ORIGINAL ARTICLE
Effect of selenium on alleviating oxidative stress in pea leaves caused by pea aphid feeding
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1
Department of Plant Physiology, Poznań University of Life Sciences, Poznań, Poland
2
Department of Entomology and Environmental Protection, Poznań University of Life Sciences, Poznań, Poland
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
Submission date: 2020-10-05
Acceptance date: 2020-11-18
Online publication date: 2021-03-11
Corresponding author
Barbara Politycka
Department of Plant Physiology, Poznań University of Life Sciences, Wołyńska 35, 60-637, Poznań, Poland
Journal of Plant Protection Research 2021;61(1):83-94
KEYWORDS
TOPICS
ABSTRACT
The aim of this study was to evaluate the antioxidant effect of selenium in Pisum sativum L.
plants pre-treated with sodium selenite or sodium selenate at a concentration of 10 and
20 μM, and then colonized by pea aphid Acyrthosiphon pisum (Harris). It has been hypothesized
that selenium at low concentrations alleviates oxidative stress caused by aphid
feeding on pea leaves. The study focused on the generation of reactive oxygen species (superoxide
anion, hydrogen peroxide and hydroxyl radical), the activities of the antioxidant
enzymes (superoxide dismutase and ascorbate peroxidase) scavenging the reactive oxygen
species levels, as well as on total antioxidant activity in pea leaves. Selenium in pea leaves
exposed to aphid feeding affected changes in the levels of reactive oxygen species, the activity
of studied antioxidant enzymes, and the total antioxidant capacity. Effects depended
on the form and concentration of selenium, as well as on the time after the colonization of
pea plants by aphids. Obtained results showed beneficial effects of selenium in alleviating
oxidative stress in pea leaves caused by aphid feeding.
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (57)
1.
Andrade F.R., da Silva G.N., Guimarães K.C., Barreto H.B.F., de Souza K.R.D., Guilherme L.R.G., Faquin V., Reis A.R. 2018. Selenium protects rice plants from water deficit stress. Ecotoxicology and Environmental Safety 164: 562–570. DOI:
https://doi.org/10.1016/j.ecoe....
2.
Apel K., Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55: 373–399. DOI:
https://doi.org/10.1146/annure....
3.
Bartosz G. 2013. Druga twarz tlenu. Wolne rodniki w przyrodzie. [Second Face of Oxygen. Free Radicals in Nature]. Wydawnictwo Naukowe PWN, Warszawa, Poland, 447 pp. (in Polish).
4.
Beauchamp C., Fridovich I. 1971. Superoxide dismutase, improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44 (1): 276–287. DOI:
https://doi.org/10.1016/0003-2....
5.
Bradford M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1–2): 248–254. DOI:
https://doi.org/10.1016/0003-2....
6.
Cartes P., Jara A., Pinilla L., Rosas A., Mora M. 2010. Selenium improves the antioxidant ability against aluminium-induced oxidative stress in ryegrass roots. Annales of Applied Biology 156: 297–307. DOI:
https://doi.org/10.1111/j.1744....
7.
Coppola V., Coppola M., Rocco M., Digilio M.C., D’Ambrosio C., Renzone G., Renzone G., Martinelli R., Scaloni A., Pennacchio F., Rao R., Corrado G. 2013. Transcriptomic and proteomic analysis of a compatible tomato-aphid interaction reveals a predominant salicylic acid-dependent plant response. BMC Genomocs 14: 515–532. DOI:
https://doi.org/10.1186/1471-2....
8.
Czerniewicz P., Sytykiewicz H., Durak R., Borowiak-Sobkowiak B., Chrzanowski G. 2017. Role of phenolic compounds during antioxidative responses of winter triticale to aphid and beetle attack. Plant Physiology and Biochemistry 118: 529–540. DOI:
https://doi.org/10.1016/j.plap....
9.
Dampc J., Kula-Maximenko M., Molon M., Durak R. 2020. Enzymatic defense response of apple aphid Aphis pomi to increased temperature. Insects 11 (7): 436. DOI:
https://doi.org/10.3390/insect....
10.
Das K., Roychoudhury A. 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science 2: 53. DOI:
https://doi.org/10.3389/ fenvs.2014.00053.
11.
Dat J., Vandenabeele S., Vranová E., Van Montagu M., Inzé D., van Breusegem F. 2000. Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57: 779–795. DOI:
https://doi: 10.1007/s000180050041.
12.
del Pino A.M., Guiducci M., D’Amato R., Di Michele A., Tosti G., Datti A., Palmerini C.A. 2019. Selenium maintains cytosolic Ca2+ homeostasis and preserves germination rates of maize pollen under H2O2-induced oxidative stress. Scientific Reports 9 (1): 1–9. DOI:
https://doi.org/1038/s41598-01....
13.
del Río L.A., Corpas F.J., Sandalio L.M., Palma J.M., Gómez M., Barroso J.B. 2002. Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. Journal of Experimental Botany 53: 1255–1272. DOI:
https://doi.org/10.1093/jexbot....
14.
Doke N. 1983. Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiological Plant Pathology 23 (3): 345–357. DOI:
https://doi.org/10.1016/0048-4....
15.
Feng R., Wei C., Tu S. 2013. The roles of selenium in protecting plants against abiotic stresses. Environmental and Experimental Botany 87: 58–68. DOI:
https://doi.org/10.1016/j.enve....
16.
Foyer C.H., Rasool B., Davey J.W., Hancock R.D. 2016. Cross-tolerance to biotic and abiotic stresses in plants: a focus on resistance to aphid infestation. Journal of Experimental Botany 67 (7): 2025–2037. DOI:
https://doi.org/10.1093/jxb/er....
17.
Gill S.S., Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48 (12): 909–930. DOI:
https://doi.org/10.1016/j.plap....
18.
Gouveia G.C.C., Galindo F.S., Lanza M.G.D.B., Silva A.C.R., Mateus M.P.B., Silva M.S., Tavanti R.F.R., Tavanti T.R., Lavres J., Reis A.R. 2020. Selenium toxicity stress-induced phenotypical, biochemical and physiological responses in rice plants: Characterization of symptoms and plant metabolic adjustment. Ecotoxicology and Environmental Safety 202: e110916. DOI:
https://doi.org/10.1016/j.ecoe....
19.
Guardado-Félixa D., Serna-Saldivarb S.O., Cuevas-Rodrígueza E.O., Jacobo-Velázquezb D.A., Gutiérrez-Uribeb J.A. 2017. Effect of sodium selenite on isoflavonoid contents and antioxidant capacity of chickpea (Cicer arietinum L.) sprouts. Food Chemistry 226: 69–74. DOI:
https://doi.org/10.1016/j.food....
20.
Gupta M., Gupta S. 2017. An overview of plant selenium uptake, metabolism and toxicity in plants. Frontiers in Plant Science 7: e2074. DOI:
https://doi.org/10.3389/fpls.2....
21.
Habibi G. 2013. Effect of drought stress and selenium spraying on photosynthesis and antioxidant activity of spring barley. Acta Agriculturae Slovenica 101: 31–39. DOI:
https://doi.org/10.2478/acas-2....
23.
He J., Chen F., Chen S., Lv G., Deng Y., Fang W., Guan Z., He C. 2011. Chrysanthemum leaf epidermal surface morphology and antioxidant and defence enzyme activity in response to aphid infestation. Journal of Plant Physiology 168 (7): 687–693. DOI:
https://doi.org/10.1016/j.jplp....
24.
Holman J. 2009. Host Plant Catalog for Aphids. Palearctic Region. Springer Science + Business Media B.V., Berlin/Heidelberg, Germany, 1216 pp.
25.
Hossain M.A., Bhattacharjee S., Armin S.M., Qian P., Xin W., Li H.Y., Burritt D.J., Fujita M., Tran L.-S.P. 2015. Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Frontiers in Plant Science 6: e420. DOI:
https://doi.org/10.3389/ fpls.2015.00420.
26.
Kasote D.M., Katyare S.S., Hegde M.V., Bae H. 2015. Significance of antioxidant potential of plants and its relevance to therapeutic applications. International Journal of Biological Sciences 11 (8): 982–991. DOI:
https://doi:10.7150/ijbs.12096.
27.
Kuśnierczyk A., Winge P., Jorstad T.S., Troczyńska J., Rossiter J.T., Bunes A.M. 2008. Towards global understanding of plant defence against aphids timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant, Cell and Environment 31 (8): 1097–1115. DOI:
https://doi.org/10.1111/j.1365....
28.
Lehmann S., Serrano M., L’Haridon F., Tjamos S.E., Metraux J.P. 2015. Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry 112: 54–62. DOI:
https://doi.org/10.1016/j.phyt....
29.
Łukasik I., Goławska S., Wójcicka A. 2012. Effect of cereal aphid infestation on ascorbate content and ascorbate peroxidase activity in triticale. Polish Journal of Environmental Studies 21 (6): 1937–1941.
30.
Łukasik I., Goławska S. 2013. Effect of host plant on levels of reactive oxygen species andantioxidants in the cereal aphids Sitobion avenae and Rhopalosiphum padi. Biochemical Systematic and Ecology 51: 232–239. DOI:
https://doi.org/10.1016/j.bse.....
31.
Łukaszewicz S., Politycka B., Smoleń S. 2018. Effect of selenium on the content of essential micronutrients and their translocation in garden pea. Journal of Elementology 23 (4): 1307–1317. DOI:
https://doi.org/10.5601/jelem.....
32.
Maffei M.E., Mithöfer A., Boland W. 2007. Insects feeding on plants: Rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68 (22–24): 2946–2959. DOI:
https://doi.org/10.1016/j.phyt....
33.
Mai V.C., Bednarski W., Borowiak-Sobkowiak B., Wilkaniec B., Samardakiewicz S., Morkunas I. 2013. Oxidative stress in pea seedling leaves in response to Acirthosiphon pisum infestation. Phytochemistry 93: 49–62. DOI:
https://doi.org/10.1016/j.phyt....
34.
Mai V.C., Tran N.T., Nguyen D.S. 2016. The involvement of peroxidases in soybean seedlings’ defence against infestation of cowpea aphid. Arthropod-Plant Interactions 10: 283–292. DOI:
https://doi.org/10.1007/s11829....
35.
Marchi-Werle L., Heng-Moss T.M., Hunt T.E., Baldin E.L.L., Baird L.M. 2014. Characterization of peroxidase changes in tolerant and susceptible soybeans challenged by soybean aphid (Hemiptera: Aphididae). Journal of Economic Entomology 107 (5): 1985–1991. DOI:
https://doi.org/10.1603/EC1422....
36.
Mechora Š., Ugrinović K. 2015. Can plant-herbivore interaction be affected by selenium? Austin Journal of Environmental Toxicology 1 (1): e5.
37.
Messner B., Boll M. 1994. Cell suspension of spruce (Picea abies): inactivation of extracellular enzymes by fungal elicitor-induced transient release of hydrogen peroxide. Plant Cell Tissue Organ and Culture 39: 69–78. DOI:
https://doi.org/10.1007/BF0003....
38.
Moloi M.J., van der Westhuizen A.J. 2008. Antioxidative enzymes and the Russian wheat aphid (Diuraphis noxia) resistance response in wheat (Triticum aestivum). Plant Biology 10 (3): 403–407. DOI:
https://doi.org/10.1111/j.1438....
39.
Nakano Y., Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiology 22 (5): 867–880. DOI:
https://doi.org/10.1093/oxford....
40.
Ni X., Quinsberry S.S. 2003. Possible roles of esterase, glutathione S-transferase, and superoxide dismutase activities in understanding aphid–cereal interactions. Entomologia Experimentalis et Applicata 108: 187–195. DOI:
https://doi.org/10.1046/j.1570....
41.
Ni X., Quisenberry S.S., Heng-Moss T.M., Markwell J., Sarath G., Klucas R., Baxendale F. 2001. Oxidative responses of resistant and susceptible cereal leaves to symptomatic and nonsymptomatic cereal aphid (Hemiptera: Aphididae) feeding. Journal of Economic Entomology 94: 743–751. DOI:
https://doi.org/10.1603/0022-0....
42.
Pereira A.S., Dorneles A.O.S., Bernardy K., Sasso V.M., Bernardy D., Possebom G., Rossato L.V., Dressler V.L., Tabaldi L.A. 2018. Selenium and silicon reduce cadmium uptake and mitigate cadmium toxicity in Pfaffia glomerata (Spreng.) Pedersen plants by activation antioxidant enzyme system. Environmental Science and Pollution Research 25: 18548–18558. DOI:
https://doi.org/10.1007/s11356....
43.
Pierson L.M., Heng-Moss T.M., Hunt T.E., Reese J. 2011. Physiological responses of resistant and susceptible reproductive stage soybean to soybean aphid (Aphis glycines Matsumura) feeding. Arthropod-Plant Interactions 5: 49–58. DOI:
https://doi.org/10.1007/s11829....
44.
Prochaska T.J. 2011. Characterization of the Tolerance Response in the Soybean KS4202 to Aphis glycines Matsumura. M.Sc. Thesis, University of Nebraska, Lincoln, USA.
45.
Prochaska T.J., Pierson L.M., Baldin E.L.L., Hunt T.E., Heng-Moss T.M., Reese J.C. 2013. Evaluation of late vegetative and reproductive stage soybeans for resistance to soybean aphid (Hemiptera: Aphididae). Journal of Economic Entomology 106 (2): 1036–1044. DOI:
https://doi.org/10.1603/EC1232....
46.
Quan L.J., Zhang B., Shi W.W., Li H.Y. 2008. Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. Journal od Integrative Plant Biology 50: 2–18. DOI:
https://doi.org/10.1111/j.1744....
47.
Re R., Pellegrini N., Proteggente A., Pannala A., Yang M., Rice-Evans C. 1999. Antioxidant activity applying and improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine 26: 1231–1237. DOI:
https://doi.org/10.1016/s0891-....
48.
Ríos J.J., Blasco B., Cervilla L.M., Rosales M.A., Sanchez-Rodriguez E., Romero L., Ruiz J.M. 2009. Production and detoxification of H2O2 in lettuce plants exposed to selenium. Annals of Applied Biology 154: 107–116. DOI:
https://doi.org/10.1111/j.1744....
49.
Saxena I., Srikanth S., Chen Z. 2016. Cross talk between H2O2 and interacting signal molecules under plant stress response. Frontiers in Plant Science 7: e570. DOI:
https://doi.org/10.3389/fpls.2....
50.
Shalaby T., Bayoumi Y., Alshaal T., Elhawat N., Sztrik A., El-Ramady H. 2017. Selenium fortification induces growth, antioxidant activity, yield and nutritional quality of lettuce in salt-affected soil using foliar and soil applications. Plant Soil 421: 245–258. DOI:
https://doi.org/10.1007/s11104....
51.
Shao Y., Guo M., He X., Fan Q., Wang Z., Jia J., Guo J. 2019. Constitutive H2O2 is involved in sorghum defense against aphids. Brazilian Journal of Botany 42 (2): 271–281. DOI:
https://doi.org/10.1007/s40415....
52.
Sieprawska A., Kornaś A., Filek M. 2015. Involvement of selenium in protective mechanisms of plants under environmental stress conditions – review. Acta Biologica Cracoviensia. Series Botanica 57 (1): 9–20. DOI:
http://dx.doi.org/10.1515/abcs....
53.
van Breusegem F., Vranová E., Dat J.F., Inzé D. 2001. The role of active oxygen species in plant signal transduction. Plant Science 161 (3): 405–416. DOI:
https://doi.org/10.1016/S0168-....
54.
von Tiedemann A.V. 1997. Evidence for a primary role of active oxygen species in induction of host cell death during infection of bean leaves with Botrytis cinerea. Physiological and Molecular Plant Pathology 50 (3): 151–166. DOI:
https://doi.org/10.1006/pmpp.1....
55.
Walz C., Juenger M., Schad M., Kehr J. 2002. Evidence for the presence and activity of a complete defence system in mature sieve tubes. The Plant Journal 31 (2): 189–197. DOI:
https://doi.org/10.1046/j.1365....
56.
Wu J., Baldwin I.T. 2010. New insights into plant responses to the attack from insect herbivores. Annual Review of Genetics 44: 1–24. DOI:
https://doi.org/10.1146/annure....
57.
Yang T., Poovaiah B. W. 2002. Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proceedings of the National Academy of Sciences of the United States of America 99 (6): 4097–4102. DOI:
https://doi.org/10.1073/pnas.0....