Abstract
Aquatic plants suffer stress caused by abiotic and biotic variables. In estuaries, salinity is one of the main abiotic factors responsible for stress. This study aimed to evaluate oxidative stress in two species of aquatic macrophytes (Crinum americanum and Spartina alterniflora) that are common in Brazilian tropical estuaries. We measured reactive oxygen species (hydrogen peroxide and malondialdehyde) and total nitrogen (TN) and total phosphorus (TP) in the aboveground and belowground biomass of the species. In addition, we measured salinity, TN, and TP content in the sediment. Statistical tests included t test and the analysis of variance (ANOVA) followed by the Tukey’s test. Our results showed that the greatest oxidative stress, in both species, occurred in areas of the estuary with lower salinity. For C. americanum, limitation by TN and TP content in the sediment is the main cause of oxidative stress. For S. alterniflora, the presence of C. americanum and the allelopathic compounds released by it seem to be the major cause of oxidative stress. Salinity did not induce oxidative stress in C. americanum and S. alterniflora in the estuary; however, the difference in TP and TN contents in the sediment played an important role in their responses to oxidative stress.
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Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal R (2017) Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiol Mol Biol Plants 23:731-744. https://doi.org/10.1007/s12298-017-0462-7
Ahmad P, Jaleel CA, Azooz MM, Nabi G (2009) Generation of ROS and non-enzymatic antioxidants during abiotic stress in plants. Bot Res Intl 2:11–20. https://doi.org/10.3109/07388550903524243
Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344. https://doi.org/10.1046/j.1365-3040.2001.00778.x
Ali AA, El Saved HM, Abdalliah OM, Steglich W (1986) Oxocrinine and other alkaloids from Crinum americanum. Phytochem 25:2399–2401. https://doi.org/10.1016/S0031-9422(00)81704-5
Asada K (1996) Radical production and scavenging in the chloroplasts. In: Baker NR (ed) Photosynthesis and the environment. Advances in photosynthesis and respiration. Springer, Dordrecht, pp 123–150
Asaeda T, Rahman M, Liping X, Schoelynck J (2022) Hydrogen Peroxide variation patterns as abiotic stress responses of Egeria densa. Front Plant Sci 13:855477. https://doi.org/10.3389/fpls.2022.855477
Asaeda T, Rashid MH, Liping X, Vamsi-Krishna L, Barnuevo A, Takeuchi C, Rahman M (2023) The distribution of submerged macrophytes in response to intense solar radiation and salinity reveals hydrogen peroxide as an abiotic stress indicator. Sci Rep 13:4548. https://doi.org/10.21203/rs.3.rs-2058053/v1
Atia A, Debez A, Rabhi M et al (2019) Salt tolerance and potential uses for saline agriculture of halophytes from the Poaceae. In: Gul B, Böer B, Khan M, Clüsener-Godt M, Hameed A (eds) Sabkha ecosystems. Tasks for vegetation science. Springer, Cham, pp 223–237
Barko JW, Smart RM (1986) Sediment-related mechanisms of growth limitation on submersed macrophytes. Ecology 6:1328–2134
Barreiros ALBS, David JM, David JP (2006) Oxidative stress: relations between the formation of reactive species and the organism’s defense. Quim Nova 29:113–123. https://doi.org/10.1590/S0100-40422006000100021
Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:1–69. https://doi.org/10.1111/j.1469-8137.2007.01996.x
Candido LP, Varela RM, Torres A, Molinillo JM, Gualtieri SC, Macias FA (2016) Evaluation of the allelopathic potential of leaf, stem, and root extracts of Ocotea pulchella Nees et Mart. Chem Biodivers 13(8):1058–1067. https://doi.org/10.1002/cbdv.201500501
Carreiras J, Pérez-Romero JA, Mateos-Naranjo E, Redondo-Gómez S, Matos AR, Cacador I, Duarte B (2020) The effect of heavy metal contamination pre-conditioning in the heat stress tolerance of native and invasive Mediterranean halophytes. Ecol Indic 111:1–15. https://doi.org/10.1016/j.ecolind.2019.106045
Carvalho RF, Quecini V, Peres LEP (2010) Hormonal modulation of photomorphogenesis-controlled anthocyanin accumulation in tomato (Solanum lycopersicum L. cv Micro-Tom) hypocotyls: physiological and genetic studies. Plant Sci 178:258–264. https://doi.org/10.1016/j.plantsci.2010.01.013
Cavalieri AJ, Huang AH (1981) Accumulation of proline and glycinebetaine in Spartina alterniflora Loisel. in response to NaCl and nitrogen in the marsh. Oecologia 49:224–228. https://doi.org/10.1007/BF00349192
Céccoli G, Ramos J, Pilatti V, Dellaferrera I, Tivano JC (2015) Salt glands in the Poaceae family and their relationship to salinity tolerance. Bot Rev 81:162–178. https://doi.org/10.1007/s12229-015-9153-7
Černý M, Habánová H, Berka M, Luklová M, Brzobohatý B (2018) Hydrogen peroxide: Its role in plant biology and crosstalk with signalling networks. Int J Mol Sci 19:1–30. https://doi.org/10.3390/ijms19092812
Chambers PA, Prepas EE, Bothwell ML, Hamilton HR (1989) Roots versus shoots in nutrient uptake by aquatic macrophytes in flowing waters. Can J of Fish Aquat Sci 46:435–439. https://doi.org/10.1139/f89-058
Chen X, Cheng X, Zhu H, Bañuelos G, Shutes B, Wu H (2019) Influence of salt stress on propagation, growth and nutrient uptake of typical aquatic plant species. Nord J Bot 37:1–12
Courtney AJ, Xu J, Xu Y (2016) Responses of growth, antioxidants and gene expression in smooth cordgrass (Spartina alterniflora) to various levels of salinity. Plant Physiol Biochem 99:162–170. https://doi.org/10.1016/j.plaphy.2015.12.016
Crain CM (2007) Shifting nutrient limitation and eutrophication effects in marsh vegetation across estuarine salinity gradients. Estuaries Coasts 30:26–34. https://doi.org/10.1007/BF02782964
Crain CM, Silliman BR, Bertness SL, Bertness MD (2004) Physical and biotic drivers of plant distribution across estuarine salinity gradients. Ecology 85:2539–2549. https://doi.org/10.1890/03-0745
Crawford RMM, Braendle R (1996) Oxygen deprivation stress in a changing environment. J Exp Bot 47:145–159. https://doi.org/10.1093/jxb/47.2.145
del-Rio LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837. https://doi.org/10.1093/jxb/erv099
Embrapa (2015) Empresa brasileira de pesquisa agropecuária. Banco de Dados Climáticos do Brasil [Brazil’s Climate Database]. http://www.bdclima.cnpm.embrapa.br/resultados/?UF=sp. Accessed 12 Aug 2021
Esteves BS, Suzuki MS (2009) Efeito da salinidade sobre as plantas. Oecol Aust 12:662–679. https://doi.org/10.4257/oeco.2008.1204.06
Eyre D, Balls P (1999) A comparative study of nutrient behavior along the gradient of tropical and temperate estuaries. Estuaries 22:313–326. https://doi.org/10.2307/1352987
Ferrat L, Pergent-Martini C, Roméo M (2003) Assessment of the use of biomarkers in aquatic plants for the evaluation of environmental quality: application to seagrasses. Aquat Toxicol 65:187–204. https://doi.org/10.1016/S0166-445X(03)00133-4
Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431. https://doi.org/10.1093/aob/mcu217
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18. https://doi.org/10.1104/pp.110.167569
Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474:877–883. https://doi.org/10.1042/BCJ20160814
Garg N, Manchanda G (2009) ROS generation in plants: Boon or bane? Plant Biosyst 143:81–96. https://doi.org/10.1080/11263500802633626
Gil L, Capó X, Tejada S et al (2020) Salt variation induces oxidative stress response in aquatic macrophytes: The case of the Eurasian water-milfoil Myriophyllum spicatum L. (Saxifragales: Haloragaceae). Estuar Coast Shelf Sci 239:1–6. https://doi.org/10.1016/j.ecss.2020.106756
Gil R, Bautista I, Boscaiu M, Lidón A, Wankhade S, Sánchez H, Llinares J, Vicente O (2014) Responses of five Mediterranean halophytes to seasonal changes in environmental conditions. AoB Plants 6:plu049. https://doi.org/10.1093/aobpla/plu049
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Golterman HL, Clymo RS, Ohnstad MAM (1978) Methods for physical and chemical analysis of freshwaters. Blackwell Scientific Publications, Oxford
Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494. https://doi.org/10.1071/FP05016
Gratão PL, Monteiro CC, Carvalho RF, Tezotto T, Piotto FA, Peres LEP, Azevedo RA (2012) Biochemical dissection of diageotropica and Never ripe tomato mutants to Cd-stressful conditions. Plant Physiol Biochem 56:79–96. https://doi.org/10.1016/j.plaphy.2012.04.009
Guo H, Pennings SC (2012) Mechanisms mediating plant distributions across estuarine landscapes in a low-latitude tidal estuary. Ecology 93:90–100. https://doi.org/10.1890/11-0487.1
Hafsi C, Romero-Puertas MC, Gupta DK, del Río LA, Sandalio LM, Abdelly C (2010) Moderate salinity enhances the antioxidative response in the halophyte Hordeum maritimum L. under potassium deficiency. Environ Exp Bot 69:129–136. https://doi.org/10.1016/J.ENVEXPBOT.2010.04.008
Halliwel B, Gutteridge JM (2015) Free radicals in biology and medicine. Oxford Academic, Oxford
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:2141–2145. https://doi.org/10.1016/0003-9861(68)90654-1
Hessini K, Hamed KB, Gandour M, Mejri M, Abdelly C, Cruz C (2013) Ammonium nutrition in the halophyte Spartina alterniflora under salt stress: evidence for a priming effect of ammonium? Plant Soil 370:163–173. https://doi.org/10.1007/s11104-013-1616-1
Hippler FWR, Boaretto RM, Quaggio JA, Azevedo RA, Mattos D (2015) Towards soil management with Zn and Mn: Estimates of fertilisation efficacy of Citrus trees. Ann Appl Biol 166:484–495. https://doi.org/10.1111/aab.12197
Houle G, Morel L, Reynolds CE, Siegel J (2001) The effect of salinity on different developmental stages of an endemic annual plant, Aster laurentianus (Asteraceae). Am J Bot 88:62–67. https://doi.org/10.2307/2657127
Hu Y, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. J Soil Sci Plant Nutr 168:541–549. https://doi.org/10.1002/jpln.200420516
Hussain T, Koyro HW, Huchzermeyer B, Khan MA (2015) Eco-physiological adaptations of Panicum antidotale to hyperosmotic salinity: Water and ion relations and anti-oxidant feedback. Flora 212:30–37. https://doi.org/10.1016/j.flora.2015.02.006
Koyro HW, Ahmad P, Prasad MNV (2012) abiotic stress responses in plants: an overview. In: Ahmad P, Prasad M (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 1–28
Koyro HW, Hussain T, Huchzermeyer B, Khan MA (2013) Photosynthetic and growth responses of a perennial halophytic grass Panicum turgidum to increasing NaCl concentrations. Environ Exp Bot 91:22–29. https://doi.org/10.1016/j.envexpbot.2013.02.007
Li Y, Niu W, Cao X et al. (2019) Effect of soil aeration on root morphology and photosynthetic characteristics of potted tomato plants (Solanum lycopersicum) at different NaCl salinity levels. BMC Plant Biol 19:1–15. https://doi.org/10.1186/s12870-019-1927-3
Mackereth FJ, Heron HJ, Talling JF (1978) Water analysis: some revised methods for limnologists. Freshwater Biological Association, London
Maricle BR, Cobos DR, Campbell CS (2007) Biophysical and morphological leaf adaptations to drought and salinity in salt marsh grasses. Environ Exp Bot 60(3):458–467. https://doi.org/10.1016/j.envexpbot.2007.01.001
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Neves JP, Ferreira LF, Simões MP, Gazarini LC (2007) Primary production and nutrient content in two salt marsh species, Atriplex portulacoides L. and Limoniastrum monopetalum L., in southern Portugal. Estuaries Coast 30:459–468
Nunes LSC, Camargo AFM (2017) A simple non-destructive method for estimating aboveground biomass of emergent aquatic macrophytes. Acta Limnol Bras 29:1–9. https://doi.org/10.1590/S2179-975X6416
Nunes LSC, Camargo AFM (2018) Do interspecific competition and salinity explain plant zonation in a tropical estuary? Hydrobiologia 812:67–77. https://doi.org/10.1007/s10750-016-2821-8
Nunes LSC, Camargo AFM (2020) Effects of salinity on growth, competitive interaction and total nitrogen content of two estuarine macrophyte species cultivated on artificial substrate. Aquat Ecol 54:973–983. https://doi.org/10.1007/s10452-020-09787-5
Nunes LSC, Camargo AFM (2022) Arrival order and aquatic macrophyte community organization in a tropical estuary. Oecol Aust 26:286–299. https://doi.org/10.4257/oeco.2022.2602.15
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349. https://doi.org/10.1016/j.ecoenv.2004.06.010
Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22:4056–4075. https://doi.org/10.1007/s11356-014-3739-1
Pezeshki S, DeLaune R (1995) Variations in response of two US Gulf Coast populations of Spartina alterniflora to hypersalinity. J Coast Res 11:89–95
Ribeiro JPN, Matsumoto RS, Takao LK, Voltarelli VM, Lima MIS (2009) Efeitos alelopáticos de extratos aquosos de Crinum americanum L. Rev Bras Bot 32:183–188. https://doi.org/10.1590/S0100-84042009000100018
Ribeiro JPN, Matsumoto RS, Takao LK, Peret AC, Lima MIS (2011) Spatial distribution of Crinum americanum L. in tropical blind estuary: hydrologic, edaphic and biotic drivers. Environ Exp Bot 71:287–291. https://doi.org/10.1016/j.envexpbot.2010.12.011
Rogers ME, Grieve CM, Shannon MC (2003) Plant growth and ion relations in lucerne (Medicago sativa L.) in response to the combined effects of NaCl and P. Plant Soil 253:187–194. https://doi.org/10.1023/A:1024543215015
Santini R, Lima JP, Gratão PL, Camargo AFM (2021) Evaluation of growth and oxidative stress as indicative of salinity tolerance by the invasive tropical aquatic macrophyte tanner grass. Hydrobiologia 849:1261–1271. https://doi.org/10.1007/s10750-021-04787-4
Schaeffer-Novelli Y, Cintrón-Molero G, Adaime RR, Camargo TM (1990) Variability of mangrove ecosystems along the Brazilian coast. Estuaries 13:204–218
Shao D, Zhou W, Bouma TJ, Asaeda T, Wang ZB, Liu X et al (2020) Physiological and biochemical responses of the salt-marsh plant Spartina alterniflora to long-term wave exposure. Ann Bot 125:291–300. https://doi.org/10.1093/aob/mcz067
Tessler MG, Goya SC, Yoshikawa PS, Hurtado SN (2006) Erosão de progradação do litoral brasileiro: São Paulo. In: Ministério do Meio Ambiente. Erosão de progradação do litoral brasileiro. MMA, Brasília
Tewari RK, Kumar P, Sharma PN (2007) Oxidative stress and antioxidant responses in young leaves of mulberry plants grown under nitrogen, phosphorus or potassium deficiency. J Integr Plant Biol 49:313–322. https://doi.org/10.1111/j.1744-7909.2007.00358.x
Tewari RK, Yadav N, Gupta R, Kumar P (2021) Oxidative stress under macronutrient deficiency in plants. Soil Sci Plant Nutr 21:832–859. https://doi.org/10.1007/s42729-020-00405-9
Thiébaut G, Tarayre M, Rodríguez-Pérez H (2019) Allelopathic effects of native versus invasive plants on one major invader. Front Plant Sci 10:854. https://doi.org/10.3389/fpls.2019.00854
Uddin MD, Juraimi AS (2013) Salinity tolerance turfgrass: history and prospects. Sci World J 2013:1–6. https://doi.org/10.1155/2013/409413
Wieski K, Guo H, Craft CB, Pennings SC (2010) Ecosystem functions of tidal fresh, brackish, and salt marshes on the Georgia coast. Estuaries Coast 33:161–169. https://doi.org/10.1007/s12237-009-9230-4
Willadino L, Camara TR (2010) Tolerância das plantas à salinidade: aspectos fisiológicos e bioquímicos. Enciclopédia Biosfera 6:1–23
Wolanski E, Elliott M (2015) Estuarine ecohydrology. Elsevier, Amsterdam
Yu J, Chen S, Zhao Q, Wang T, Yang C, Diaz C, Sun G, Dai S (2011) Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J Proteome Res 10:3852–3870. https://doi.org/10.1021/pr101102p
Acknowledgements
We thank Carlos Fernando Sanches for assistance with the field work; Sonia Maria R. Carregari for assistance with laboratory analysis; and Baltasar F. Garcia Neto, Dr., for assistance with statistical analyses.
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This work was supported by the Improvement of Higher Education Personnel—Brazil (CAPES)—Finance Code 001.
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RS, PLG and AFMC conceived of the presented idea; RS and LSCN collected the field data; RS and MVC conduced the laboratory analysis; and RS, MVC, LSCN, PLG and AFMC discussed the results and wrote the manuscript.
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Santini, R., Vantini Checchio, M., Correia Nunes, L.S. et al. Do salinity, total nitrogen and phosphorus variation induce oxidative stress in emergent macrophytes along a tropical estuary?. Aquat Ecol 58, 399–409 (2024). https://doi.org/10.1007/s10452-023-10079-x
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DOI: https://doi.org/10.1007/s10452-023-10079-x