Abstract
Intertidal macroalgae can cope with the dual effects of UV-B irradiation and allelopathy. To study the impacts of the two stressors, we co-cultured Corallina pilulifera with Sargassum thunbergii in 1:1 and 1:10 ratios under different doses of UV-B radiation. The response of the antioxidant defense system, focusing on activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), peroxidase (POX) and glutathione reductase (GR), was monitored. In addition, isoenzyme patterns were analyzed using non-denaturing polyacrylamide gel electrophoresis. The results show that the activities of SOD, APX, and GR were all significantly affected by both UV-B radiation and allelopathy, and the effect of their interaction was significant. However, POX activity was only influenced by UV-B radiation. The enzymatic assay revealed four distinct bands of SOD. The SODIII band weakened significantly when the co-cultures were exposed to extremely high dosage of UV-B irradiation under both co-culturing ratios of 1:1 and 1:10. When the co-culturing ratio was 1:10, both POXII and APXII enzyme activities increased with different UV-B doses. GR activity was at its greatest when the co-culture ratio was 1:10 and exposure was to the higher UV-B doses. The activities of GRIII and GRIV were elevated under all UV treatments whereas the activities of GRI and GRII were reduced under the lower UV-B treatments but were elevated under the higher UV-B treatments. However, lipid peroxidation, as indicated by the thiobarbituric acid-reacting substance (TBARS) assay, increased significantly under the dual stressors. Our data suggest that allelopathy and UV-B radiation stress can each affect the antioxidant enzyme activities of C. pilulifera. Critically, the adverse effects of UV-B on C. pilulifera were intensified by the compounding effects of allelopathy.
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Data Availability Statement
The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Adelaide Dias M, Manuela Costa M. 1983. Effect of low salt concentrations on nitrate reductase and peroxidase of sugar beet leaves. Journal of Experimental Botany, 34(5): 537–543, https://doi.org/10.1093/jxb/34.5.537.
Aguilera J, Dummermuth A, Karsten U, Schriek R, Wiencke C. 2002. Enzymatic defences against photooxidative stress induced by ultraviolet radiation in Arctic marine macroalgae. Polar Biology, 25(6): 432–441, https://doi.org/10.1007/s00300-002-0362-2.
Asada K. 1992. Ascorbate peroxidase-a hydrogen peroxide-scavenging enzyme in plants. Physiologia Plantarum, 85(2): 235–241, https://doi.org/10.1111/j.1399-3054.1992.tb04728.x.
Bano C, Amist N, Sunaina, Singh N B. 2017. UV-B radiation escalate allelopathic effect of benzoic acid on Solanum lycopersicum L. Scientia Horticulturae, 220: 199–205, https://doi.org/10.1016/j.scienta.2017.03.052.
Beauchamp C, Fridovich I. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44(1): 276–287, https://doi.org/10.1016/0003-2697(71)90370-8.
Bowler C, Van Camp W, Van Montagu M, Inzé D, Asada P K. 1994. Superoxide dismutase in plants. Critical Reviews in Plant Sciences, 13(3): 199–218, https://doi.org/10.1080/07352689409701914.
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, https://doi.org/10.1016/0003-2697(76)90527-3.
Calabrese E J, Baldwin L A. 2003. Toxicology rethinks its central belief. Nature, 421(6924): 691–692, https://doi.org/10.1038/421691a.
Caldwell M M, Björn L O, Bornman J F, Flint S D, Kulandaivelu G, Teramura A H, Tevini M. 1998. Effects of increased solar ultraviolet radiation on terrestrial ecosystems. Journal of Photochemistry and Photobiology B: Biology, 46(1–3): 40–52, https://doi.org/10.1016/S1011-1344(98)00184-5.
Copin P J, Chèvre N. 2018. Modelling the effects of PSII inhibitor pulse exposure on two algae in co-culture. Ecotoxicology, 27(2): 154–168, https://doi.org/10.1007/s10646-017-1881-5.
Corcoran A A, Seger M, Niu R L, Khandan N N, Lammers P J, Holguin F O, Boeing W J. 2019. Evidence for induced allelopathy in an isolate of Coelastrella following co-culture with Chlorella sorokiniana. Algal Research, 41: 101535, https://doi.org/10.1016/j.algal.2019.101535.
Costa H, Gallego S M, Tomaro M L. 2002. Effect of UV-B radiation on antioxidant defense system in sunflower cotyledons. Plant Science, 162(6): 939–945, https://doi.org/10.1016/S0168-9452(02)00051-1.
de Wit M, Galvão V C, Fankhauser C. 2016. Light-mediated hormonal regulation of plant growth and development. Annual Review of Plant Biology, 67: 513–537, https://doi.org/10.1146/annurev-arplant-043015-112252.
Ding S H, Lu Q T, Zhang Y, Yang Z P, Wen X G, Zhang L X, Lu C M. 2009. Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state. Plant Molecular Biology, 69(5): 577–592, https://doi.org/10.1007/s11103-008-9440-3.
Dong J, Chang M Y, Li C L, Dai D J, Gao Y N. 2019. Allelopathic effects and potential active substances of Ceratophyllum demersum L. on Chlorella vulgaris Beij. Aquatic Ecology, 53(4): 651–663, https://doi.org/10.1007/s10452-019-09715-2.
Farjalla V F, Anesio A M, Bertilsson S, Granéli W. 2001. Photochemical reactivity of aquatic macrophyte leachates: abiotic transformations and bacterial response. Aquatic Microbial Ecology, 24(2): 187–195, https://doi.org/10.3354/ame024187.
Fistarol G O, Legrand C, Selander E, Hummert C, Stolte W, Granéli E. 2004. Allelopathy in Alexandrium spp.: effect on a natural plankton community and on algal monocultures. Aquatic Microbial Ecology, 35(1): 45–56, https://doi.org/10.3354/ame035045.
Foyer C H, Lelandais M, Kunert K J. 1994. Photooxidative stress in plants. Physiologia Plantarum, 92(4): 696–717, https://doi.org/10.1111/j.1399-3054.1994.tb03042.x.
Franklin L, Forster R. 1997. The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. European Journal of Phycology, 32(3): 207–232, https://doi.org/10.1080/09670269710001737149.
Franzè G, Pierson J J, Stoecker D K, Lavrentyev P J. 2018. Diatom-produced allelochemicals trigger trophic cascades in the planktonic food web. Limnology and Oceanography, 63(3): 1093–1108, https://doi.org/10.1002/lno.10756.
Friedlander M, Gonen Y, Kashman Y, Beer S. 1996. Gracilaria conferta and its epiphytes: 3. Allelopathic inhibition of the red seaweed by Ulva cf. lactuca. Journal of Applied Phycology, 8(1): 21–25, https://doi.org/10.1007/BF02186217.
Gao Y N, Ge F J, Zhang L P, He Y, Lu Z Y, Zhang Y Y, Liu B Y, Zhou Q H, Wu Z B. 2017. Enhanced toxicity to the cyanobacterium Microcystis aeruginosa by low-dosage repeated exposure to the allelochemical N-phenyl-1-naphthylamine. Chemosphere, 174: 732–738, https://doi.org/10.1016/j.chemosphere.2017.01.102.
Giannopolitis C N, Ries S K. 1977. Superoxide dismutases: II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiology, 59(2): 315–318, https://doi.org/10.1104/pp.59.2.315.
Gill S S, Anjum N A, Hasanuzzaman M, Gill R, Trivedi D K, Ahmad I, Pereira E, Tuteja N. 2013. Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiology and Biochemistry, 70: 204–212, https://doi.org/10.1016/j.plaphy.2013.05.032.
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, https://doi.org/10.1016/j.plaphy.2010.08.016.
Guillard R R L, Ryther J H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology, 8(2): 229–239, https://doi.org/10.1139/m62-029.
Heath R L, Packer L. 1968. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125(1): 189–198, https://doi.org/10.1016/0003-9861(68)90654-1.
Holzinger A, Albert A, Aigner S, Uhl J, Schmitt-Kopplin P, Trumhová K, Pichrtová M. 2018. Arctic, Antarctic, and temperate green algae Zygnema spp. under UV-B stress: vegetative cells perform better than pre-akinetes. Protoplasma, 255(4): 1239–1252, https://doi.org/10.1007/s00709-018-1225-1.
Hong Y, Hu H Y, Li F M. 2008. Physiological and biochemical effects of allelochemical ethyl 2-methyl acetoacetate (EMA) on cyanobacterium Microcystis aeruginosa. Ecotoxicology and Environmental Safety, 71(2): 527–534, https://doi.org/10.1016/j.ecoenv.2007.10.010.
Karsten U, Holzinger A. 2014. Green algae in alpine biological soil crust communities: acclimation strategies against ultraviolet radiation and dehydration. Biodiversity and Conservation, 23(7): 1845–1858, https://doi.org/10.1007/s10531-014-0653-2.
Keating K I. 1977. Allelopathic influence on blue-green bloom sequence in a eutrophic lake. Science, 196(4292): 885–887, https://doi.org/10.1126/science.196.4292.885.
Laemmli U K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227(5259): 680–685, https://doi.org/10.1038/227680a0.
Lee T M, Shiu C T. 2009. Implications of mycosporine-like amino acid and antioxidant defenses in UV-B radiation tolerance for the algae species Ptercladiella capillacea and Gelidium amansii. Marine Environmental Research, 67(1): 8–16, https://doi.org/10.1016/j.marenvres.2008.09.006.
Li H, Wang H, Wen W J, Yang G W. 2020. The antioxidant system in Suaeda salsa under salt stress. Plant Signaling & Behavior, 15(7): 1771939, https://doi.org/10.1080/15592324.2020.1771939.
Li L X, Wang X J, Zhao J Q. 2017. Effect of UV radiation on the activities of antioxidant enzymes and their isoforms in Ulva pertusa (Chlorophyta). Marine Sciences, 41(4): 1–9, https://doi.org/10.11759/hykx20160528002. (in Chinese with English abstract)
Li L X, Zhang P Y, Zhao J Q, Zhou W L, Tang X X. 2010. Effect of UV-B irradiation on interspecific competition between Ulva pertusa and Grateloupia filicina. Chinese Journal of Oceanology and Limnology, 28(2): 288–294, https://doi.org/10.1007/s00343-010-9255-3.
Luan X L, Qiao T F, Lyu M, Liao C Y, Wang D Q, Liu D Y, Chen L X. 2020. Sediment records of DDTs in intertidal sediment core of Daliao River Estuary and their responses to anthropogenic activities in the past century. Environmental Chemistry, 39(1): 119–127, https://doi.org/10.7524/j.issn.0254-6108.2019043001. (in Chinese with English abstract)
Luengo Escobar A, Alberdi M, Acevedo P, Machado M, Nunes-Nesi A, Inostroza-Blancheteau C, Reyes-Díaz M. 2017. Distinct physiological and metabolic reprogramming by highbush blueberry (Vaccinium corymbosum) cultivars revealed during long-term UV-B radiation. Physiologia Plantarum, 160(1): 46–64, https://doi.org/10.1111/ppl.12536.
Mahmood K, Khan M B, Song Y Y, Ijaz M, Luo S M, Zeng R S. 2013. UV-irradiation enhances rice allelopathic potential in rhizosphere soil. Plant Growth Regulation, 71(1): 21–29, https://doi.org/10.1007/s10725-013-9804-9.
Mittler R, Zilinskas B A. 1993. Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium. Analytical Biochemistry, 212(2): 540–546, https://doi.org/10.1006/abio.1993.1366.
Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7(9): 405–410, https://doi.org/10.1016/S1360-1385(02)02312-9.
Mulderij G, Mau B, van Donk E, Gross E M. 2007. Allelopathic activity of Stratiotes aloides on phytoplankton-towards identification of allelopathic substances. Hydrobiologia, 584(1): 89–100, https://doi.org/10.1007/s10750-007-0602-0.
Mulderij G, Mooij W M, Smolders A J P, van Donk E. 2005. Allelopathic inhibition of phytoplankton by exudates from Stratiotes aloides. Aquatic Botany, 82(4): 284–296, https://doi.org/10.1016/j.aquabot2005.04.001.
Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22(5): 867–880, https://doi.org/10.1093/oxfordjournals.pcp.a076232.
Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer C H. 2012. Glutathione in plants: an integrated overview. Plant, Cell & Environment, 35(2): 454–484, https://doi.org/10.1111/j.1365-3040.2011.02400.x.
Ohsawa N, Ogata Y, Okada N, Itoh N. 2001. Physiological function of bromoperoxidase in the red marine alga, Corallina pilulifera: production of bromoform as an allelochemical and the simultaneous elimination of hydrogen peroxide. Phytochemistry, 58(5): 683–692, https://doi.org/10.1016/S0031-9422(01)00259-X.
Poulin R X, Poulson-Ellestad K L, Roy J S, Kubanek J. 2018. Variable allelopathy among phytoplankton reflected in red tide metabolome. Harmful Algae, 71: 50–56, https://doi.org/10.1016/j.hal.2017.12.002.
Ramlall C, Varghese B, Ramdhani S, Pammenter N W, Bhatt A, Berjak P, Sershen. 2015. Effects of simulated acid rain on germination, seedling growth and oxidative metabolism of recalcitrant-seeded Trichilia dregeana grown in its natural seed bank. Physiologia Plantarum, 153(1): 149–160, https://doi.org/10.1111/ppl.12230.
Rao M V, Hale B A, Ormrod D P. 1995. Amelioration of ozone-induced oxidative damage in wheat plants grown under high carbon dioxide (Role of antioxidant enzymes). Plant Physiology, 109(2): 421–432, https://doi.org/10.1104/pp.109.2.421.
Rao M V, Paliyath G, Ormrod D P. 1996. Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiology, 110(1): 125–136, https://doi.org/10.1104/pp.110.L125.
Rautenberger R, Wiencke C, Bischof K. 2013. Acclimation to UV radiation and antioxidative defence in the endemic Antarctic brown macroalga Desmarestia anceps along a depth gradient. Polar Biology, 36(12): 1779–1789, https://doi.org/10.1007/s00300-013-1397-2.
Roleda M Y, Wiencke C, Hanelt D, Bischof K. 2007. Sensitivity of the early life stages of macroalgae from the northern hemisphere to ultraviolet radiation. Photochemistry and Photobiology, 83(4): 851–862, https://doi.org/10.1562/2006-08-17-IR-1005.
Roleda M Y. 2009. Photosynthetic response of Arctic kelp zoospores exposed to radiation and thermal stress. Photochemical & Photobiological Sciences, 8(9): 1302–1312, https://doi.org/10.1039/b901098j.
Schweikert K, Burritt D J. 2012. The organophosphate insecticide Coumaphos induces oxidative stress and increases antioxidant and detoxification defences in the green macroalgae Ulva pertusa. Aquatic Toxicology, 122–123: 86–92, https://doi.org/10.1016/j.aquatox.2012.05.003.
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K. 2002. Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany, 53(372): 1305–1319, https://doi.org/10.1093/jexbot/53.372.1305.
Shiu C T, Lee T M. 2005. Ultraviolet-B-induced oxidative stress and responses of the ascorbate-glutathione cycle in a marine macroalga Ulva fasciata. Journal of Experimental Botany, 56(421): 2851–2865, https://doi.org/10.1093/jxb/eri277.
Smerilli A, Balzano S, Maselli M, Blasio M, Orefice I, Galasso C, Sansone C, Brunet C. 2019. Antioxidant and Photoprotection Networking in the Coastal Diatom Skeletonema marinoi. Antioxidants, 8(6): 154, https://doi.org/10.3390/antiox8060154.
Srivastava P K, Singh V P, Prasad S M. 2012. Compatibility of ascorbate-glutathione cycle enzymes in cyanobacteria against low and high UV-B exposures, simultaneously exposed to low and high doses of chlorpyrifos. Ecotoxicology and Environmental Safety, 83: 79–88, https://doi.org/10.1016/j.ecoenv.2012.06.009.
Strom S L. 2008. Microbial ecology of ocean biogeochemistry: a community perspective. Science, 320(5879): 1043–1045, https://doi.org/10.1126/science.1153527.
Tahmasebi A, Aram F, Ebrahimi M, Mohammadi-Dehcheshmeh M, Ebrahimie E. 2012. Genome-wide analysis of cytosolic and chloroplastic isoforms of glutathione reductase in plant cells. Plant Omics, 5(2): 94–102, https://doi.org/10.3316/informit.183077184816825.
Temmerman S, Meire P, Bouma T J, Herman P M J, Ysebaert T, De Vriend H J. 2013. Ecosystem-based coastal defence in the face of global change. Nature, 504(7478): 79–83, https://doi.org/10.1038/nature12859.
Tóth T, Zsiros O, Kis M, Garab G, Kovács L. 2012. Cadmium exerts its toxic effects on photosynthesis via a cascade mechanism in the cyanobacterium, Synechocystis PCC 6803. Plant, Cell & Environment, 35(12): 2075–2086, https://doi.org/10.1111/j.1365-3040.2012.02537.x.
Van de Poll W H, Eggert A, Buma A G J, Breeman A M. 2001. Effects of UV-B-induced DNA damage and photoinhibition on growth of temperate marine red macrophytes: habitat-related differences in UV-B tolerance. Journal of Phycology, 37(1): 30–38, https://doi.org/10.1046/j.1529-8817.2001.037001030.x.
Van Loon L C. 1971. Tobacco polyphenoloxidases: a specific staining method indicating non-identity with peroxidases. Phytochemistry, 10(3): 503–507, https://doi.org/10.1016/S0031-9422(00)94689-2.
Wang F B, Liu J C, Zhou L J, Pan G, Li Z W, Zaidi S H R, Cheng F M. 2016. Senescence-specific change in ROS scavenging enzyme activities and regulation of various SOD isozymes to ROS levels in psf mutant rice leaves. Plant Physiology and Biochemistry, 109: 248–261, https://doi.org/10.1016/j.plaphy.2016.10.005.
Wang R J, Tang X X. 2016. Allelopathic effects of macroalga Corallina pilulifera on the red-tide forming alga Heterosigma akashiwo under laboratory conditions. Chinese Journal of Oceanology and Limnology, 34(2): 314–321, https://doi.org/10.1007/s00343-015-4336-y.
Wang Y, Tang X X, Li Y Q, Yu Z M. 2007. Antioxidant and isozyme features of two strains of Laminaria japonica (Phaeophyceae). Chinese Journal of Oceanology and Limnology, 25(1): 67–72, https://doi.org/10.1007/s00343-007-0067-z.
Wu Y H, Tang J, Liu J Z, Graham B, Kerr P G, Hong C. 2017. Sustained high nutrient supply as an allelopathic trigger between periphytic biofilm and Microcystis aeruginosa. Environmental Science & Technology, 51(17): 9614–9623, https://doi.org/10.1021/acs.est.7b01027.
Ye C P, Liao H P, Yang Y F. 2014. Allelopathic inhibition of photosynthesis in the red tide-causing marine alga, Scrippsiella trochoidea (Pyrrophyta), by the dried macroalga, Gracilaria lemaneiformis (Rhodophyta). Journal of Sea Research, 90: 10–15, https://doi.org/10.1016/j.seares.2014.02.015.
Zapata J M, Sabater B, Martín M. 1998. Identification of a thylakoid peroxidase of barley which oxidizes hydroquinone. Phytochemistry, 48(7): 1119–1123, https://doi.org/10.1016/S0031-9422(98)00133-2.
Zhang S L, Zhang B, Dai W, Zhang X M. 2011. Oxidative damage and antioxidant responses in Microcystis aeruginosa exposed to the allelochemical berberine isolated from golden thread. Journal of Plant Physiology, 168(7): 639–643, https://doi.org/10.1016/j.jplph.2010.10.005.
Zhao J Q, Li L X. 2014. Effects of UV-B irradiation on isoforms of antioxidant enzymes and their activities in red alga Grateloupia filicina (Rhodophyta). Chinese Journal of Oceanology and Limnology, 32(6): 1364–1372, https://doi.org/10.1007/s00343-015-3366-9.
Zhao X Y, Zheng W, Qu T F, Zhong Y, Xu J H, Jiang Y S, Zhan H X, Tang X X, Wang Y. 2021. Dual roles of reactive oxygen species in intertidal macroalgae Ulva prolifera under ultraviolet-B radiation. Environmental and Experimental Botany, 189: 104534, https://doi.org/10.1016/j.envexpbot.2021.104534.
Zhou J, Lyu Y, Richlen M L, Anderson D M, Cai Z H. 2016. Quorum sensing is a language of chemical signals and plays an ecological role in algal-bacterial interactions. Critical Reviews in Plant Sciences, 35(2): 81–105, https://doi.org/10.1080/07352689.2016.1172461.
Zhou X J, Zhang Y R, An X L, de Philippis R, Ma X Y, Ye C R, Chen L Z. 2019. Identification of aqueous extracts from Artemisia ordosica and their allelopathic effects on desert soil algae. Chemoecology, 29(2): 61–71, https://doi.org/10.1007/s00049-018-00276-8
Zuo S P, Wan K, Ma S M. 2015. Combined effect of predatory zooplankton and allelopathic aquatic macrophytes on algal suppression. Environmental Technology, 36(1): 54–59, https://doi.org/10.1080/09593330.2014.936520.
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The authors are grateful to Professor Emerita Paula Jameson, University of Canterbury, New Zealand, financially supported by “Double Hundred” Plan for Foreign Experts in Shandong Province, China, for critical reviewing and editing of this manuscript.
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Liu, M., Zhao, J., Pang, Y. et al. UV-B irradiation and allelopathy by Sargassum thunbergii affects the activities of antioxidant enzymes and their isoenzymes in Corallina pilulifera. J. Ocean. Limnol. 40, 1950–1962 (2022). https://doi.org/10.1007/s00343-021-1124-8
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DOI: https://doi.org/10.1007/s00343-021-1124-8