Selenium application influenced selenium biofortification and physiological traits in water-deficit common bean plants
Ruby Antonieta Vega Ravello
A B , Cynthia de Oliveira A , Josimar Lessa A , Lissa Vasconcellos Vilas Boas C , Evaristo Mauro de Castro C , Luiz Roberto Guimarães Guilherme A and Guilherme Lopes A D
+ Author Affiliations
- Author Affiliations
A Soil Science Department, Federal University of Lavras UFLA, Lavras, Minas Gerais State, 37200-900, Brazil.
B Soil Science Department, La Molina National Agrarian University – UNALM, La Molina 15024, Lima, Peru.
C Biology Department, Federal University of Lavras, Lavras, Minas Gerais State, 37200-900, Brazil.
D Corresponding author. Email: guilherme.lopes@ufla.br
Crop and Pasture Science - https://doi.org/10.1071/CP20519
Submitted: 23 December 2020 Accepted: 4 May 2021 Published online: 16 July 2021
Abstract
Agronomic biofortification with selenium (Se) maybe employed to improve the nutritional value of food crops while increasing the plant’s tolerance to water deficit conditions. Although not essential for plants, Se may increase plant tolerance to water stress by boosting plants’ defence system activity. This study aimed to enrich common bean grains with Se and alleviate water deficit effects on common bean by applying Se to plants growing under greenhouse. Selenium was applied to soil at 0, 0.25, 0.5, 1.0, and 2.0 mg kg–1, under irrigated and water-deficit conditions. Antioxidant enzyme activities (SOD, CAT, and APX), H2O2 content, gas exchange, and SPAD index were assessed in plant leaves, and Se and nutrient concentrations were determined in grains. Results showed that water deficit decreased photosynthetic rate, stomatal conductance, transpiration rate, and increased water use efficiency. Selenium did not influence SPAD index in leaves from pod formation to maturity stage but improved the plant defence system by decreasing H2O2 content. Increasing Se rates increased Se concentration in grains and leaves. At lower Se rates, mainly at 0.25 mg Se kg–1, under water deficit, the activities of SOD, CAT, and APX reached their maximum values, and H2O2 content was minimum without reducing biomass production and nutrients accumulation. The highest Se rate (2 mg kg–1) was detrimental, since it decreased biomass production and the plant defence system under water deficit. Conclusively, soil Se addition enriched common bean plants with Se and showed positive responses against water deficit when applied at lower rates.
Keywords: common bean, Phaseolus vulgaris, abiotic stress, functional agriculture, human-essential nutrient, gas exchange, relative chlorophyll content, Se, selenium, agronomic biofortification, plant-based foods.
References
Aggarwal M, Sharma S, Kaur N, Pathania D, Bhandhari K, Kaushal N, Kaur R, Singh K, Srivastava A, Nayyar H (2011) Exogenous proline application reduces phytotoxic effects of selenium by minimising oxidative stress and improves growth in bean (Phaseolus vulgaris L.) seedlings. Biological Trace Element Research 140, 354–367.| Exogenous proline application reduces phytotoxic effects of selenium by minimising oxidative stress and improves growth in bean (Phaseolus vulgaris L.) seedlings.Crossref | GoogleScholarGoogle Scholar | 20455031PubMed |
Ahmad N, Malagoli M, Wirtz M, Hell R (2016a) Drought stress in maize causes differential acclimation responses of glutathione and sulfur metabolism in leaves and roots. BMC Plant Biology 16, 247
| Drought stress in maize causes differential acclimation responses of glutathione and sulfur metabolism in leaves and roots.Crossref | GoogleScholarGoogle Scholar | 27829370PubMed |
Ahmad R, Waraich EA, Nawaz F, Ashraf MY, Khalid M (2016b) Selenium (Se) improves drought tolerance in crop plants – a myth or fact? Journal of the Science of Food and Agriculture 96, 372–380.
| Selenium (Se) improves drought tolerance in crop plants – a myth or fact?Crossref | GoogleScholarGoogle Scholar | 25906838PubMed |
Aissa N, Malagoli M, Radhouane L (2018) An approach to alleviate the impact of drought stress with selenium amendment. Iranian Journal of Science and Technology. Transaction A, Science 42, 283–288.
| An approach to alleviate the impact of drought stress with selenium amendment.Crossref | GoogleScholarGoogle Scholar |
Andrade FR, da Silva GN, Guimarães KC, Barreto HBF, de Souza KRD, Guilherme LRG, Faquin V, dos Reis AR (2018) Selenium protects rice plants from water deficit stress. Ecotoxicology and Environmental Safety 164, 562–570.
| Selenium protects rice plants from water deficit stress.Crossref | GoogleScholarGoogle Scholar | 30149355PubMed |
Aon (2017) Weather, Climate and Catastrophe Insight: 2017 Annual Report. Aon Benfield. (London, England). Available at: http://thoughtleadership.aon.com/Documents/20180124-ab-if-annual-companion-volume.pdf
Araujo AM, de Lima Lessa JH, de Lima FRD, Raymundo JF, Curi N, Guilherme LRG, Lopes G (2020) Adsorption of selenite in tropical soils as affected by soil management, ionic strength, and soil properties. Journal of Soil Science and Plant Nutrition 20, 139–148.
| Adsorption of selenite in tropical soils as affected by soil management, ionic strength, and soil properties.Crossref | GoogleScholarGoogle Scholar |
Ashraf MA, Akbar A, Parveen A, Rasheed R, Hussain I, Iqbal M (2018) Phenological application of selenium differentially improves growth, oxidative defense and ion homeostasis in maize under salinity stress. Plant Physiology and Biochemistry 123, 268–280.
| Phenological application of selenium differentially improves growth, oxidative defense and ion homeostasis in maize under salinity stress.Crossref | GoogleScholarGoogle Scholar | 29275208PubMed |
Biemelt S, Keetman U, Albrecht G (1998) Re-Aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiology 116, 651–658.
| Re-Aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 9490765PubMed |
Bocchini M, D’Amato R, Ciancaleoni S, Fontanella MC, Palmerini CA, Beone GM, Onofri A, Negri V, Marconi G, Albertini E, Businelli D (2018) Soil selenium (Se) biofortification changes the physiological, biochemical and epigenetic responses to water stress in Zea mays L. by inducing a higher drought tolerance. Frontiers in Plant Science 9, 389
| Soil selenium (Se) biofortification changes the physiological, biochemical and epigenetic responses to water stress in Zea mays L. by inducing a higher drought tolerance.Crossref | GoogleScholarGoogle Scholar | 29636765PubMed |
Boldrin PF, Faquin V, Ramos SJ, Boldrin KVF, Ávila FW, Guilherme LRG (2013) Soil and foliar application of selenium in rice biofortification. Journal of Food Composition and Analysis 31, 238–244.
| Soil and foliar application of selenium in rice biofortification.Crossref | GoogleScholarGoogle Scholar |
Cabral Gouveia GC, Galindo FS, Dantas Bereta Lanza MG, Caroline da Rocha Silva A, Pereira de Brito Mateus M, Souza da Silva M, Rimoldi Tavanti RF, Tavanti TR, Lavres J, dos Reis AR (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,
| Selenium toxicity stress-induced phenotypical, biochemical and physiological responses in rice plants: characterization of symptoms and plant metabolic adjustment.Crossref | GoogleScholarGoogle Scholar | 32800251PubMed |
Calabrese EJ, Baldwin LA (2003) Inorganics and hormesis. Critical Reviews in Toxicology 33, 215–304.
| Inorganics and hormesis.Crossref | GoogleScholarGoogle Scholar | 12809427PubMed |
Cargnin A, Albrecht JC (2010) BRS Estilo: nova cultivar de feijoeiro comum do grupo comercial preto para o Distrito Federal. Embrapa Arroz e Feijão 6, 1–4.
Carvalho GS, Oliveira JR, Curi N, Schulze DG, Marques JJ (2019) Selenium and mercury in Brazilian Cerrado soils and their relationships with physical and chemical soil characteristics. Chemosphere 218, 412–415.
| Selenium and mercury in Brazilian Cerrado soils and their relationships with physical and chemical soil characteristics.Crossref | GoogleScholarGoogle Scholar | 30476773PubMed |
Cavalcante AG, Lemos LB, Meirelles FC, Cavalcante ACP, de Aquino LA (2020) Thermal sum and phenological descriptions of growth stages of the common bean according to the BBCH scale. Annals of Applied Biology 176, 342–349.
| Thermal sum and phenological descriptions of growth stages of the common bean according to the BBCH scale.Crossref | GoogleScholarGoogle Scholar |
Curi N, Silva SHG, Poggere GC, Menezes MD (2017) ‘Mapeamento de solos e magnetismo no campus da UFLA como traçadores ambientais.’ (Editora UFLA: Lavras)
Dai H, Wei S, Twardowska I (2020) Biofortification of soybean (Glycine max L.) with Se and Zn, and enhancing its physiological functions by spiking these elements to soil during flowering phase. The Science of the Total Environment 740, 139648
| Biofortification of soybean (Glycine max L.) with Se and Zn, and enhancing its physiological functions by spiking these elements to soil during flowering phase.Crossref | GoogleScholarGoogle Scholar | 32927528PubMed |
de Araújo SN (2020) Estratégias de aplicação de selênio para biofortificação do feijoeiro comum e seus efeitos residuais no capim Mombaça. Dissertação (mestrado acadêmico) - Universidade Federal de Lavras, Brazil.
de Figueiredo MA, Boldrin PF, Hart JJ, de Andrade MJB, Guilherme LRG, Glahn RP, Li L (2017) Zinc and selenium accumulation and their effect on iron bioavailability in common bean seeds. Plant Physiology and Biochemistry 111, 193–202.
| Zinc and selenium accumulation and their effect on iron bioavailability in common bean seeds.Crossref | GoogleScholarGoogle Scholar | 27940270PubMed |
de Oliveira VC, Faquin V, Andrade FR, Carneiro JP, da Silva Júnior EC, de Souza KRD, Pereira J, Guilherme LRG (2019) Physiological and physicochemical responses of potato to selenium biofortification in tropical soil. Potato Research 62, 315–331.
| Physiological and physicochemical responses of potato to selenium biofortification in tropical soil.Crossref | GoogleScholarGoogle Scholar |
Doğru A, Çakirlar H (2020) Effects of leaf age on chlorophyll fluorescence and antioxidant enzymes activity in winter rapeseed leaves under cold acclimation conditions. Brazilian Journal of Botany 43, 11–20.
| Effects of leaf age on chlorophyll fluorescence and antioxidant enzymes activity in winter rapeseed leaves under cold acclimation conditions.Crossref | GoogleScholarGoogle Scholar |
Elkelish AA, Soliman MH, Alhaithloul HA, El-Esawi MA (2019) Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism. Plant Physiology and Biochemistry 137, 144–153.
| Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism.Crossref | GoogleScholarGoogle Scholar | 30784986PubMed |
FAO (2017) ‘Seminario Internacional sobre Sequía y Agricultura.’ (FAO: Rome) Available at: http://www.fao.org/documents/card/en/c/f95dcbab-d3ba-44b0-b5d2-feb1d26b2db6/
FAO (2018) Legumbres. Pequeñas semillas, grandes soluciones. (Panamá). (FAO: Rome) Available at: http://www.fao.org/3/ca2597es/CA2597ES.pdf
FAO (2019) Proactive approaches to drought preparedness – Where are we now and where do we go from here? (FAO: Rome) Available at: http://www.fao.org/3/ca5794en/ca5794en.pdf
FAOSTAT (2012) FAOSTAT Database. (FAO: Rome) Available at: http://www.fao.org/faostat/en/#data/QC (accessed 1 December 2020)
Farooq M, Hussain M, Wahid A, Siddique KHM (2012) Drought stress in plants: an overview. In ‘Plant responses to drought stress’. (Ed. R Aroca) pp. 1–33. (Springer: Berlin, Heidelberg)
Farooqi ZUR, Ayub MA, Ziaur Rehman M, Sohail MI, Usman M, Khalid H, Naz K (2020) Regulation of drought stress in plants. In ‘Plant life under changing environment’. (Eds DK Tripathi, VP Singh, DK Chauhan, S Sharma, SM Prasad, NK Dubey, N Ramawat) pp. 77–104. (Academic Press)
Flexas J, Gallé A, Galmés J, Ribas-Carbo M, Medrano H (2012) The response of photosynthesis to soil water stress. In ‘Plant responses to drought stress’. (Ed. R Aroca) pp. 129–144. (Springer: Berlin, Heidelberg)
Giannopolitis CN, Ries SK (1977) Superoxide dismutases. Plant Physiology 59, 309–314.
| Superoxide dismutases.Crossref | GoogleScholarGoogle Scholar | 16659839PubMed |
Gupta M, Gupta S (2017) An overview of selenium uptake, metabolism, and toxicity in plants. Frontiers in Plant Science 7, 1–14.
| An overview of selenium uptake, metabolism, and toxicity in plants.Crossref | GoogleScholarGoogle Scholar |
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiology 84, 450–455.
| Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves.Crossref | GoogleScholarGoogle Scholar | 16665461PubMed |
Hawrylak-Nowak B, Hasanuzzaman M, Matraszek-Gawron R (2018) Mechanisms of selenium-induced enhancement of abiotic stress tolerance in plants. In ‘Plant nutrients and abiotic stress tolerance’. (Eds M Hasanuzzaman, M Fujita, H Oku, K Nahar, B Hawrylak-Nowak) pp. 269–295. (Springer Singapore: Singapore)
Huang C, Yu M, Sun L, Qin N, Wei L (2020) Physiological responses of sweet potato seedlings under drought-stress conditions with selenium applications. Journal of Agricultural and Crop Research 8, 98–112.
| Physiological responses of sweet potato seedlings under drought-stress conditions with selenium applications.Crossref | GoogleScholarGoogle Scholar |
Jacobsen SE, Liu F, Jensen CR (2009) Does root-sourced ABA play a role for regulation of stomata under drought in quinoa (Chenopodium quinoa Willd.). Scientia Horticulturae 122, 281–287.
| Does root-sourced ABA play a role for regulation of stomata under drought in quinoa (Chenopodium quinoa Willd.).Crossref | GoogleScholarGoogle Scholar |
Lara TS, Lessa JH de L, de Souza KRD, Corguinha APB, Martins FAD, Lopes G, Guilherme LRG (2019) Selenium biofortification of wheat grain via foliar application and its effect on plant metabolism. Journal of Food Composition and Analysis 81, 10–18.
| Selenium biofortification of wheat grain via foliar application and its effect on plant metabolism.Crossref | GoogleScholarGoogle Scholar |
Lessa JHL, Araujo AM, Silva GNT, Guilherme LRG, Lopes G (2016) Adsorption-desorption reactions of selenium (VI) in tropical cultivated and uncultivated soils under Cerrado biome. Chemosphere 164, 271–277.
| Adsorption-desorption reactions of selenium (VI) in tropical cultivated and uncultivated soils under Cerrado biome.Crossref | GoogleScholarGoogle Scholar |
Lessa JL, Araujo AM, Ferreira LA, Júnior E, Oliveira C, Corguinha AP, Martins F, Carvalho H, Guilherme LR, Lopes G (2019) Agronomic biofortification of rice (Oryza sativa L.) with selenium and its effect on element distributions in biofortified grains. Plant and Soil 444, 331–342.
| Agronomic biofortification of rice (Oryza sativa L.) with selenium and its effect on element distributions in biofortified grains.Crossref | GoogleScholarGoogle Scholar |
Lessa JH de L, Raymundo JF, Branco Corguinha AP, Dias Martins FA, Araujo AM, Melo Santiago FE, Pereira de Carvalho HW, Guimarães Guilherme LR, Lopes G (2020) Strategies for applying selenium for biofortification of rice in tropical soils and their effect on element accumulation and distribution in grains. Journal of Cereal Science 96,
Liang Y, Li D, Chen Y, Cheng J, Zhao G, Fahima T, Yan J (2020) Selenium mitigates salt-induced oxidative stress in durum wheat (Triticum durum Desf.) seedlings by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. 3 Biotech 10, 368
| Selenium mitigates salt-induced oxidative stress in durum wheat (Triticum durum Desf.) seedlings by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system.Crossref | GoogleScholarGoogle Scholar | 32832329PubMed |
Malavolta E (1981) ‘Manual de química agrícola: adubos e adubação.’ (Agronômica Ceres: São Paulo)
Malavolta E, Vitti GC, de Oliveira SA (1997) ‘Avaliação do estado nutricional das plantas: princípios e aplicações.’ (Associação Brasileira para Pesquisa da Potassa e do Fosfato, POTAFOS: São Paulo)
Mathobo R, Marais D, Steyn JM (2017) The effect of drought stress on yield, leaf gaseous exchange and chlorophyll fluorescence of dry beans (Phaseolus vulgaris L.). Agricultural Water Management 180, 118–125.
| The effect of drought stress on yield, leaf gaseous exchange and chlorophyll fluorescence of dry beans (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar |
Meier U (Ed.) (2001) ‘Growth stages of mono-and dicotyledonous plants - BBCH monograph.’ (Federal Biological Research Centre for Agriculture and Forestry: Bonn)
Mouta ER, de Melo WJ, Soares MR, Alleoni LRF, Casagrande JC (2008) Adsorção de selênio em latossolos. Revista Brasileira de Ciência do Solo 32, 1033–1041.
| Adsorção de selênio em latossolos.Crossref | GoogleScholarGoogle Scholar |
Nakano Y, Asada K (1981) Hydrogen Peroxide is Scavenged by Ascorbate-specific Peroxidase in Spinach Chloroplasts. Plant & Cell Physiology 22, 867–880.
Namorato FA (2019) Uso da ureia enriquecida com selênio na biofortificação do feijão-comum. Dissertação (mestrado acadêmico) - Universidade Federal de Lavras, Brazil.
Natasha Shahid M, Niazi NK, Khalid S, Murtaza B, Bibi I, Rashid MI (2018) A critical review of selenium biogeochemical behavior in soil-plant system with an inference to human health. Environmental Pollution 234, 915–934.
| A critical review of selenium biogeochemical behavior in soil-plant system with an inference to human health.Crossref | GoogleScholarGoogle Scholar |
Obiero CO, Milroy SP, Bell RW (2020) Photosynthetic and respiratory response of potato leaves of different ages during and after an episode of high temperature. Journal of Agronomy & Crop Science 206, 352–362.
| Photosynthetic and respiratory response of potato leaves of different ages during and after an episode of high temperature.Crossref | GoogleScholarGoogle Scholar |
Oliveira MG de C, Oliveira LFC de, Wendland A, Guimarães CM, Quintela ED, Barbosa FR, Carvalho M da CS, Junior ML, Silveira PM da (2018) ‘Conhecendo a Fenologia do Feijoeiro e Seus Aspectos Fitotécnicos.’ (Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA): Brasilia, DF)
R Core Team (2019) R: A language and environment for statistical computing. Available at: https://www.r-project.org/
Ray JD, Sinclair TR (1997) Stomatal closure of maize hybrids in response to drying soil. Crop Science 37, 803–807.
| Stomatal closure of maize hybrids in response to drying soil.Crossref | GoogleScholarGoogle Scholar |
Sedlar A, Kidrič M, Šuštar-Vozlič1 J, Pipan B, Zadražnik T, Meglič V (2019) Drought stress response in agricultural plants: a case study of common bean (Phaseolus vulgaris L.). In ‘Drought – detections and solutions’. (Ed. G Ondrasek) pp. 1–19. (IntechOpen)
Sinclair TR, Ludlow MM (1986) Influence of soil water supply on the plant water balance of four tropical grain legumes. Australian Journal of Plant Physiology 13, 329–341.
Sun Y, Wang C, Chen HYH, Ruan H (2020) Response of plants to water stress: a meta-analysis. Frontiers in Plant Science 11, 978
| Response of plants to water stress: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 32676096PubMed |
Teixeira PC, Donagemma GK, Fontana A, Teixeira WG (2017) ‘Manual de Métodos de Análise de Solo.’ (Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA) – Ministerio da Agricultura, Pecuária e Abastecimento: Brasilia, DF)
USEPA (2007) Method 3051 A: micro- wave assisted acid digestion of sediments sludges, soils and oils. ‘Sw-846 Test Methods for Evaluation of Solid Waste Physical and Chemical Methods’. pp. 1–30. (Office of Solid Waste, United States Environmental Protection Agency: Washington, DC) Available at: https://www.epa.gov/sites/production/files/2015-12/documents/3051a.pdf
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Science 151, 59–66.
| Oxidative stress and some antioxidant systems in acid rain-treated bean plants.Crossref | GoogleScholarGoogle Scholar |
White PJ (2018) Selenium metabolism in plants. Biochimica et Biophysica Acta. G, General Subjects 1862, 2333–2342.
| Selenium metabolism in plants.Crossref | GoogleScholarGoogle Scholar |
Winkel LHE, Vriens B, Jones GD, Schneider LS, Pilon-Smits E, Bañuelos GS (2015) Selenium cycling across soil-plant-atmosphere interfaces: a critical review. Nutrients 7, 4199–4239.
| Selenium cycling across soil-plant-atmosphere interfaces: a critical review.Crossref | GoogleScholarGoogle Scholar |
Xu Z, Jiang Y, Zhou G (2015) Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants. Frontiers in Plant Science 6, 1–17.
| Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants.Crossref | GoogleScholarGoogle Scholar |
Yan W, Zhong Y, Shangguan Z (2016) A meta-analysis of leaf gas exchange and water status responses to drought. Scientific Reports 6, 20917
| A meta-analysis of leaf gas exchange and water status responses to drought.Crossref | GoogleScholarGoogle Scholar | 26868055PubMed |
