Oxidative Stress, Nutritional Disorders, and Gas Exchange in Lettuce Plants Subjected to Two Selenium Sources

Abstract

Selenium (Se) is microelement beneficial to plants and essential to animals and humans. Supply of Se shows positive effects on plant growth, but high concentrations affect its growth. This study is based on the hypothesis that nutritional disorder and oxidative stress induced by toxic levels of selenium maintain a close correlation with inhibition of photosynthesis net and reduced growth in lettuce plants. In this study, we investigated impact of Se toxicity on gas exchange, oxidative stress indicators, nutritional status, and growth of lettuce plants. Two sources and ten selenium concentrations were evaluated in lettuce according to a completely randomized experimental design in a factorial scheme with two selenium sources (selenite and selenate) and ten selenium concentration (0, 2, 4, 6, 8, 16, 32, 64, 96, 128 μM). Results show that reduction in leaf area and shoot dry matter was high when selenite was supplied to plants. It was achieved due to oxidative stress and nutritional disorder that affected photosynthesis, which resulted in low photosynthesis net. These results were reinforced by strong correlation of photosynthesis with essential nutrient contents and indicators of oxidative stress in plants treated with selenite. However, photosynthesis net was increased with 8 μM concentration of selenate. Lettuce growth was reduced due to oxidative stress and nutritional disorder. The results of this study contribute to clarifying negative modulation of photosynthesis net by higher selenate or selenite concentrations in lettuce plants through growth analysis, nutritional composition, oxidative stress indicators, and gas exchange. The strong or very strong negative correlation between photosynthesis net and oxidative stress indicators (superoxide, peroxide and malondialdehyde), photosynthesis net and chlorophyll a, photosynthesis net, and selenium content support the hypothesis of this study in which selenium-induced damage to the photosynthetic apparatus reduces the growth of lettuce. These results show new evidence on the mechanism of action of selenium toxicity on the photosynthetic machinery of lettuce plants. In addition, the results found show that lettuce plants respond differently to the source and concentration of selenium, with symptoms of toxicity manifesting even in the short exposure time of lettuce plants.

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Data Availability

Data are available upon request to corresponding author.

Abbreviations

B:

Boron

Ca :

Calcium

Chl a:

Chlorophyll a

Chl b:

Chlorophyll b

Ci/Ca:

Relation between internal and external CO2

Cu:

Copper

E:

Transpiration

Fe:

Iron

Fv/Fm:

Maximal quantum yield of PSII photochemistry

gs:

Stomatal conductance

H2O2 :

Hydrogen peroxide

K:

Potassium

LA:

Leaf area

MDA:

Malondialdehyde

Mg:

Magnesium

Mn:

Manganese

N:

Nitrogen

O2 :

Superoxide

P:

Phosphorous

Pn:

Photosynthesis net

RDM:

Root dry matter

RFM:

Root fresh matter

r:

Correlation coefficient

S:

Sulfur

SeO42−:

Selenate

SeO32−:

Selenite

Se–C:

Selenium concentration

Se–S:

Selenium source

Se-C × Se-S:

Selenium concentration and source interaction

SDM:

Shoot dry matter

SFM:

Shoot fresh matter

Zn:

Zinc

References

  1. Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signal Behav 5:369–374

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  2. 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

    CAS  Article  Google Scholar 

  3. Alves LT, Monteiro CC, Carvalho RF, Ribeiro PC, Tezotto T, Azevedo RA, Gratão PL (2017) Cadmium stress related to root-to-shoot communication depends on ethylene and auxin in tomato plants. Environ Exp Bot 134:102–115. https://doi.org/10.1016/j.envexpbot.2016.11.008

    CAS  Article  Google Scholar 

  4. Andrade FR, Silva GN, Guimarães KC, Barreto HBF, Souza KRD, Guilherme LRG, Faquin V, Reis AR (2018) Selenium protects rice plants from water deficit stress. Ecotoxicol Environ Saf 164:562–570

    CAS  PubMed  Article  Google Scholar 

  5. Barbosa JC, Maldonado Júnior W (2009) Software AgroEstat: Sistema de análises estatísticas de ensaios agronômicos. Universidade Estadual Paulista, Faculdade de Ciências Agrárias e Veterinárias, Câmpus de Jaboticabal, Brasil

  6. Bataglia OC, Furlani AMC, Teixeira JPF, Furlani PR, Gallo JR (1983) Métodos de análise química de plantas. Campinas: Instituto Agronômico. 48p. (Boletim Técnico, 78)

  7. Berry MJ, Banu L, Larsen PR (1991) Type I iodothyronine deiodinase is a selenocysteine-containing enzyme. Nature 349:438–440

    CAS  PubMed  Article  Google Scholar 

  8. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR (2002) Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 23:38–89. https://doi.org/10.1210/edrv.23.1.0455

    CAS  PubMed  Article  Google Scholar 

  9. Bo L, Zhong-hua B, Qi-hang Y, Jun W, Rui-feng C, Kun L, Wen-ke L, Yi Z, Hui F, Yun-xin T (2018) The positive function of Se supplementation on reducing nitrate accumulation in hydroponic lettuce (Lactuca sativa L.). J Integr Agric 17:837–846. https://doi.org/10.1016/S2095-3119(17)61759-3

    Article  Google Scholar 

  10. Bolhàr-Nordenkampf HR, Long SP, Baker NR, Örquist G, Schreiber U, Lechner EG (1989) Chlorophyll fluorescence as probe of the photosynthetic competence of leaves in the field: a review of current instrument. Funct Ecol 3:497–514

    Article  Google Scholar 

  11. Davey MW, Stals E, Panis B, Keulemans JK, Swennen RL (2005) High-throughput determination of malondialdehyde in plant tissues. Anal Biochem 347:201–207. https://doi.org/10.1016/j.ab.2005.09.041

    CAS  PubMed  Article  Google Scholar 

  12. Diao M, Ma L, Wang J, Cui J, Fu A, Liu H (2014) Selenium Promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast antioxidant defense system. J Plant Growth Regul 33:671–682. https://doi.org/10.1007/s00344-014-9416-2

  13. Djanaguiraman M, Devi DD, Shanker AK, Sheeba JA, Bangarusamy U (2005) Selenium - an antioxidative protectant in soybean during senescence. Plant Soil 272:77–86. https://doi.org/10.1007/s11104-004-4039-1

    CAS  Article  Google Scholar 

  14. Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of phytophtorhora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357. https://doi.org/10.1016/0048-4059(83)90019-X

    CAS  Article  Google Scholar 

  15. Durán P, Viscardi S, Acuña JJ, Cornejo P, Azcón R, Mora ML (2018) Endophytic selenobacteria and arbuscular mycorrhizal fungus for selenium biofortification and Gaeumannomyces graminis biocontrol. J Soil Sci Plant Nutr 18:1021–1035

    Google Scholar 

  16. Garousi F, Kovács B, Andrási D, Veres S (2016) Selenium phytoaccumulation by sunflower plants under hydroponic conditions. Water Air Soil Pollut 227:382. https://doi.org/10.1007/s11270-016-3087-5

    CAS  Article  Google Scholar 

  17. Gigolashvili T, Kopriva S (2014) Transporters in plant sulphur metabolism. Front Plant Sci 5:422. https://doi.org/10.3389/fpls.2014.00442

    Article  Google Scholar 

  18. Gupta M, Gupta S (2017) An overview of selenium uptake, metabolism, and toxicity in plants. Front Plant Sci 7:2074. https://doi.org/10.3389/fpls.2016.02074

  19. Han D, Li X, Xiong S, Tu S, Chen Z, Li J, Xie Z (2013) Selenium uptake, speciation and stressed response of Nicotiana tabacum L. Environ Exp Bot 95:6–14. https://doi.org/10.1016/j.envexpbot.2013.07.001

    CAS  Article  Google Scholar 

  20. Hawrylak-Nowak B (2008) Effect of selenium on selected macronutrients in maize plants. J Elem 13:513–519

    Google Scholar 

  21. Hawrylak-Nowak B, Matraszek R, Pogorzelec M (2015) The dual effects of two inorganic selenium forms on the growth, selected physiological parameters and macronutrientes accumulation in cucumber plants. Acta Physiol Plant 37:41. https://doi.org/10.1007/s11738-015-1788-9

    CAS  Article  Google Scholar 

  22. He J, Quin L, Lee SK (2013) Root-zone CO2 and root-zone temperature effects on photosynthesis and nitrogen metabolism of aeroponically grown lettuce (Lactuca sativa L.) in the tropics. Photosynthetica 51:330–340. https://doi.org/10.1007/s11099-013-0030-5

    CAS  Article  Google Scholar 

  23. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1

    CAS  PubMed  Article  Google Scholar 

  24. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station, Circular-347

  25. Hsu F-C, Wirtz M, Heppel SC, Bogs J, Krämer U, Khan MS, Bub A, Hell R, Rausch T (2011) Generation of Se-fortified broccoli as functional food: impact of Se fertilization on S metabolism. Plant Cell Environ 34:192–207. https://doi.org/10.1111/j.1365-3040.2010.02235.x

    CAS  PubMed  Article  Google Scholar 

  26. Jiang C, Zu C, Shen J, Shao F, Li T (2015) Effects of selenium on the growth and photosynthetic characteristics of flue-cured tobacco (Nicotiana tabacum L.). Acta Soc Bot Pol 84:71–77. https://doi.org/10.5586/asbp.2015.006

    CAS  Article  Google Scholar 

  27. Köhrle J, Jakob F, Contempre B, Dumont JE (2005) Selenium, the thyroid, and the endocrine system. Endocr Rev 26:944–984. https://doi.org/10.1210/er.2001-0034

    CAS  PubMed  Article  Google Scholar 

  28. Kostopoulou P, Parissi ZM, Abraham EM, Karatassiou M, Kyriazopoulos AP, Barbayiannis N (2015) Effect of selenium on mineral content and nutritive value of Melilotus officinalis l. J Plant Nutr 38(1849–1861):2015

    Google Scholar 

  29. Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB (2014) Histochemical detection of superoxide and H2O2 accumulation in brassica juncea seedlings. Biol-protocol 4:1–5. https://doi.org/10.21769/BioProtoc.1108

    Article  Google Scholar 

  30. Lehotai N, Lyubenova L, Schröder P, Feigl G, Ördög A, Szilágyi K, Erdei L, Kolbert Z (2016) Nitro-oxidative stress contributes to selenite toxicity in pea (Pisum sativum L). Plant Soil 400:107–122. https://doi.org/10.1007/s11104-015-2716-x

    CAS  Article  Google Scholar 

  31. Li HF, McGrath SP, Zhao FJ (2008) Selenium uptake, translocation and speciationin wheat supplied with selenate or selenite. New Phytol 178:92–102. https://doi.org/10.1111/j.1469-8137.2007.02343.x

    CAS  PubMed  Article  Google Scholar 

  32. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigment photosynthetic biomembranes. Methods Enzymol 148:362–385. https://doi.org/10.1016/0076-6879(87)48036-1

    Article  Google Scholar 

  33. Łukaszewicz S, Politycka B, Smoleń S (2019) Accumulation of selected macronutrients and tolerance towards selenium of garden pea treated with selenite and selenate. J Elem 1:245–256. https://doi.org/10.5601/jelem.2018.23.1.1650

    Article  Google Scholar 

  34. Maathuis FJM (2009) Physiological functions of mineral macronutrientes. Curr Opin Plant Biol 12:250–258. https://doi.org/10.1016/j.pbi.2009.04.003

    CAS  PubMed  Article  Google Scholar 

  35. Marschener H (1995) Mineral nutrition of higher plants, ed. Horst Marschner, 2nd edn. Academic Press, San Diego

    Google Scholar 

  36. Matraszek R, Hawrylak-Nowak B (2009) Macronutrients accumulation in useable parts of lettuce as affected by nickel and Se concentrations in nutrient solution. Fresenius Environ Bull 18:1059–1065

    CAS  Google Scholar 

  37. Medeiros CD, Ferreira Neto JRC, Oliveira MT, Rivas R, Pandolfi V, Kido EA, Baldani JI, Santos MG (2014) Photosynthesis, antioxidant activities and transcriptional responses in two sugarcane (Saccharum officinarum L.) cultivars under salt stress. Acta Physiol Plant 36:447–459. https://doi.org/10.1007/s11738-013-1425-4

    CAS  Article  Google Scholar 

  38. Miller G, Suzuki N, Ciftci-Yilmaz SRM (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x

    CAS  PubMed  Article  Google Scholar 

  39. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/S1360-1385(02)02312-9

    CAS  PubMed  Article  Google Scholar 

  40. Mulabagal V, Ngouajio M, Nair A, Zhang Y, Gottumukkala AL, Nair MG (2010) In vitro evaluation of red and green lettuce (Lactuca sativa) for functional food properties. Food Chem 118:300–306

    CAS  Article  Google Scholar 

  41. Narváez-Ortiz WA, Martínez-Hernández M, Fuentes-Lara LO, Benavides-Mendoza A, Valenzuela-García JR, González-Fuentes JÁ (2018) Effect of selenium application on mineral macro- and micronutrients and antioxidant status in strawberries. J Appl Bot Food Qual 91:321–331

    Google Scholar 

  42. Niki E (2008) Lipid peroxidation products as oxidative stress biomarkers. BioFactors 34:171–180

    CAS  PubMed  Article  Google Scholar 

  43. Padmaja K, Prasad DD, Prasad AR (1990) Selenium as a novel regulator of porphyrin biosynthesis in germinating seedlings of mung bean (Phaseolus vulgaris). Biochem Int 22:441–446

    CAS  PubMed  Google Scholar 

  44. Pílon-Smits EAH (2015) Selenium in plants. In: Luettge U (ed) Springer - Verlag. Gemany, Heidelberg, pp 93–107

    Google Scholar 

  45. Pílon-Smits EAH, Quinn CF, Tapken W, Malagoli M, Schiavon M (2009) Physiological functions of beneficial elements. Curr Opin Plant Biol 12:267–274

    PubMed  Article  Google Scholar 

  46. Ramos SJ, Faquin V, Guilherme LRG, Castro EM, Ávila FW, Carvalho GS, Bastos CEA, Oliveira C (2010) Selenium biofortification and antioxidant activity in lettuce plants fed with selenate and selenite. Plant Soil Environ 56:584–588

    CAS  Article  Google Scholar 

  47. Raij BV, Cantarella H, Quaggio JA, Furlani AMC (1997) Recomendações de adubação e calagem para o Estado de São Paulo. Instituto Agronômico/Fundação IAC, Campinas, 285p

    Google Scholar 

  48. Ribeiro DM, Júnior DDS, Cardoso FB, Martins AO, Silva WA, Nascimento VL, Araújo WL (2016) Growth inhibition by Se is associated with changes in primary metabolism and nutrient levels in Arabidopsis thaliana. Plant Cell Environ 39:2235–2246. https://doi.org/10.1111/pce.12783

    CAS  PubMed  Article  Google Scholar 

  49. Ríos JJ, Blasco B, Leyva R, Sanchez-Rodriguez E, Rubio-Wilhelmi MM, Romero L, Ruiz JM (2013) Nutritional balance changes in lettuce plant grown under different doses and forms of Se. J Plant Nutr 36:1344–1354. https://doi.org/10.1080/01904167.2013.790427

    CAS  Article  Google Scholar 

  50. Sabatino L, Ntatsi G, Iapichino G, D’Anna F, De Pasquale C (2019) Effect of selenium enrichment and type of application on yield, functional quality and mineral composition of curly endive grown in a hydroponic system. Agronomy 9:1–15

    CAS  Google Scholar 

  51. Saffaryazdi A, Lahouti M, Ganjeali A, Bayat H (2012) Impact of selenium supplementation on growth and selenium accumulation on spinach (Spinacia oleracea L.) plants. Not Bot Horti Agrobo 4:95–100

  52. Saldaña-Sánchez WD, León-Morales JM, López-Bibiano Y, Hernández-Hernández M, Langarica-Velázquez EC, García-Morales S (2019) Effect of V, Se, and Ce on growth, photosynthetic pigments, and total phenol content of tomato and pepper seedlings. J Soil Sci Plant Nutr 19:678–688. https://doi.org/10.1007/s42729-019-00068-1

    CAS  Article  Google Scholar 

  53. Saleem MF, Kamal MA, Shahid M, Saleem A, Shakeel A, Anjum AS (2020) Exogenous selenium-instigated physiochemical transformations impart terminal heat tolerance in Bt cotton. J Soil Sci Plant Nutr 20:274–283

    CAS  Article  Google Scholar 

  54. Schiavon M, Pilon M, Malagoli M, Pílon-Smits EAH (2015) Exploring the importance of sulfate transporters and ATP sulphurylases for selenium hyperaccumulation - acomparison of Stanleya pinnata and Brassica juncea (Brassicaceae). Front Plant Sci 6:1–13. https://doi.org/10.3389/fpls.2015.00002

    Article  Google Scholar 

  55. Schober P, Boer C, Schwarter LA (2018) Correlation coefficients: appropriate use and interpretation. Anesth Analg 126:1763–1768. https://doi.org/10.1213/ANE.0000000000002864

    PubMed  Article  Google Scholar 

  56. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 212:1–26. https://doi.org/10.1155/2012/217037

    CAS  Article  Google Scholar 

  57. Sieprawska A, Kornaś A, Filek M (2015) Involvement of selenium in protective mechanisms of plants under environmental stress conditions – review. Acta Biol Cracov Bot 1:9–20. https://doi.org/10.1515/abcsb-2015-0014

  58. Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth Res 86:373–389. https://doi.org/10.1007/s11120-005-5222-9

    CAS  PubMed  Article  Google Scholar 

  59. Spallholz JE (1994) On the nature of Se toxicity and carcinostatic activity. Free Radic Biol Med 17:45–64. https://doi.org/10.1016/0891-5849(94)90007-8

    CAS  PubMed  Article  Google Scholar 

  60. Statwick J, Majestic BJ, Sher AA (2016) Characterization and benefits of selenium uptake by an Astragalus hyperaccumulator and a non-accumulator. Plant Soil 404:345–359. https://doi.org/10.1007/s11104-016-2842-0

    CAS  Article  Google Scholar 

  61. Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulfate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171–182. https://doi.org/10.1046/j.1365-313x.2000.00768.x

    CAS  PubMed  Article  Google Scholar 

  62. Taulavuori E, Hellström EK, Taulavuori K, Laine K (2001) Comparison of two methods used to analyse lipid peroxidation from Vaccinium myrtillus (L.) during snow removal, reacclimation and cold acclimation. J Exp Bot 52:2375–2380. https://doi.org/10.1093/jexbot/52.365.2375

    CAS  PubMed  Article  Google Scholar 

  63. Terry N, Zayed AM, de Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol 51:401–432. https://doi.org/10.1093/aob/mcv180

    CAS  Article  Google Scholar 

  64. Tezotto T, Favarin JL, Neto AP, Gratão PL, Azevedo RA, Mazzafera P (2013) Simple procedure for nutrient analysis of coffee plant with energy dispersive X-ray fluorescence spectrometry (EDXRF). Sci Agric 70:263–267 https://doi.org/10.1590/S0103-90162013000400007

    CAS  Article  Google Scholar 

  65. Tian M, Hui M, Thannhauser TW, Pan S, Li L (2017) Selenium-induced toxicity is counteracted by sulfur in broccoli (Brassica oleracea L. var. italica). Front Plant Sci 8:1425. https://doi.org/10.3389/fpls.2017.01425

  66. Van Hoewyk D (2013) A tale of two toxicities: malformed selenoproteins and oxidative stress both contribute to Se stress in plants. Ann Bot 112:965–972. https://doi.org/10.1093/aob/mct163

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  67. Wallenberg M, Olm E, Hebert C, Björnstedt M, Fernandes AP (2010) Selenium compounds are substrates for glutaredoxins: a novel pathway for Se metabolism and a potential mechanism for Se-mediated cytotoxicity. Biochem J 429:85–93. https://doi.org/10.1042/BJ20100368

    CAS  PubMed  Article  Google Scholar 

  68. White PJ (2016) Se accumulation by plants. Ann Bot 117:217–235. https://doi.org/10.1093/2Faob/2Fmcv180

    CAS  PubMed  Article  Google Scholar 

  69. White PJ, Bowen HC, Parmaguru P, Fritz M, Spracklen WP, Spiby RE, Meacham MC, Mead A, Harriman M, Trueman LJ, Smith BM, Thomas B, Broadley MR (2004) Interactions between selenium and sulphur nutrition in Arabidopsis thaliana. J Exp Bot 55:1927–1937. https://doi.org/10.1093/jxb/erh192

    CAS  PubMed  Article  Google Scholar 

  70. Zayed A, Lytle CM, Terry N (1998) Accumulation and volatilization of different chemical species of selenium by plants. Planta 206:284–292

    CAS  Article  Google Scholar 

  71. Zahedi SM, Abdelrahman M, Hosseini MS, Hoveizeh NFH, Tran LSP (2019) Alleviation of the effect of salinity on growth and yield of strawberry by foliar spray of selenium-nanoparticles. Environ Pollut 253:246–258. https://doi.org/10.1016/j.envpol.2019.04.078

    CAS  PubMed  Article  Google Scholar 

  72. Zhang M, Tang S, Huang X, Zhang F, Pang Y, Huang Q, Yi Q (2014) Selenium uptake, dynamic changes in se content and its influence on photosynthesis and chlorophyll fluorescence in rice (Oryza sativa L.). Environ Exp Bot 107:39–45. https://doi.org/10.1016/j.envexpbot.2014.05.005

    CAS  Article  Google Scholar 

  73. Zhu YG, Pílon-Smits EAH, Zhao FJ, Williams PN, Meharg AA (2009) Selenium in higher plants: understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci 14:436–442. https://doi.org/10.1016/j.tplants.2009.06.006

    CAS  PubMed  Article  Google Scholar 

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Acknowledgments

This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), which granted a master’s degree scholarship to the first author.

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FJRC and RMP were advisor of this project and planning all phases of this research. FJRC and RLCF conducted experiment in greenhouse and performed physiological, biochemical, nutritional, and morphological determinations. PLG and TT performed Se nutritional determination.

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Correspondence to Flávio José Rodrigues Cruz.

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da Cruz Ferreira, R.L., de Mello Prado, R., de Souza Junior, J.P. et al. Oxidative Stress, Nutritional Disorders, and Gas Exchange in Lettuce Plants Subjected to Two Selenium Sources. J Soil Sci Plant Nutr 20, 1215–1228 (2020). https://doi.org/10.1007/s42729-020-00206-0

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Keywords

  • Se stress
  • selenate
  • selenite
  • toxicity
  • reactive oxygen species
  • photosynthesis