossRef]
- Stroiński, A.; Floryszak-Wieczorek, J.; Woźny, A. Effects of cadmium on the host-pathogen system I. Alterations of potato leaves and Phytophthora infestans relations. Biochem. Physiol. Pflanzen. 1990, 186, 43–54. [Google Scholar] [CrossRef]
- Park, J.I.; Grant, C.M.; Attfield, P.V.; Dawes, I.W. The freeze-thaw stress response of the yeast Saccharomyces cerevisiae is growth phase specific and is controlled by nutritional state via the ras-cyclic amp signal transduction pathway. Appl. Environ. Microbiol. 1997, 63, 3818–3824. [Google Scholar] [CrossRef] [Green Version]
- Arasimowicz-Jelonek, M.; Floryszak-Wieczorek, J.; Izbiańska, K.; Gzyl, J.; Jelonek, T. Implication of peroxynitrite in defence responses of potato to Phytophthora infestans. Plant Pathol. 2016, 65, 754–766. [Google Scholar] [CrossRef] [Green Version]
- Doke, N. Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity. Physiol. Plant Pathol. 1983, 23, 359–367. [Google Scholar] [CrossRef]
- Becana, M.; Aparicio-Tejo, P.; Irigoyen, J.J.; Sanchez-Diaz, M. Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of Medicago sativa. Plant Physiol. 1986, 82, 1169–1171. [Google Scholar] [CrossRef] [Green Version]
- Huang, J.C.; Li, D.J.; Diao, J.C.; Hou, J.; Yuan, J.L.; Zou, G.L. A novel fluorescent method for determination of peroxynitrite using folic acid as a probe. Talanta 2007, 72, 1283–1287. [Google Scholar] [CrossRef]
- Bradford, M.A. Rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Colombo, G.; Clerici, M.; Garavaglia, M.E.; Giustarini, D.; Rossi, R.; Milzani, A.; Dalle-Donne, I. A step-by-step protocol for assaying protein carbonylation in biological samples. J. Chromatogr. B Biomed. Appl. 2016, 1019, 178–190. [Google Scholar] [CrossRef] [PubMed]
- Bartosz, G. Total antioxidant capacity. Adv. Clin. Chem. 2003, 37, 219–292. [Google Scholar]
- Beauchamp, C.; Fridovich, I. Superoxide dismutase—Improvement assays and an assays applicable to acrylamide gels. Anal. Biochem. 1971, 44, 276–287. [Google Scholar] [CrossRef]
- Chance, B.; Maehly, A.C. An assay of catalase and peroxidase. In Methods in Enzymology; Colowick, S.P., Kapland, N.D., Eds.; Academic Press: New York, NY, USA, 1995; pp. 764–791. [Google Scholar]
- Woodbury, W.; Spencer, A.K.; Stahmann, M.A. An improved procedure using ferricyanide for detecting catalase isozymes. Anal. Biochem. 1971, 44, 301–305. [Google Scholar] [CrossRef]
- Zhao, S.; Fernald, R. Comprehensive Algorithm for Quantitative Real-Time Polymerase Chain Reaction. J. Comput. Biol. 2005, 12, 1047–1064. [Google Scholar] [CrossRef]
- Pfaffl, M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29, e45. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gajewska, J.; Azzahra, N.A.; Bingöl, Ö.A.; Izbiańska-Jankowska, K.; Jelonek, T.; Deckert, J.; Floryszak-Wieczorek, J.; Arasimowicz-Jelonek, M. Cadmium Stress Reprograms ROS/RNS Homeostasis in Phytophthora infestans (Mont.) de Bary. Int. J. Mol. Sci. 2020, 21, 8375. https://doi.org/10.3390/ijms21218375
Gajewska J, Azzahra NA, Bingöl ÖA, Izbiańska-Jankowska K, Jelonek T, Deckert J, Floryszak-Wieczorek J, Arasimowicz-Jelonek M. Cadmium Stress Reprograms ROS/RNS Homeostasis in Phytophthora infestans (Mont.) de Bary. International Journal of Molecular Sciences. 2020; 21(21):8375. https://doi.org/10.3390/ijms21218375
Chicago/Turabian StyleGajewska, Joanna, Nur Afifah Azzahra, Özgün Ali Bingöl, Karolina Izbiańska-Jankowska, Tomasz Jelonek, Joanna Deckert, Jolanta Floryszak-Wieczorek, and Magdalena Arasimowicz-Jelonek. 2020. "Cadmium Stress Reprograms ROS/RNS Homeostasis in Phytophthora infestans (Mont.) de Bary" International Journal of Molecular Sciences 21, no. 21: 8375. https://doi.org/10.3390/ijms21218375