Abstract
Aims
Selenium (Se) as selenate shares similarities with sulfate in transport and assimilation by plants. Uptake and assimilation of Se might be affected by S and vice-versa, which could affect Se and S concentration in plant tissues, and metabolic pathways such as biosynthesis of sugars, amino acids, and storage proteins. This study aimed to evaluate Se and S combination on cowpea plants under field conditions.
Methods
The experimental design was a 4 × 4 interaction between four rates of Se (0, 10, 25, and 50 g ha− 1) and four rates of S (0, 15, 30, and 60 kg ha− 1) in two consecutive years of cowpea cultivation. Concentrations of Se, S, total sugars, sucrose, total free amino acids, and storage proteins in plant tissue were measured.
Results
The Se x S interaction did not affect cowpea yield or growth. Antagonistic effects of S on Se concentrations in leaves and seeds were observed mainly for the second crop season. Selenium did not decrease S concentrations in leaves and seeds of cowpea plants. The combination of 25 g Se ha− 1 and 30 kg S ha− 1 provided the greater concentrations of total sugars. Interaction between Se and S was associated with greater sucrose, amino acids, and storage proteins concentrations in cowpea seeds.
Conclusions
The Se and S interaction did not impair plant growth but application of S decreased Se content in cowpea. Further studies are needed to better understand the physiological roles of Se and S combination in producing primary metabolic compounds.
Similar content being viewed by others
References
Ambrosano EA, Tanaka RT, Mascarenhas HAA (1997) Leguminosas E Oleaginosas. In: Raij VB, Cantarella H, Quaggio JA, Furlani AMC (eds) Recomendações de Adubação e Calagem Para o Estado de São Paulo, 2nd edn. Instituto Agronômico de Campinas – IAC, Campinas – SP, pp 187–204 (Boletim Técnico 100)
Barłóg P, Grzebisz W, Lukowiak R (2018) Faba bean yield and growth dynamics in response to soil potassium availability and sulfur application. Field Crops Res 219:87–97. https://doi.org/10.1016/j.fcr.2018.01.027
Bielesk RL, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Anal Biochem 17:278–293. https://doi.org/10.1016/0003-2697(66)90206-5
Bradford MA (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–259. https://doi.org/10.1016/0003-2697(76)90527-3
Cabannes E, Buchner P, Hawkesford MJ (2012) Identification and sequence analysis of sulfate/selenate transporters in selenium hyper- and non-accumulating astragalus plant species. In: De Kok LJ, Tausz M, Hawkesford MJ, Hoefgen R, McManus MT, Norton RM, Rennenberg H, Saito K, Schung E, Tabe L (eds) Sulfur metabolism in plants. Springer, Dordrecht, pp 155–162. https://doi.org/10.1007/978-94-007-4450-9_20
Carvalho LCB, Damasceno-Silva KJ, Rocha MM, Sousa MB, Pires CJ, Nunes JAR (2012) Phenotypic correlations between combining abilities of F2 cowpea populations. Crop Breed Appl Biotechnol 12:211–214. https://doi.org/10.1590/S1984-70332012000300008
Chowdhury AH, Sultana T, Rahman A, Saha BK, Chowdhury T, Tarafder S (2020) Sulphur fertilization enhanced yield, its uptake, use efficiency and economic returns of Aloe vera L. Heliyon 6:e05726. https://doi.org/10.1016/j.heliyon.2020.e05726
Cummins I, Dixon DP, Freitag-Pohl S, Skipsey M, Edwards R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43:266–280. https://doi.org/10.3109/03602532.2011.552910
Das D, Das P, Biswas A (2018) Regulation of growth and carbohydrate metabolism in rice (Oryza Sativa L.) seedlings by Selenium and Sulphate. J Plant Stud 7:61–72. https://doi.org/10.5539/jps.v7n1p61
Deng X, Zhao Z, Lv C, Zhang Z, Yuan L, Liu X (2020) Effects of sulfur application on selenium uptake and seed selenium speciation in soybean (Glycine max L.) grown in different soil types. Ecotoxicol Environ Saf 209:111790. https://doi.org/10.1016/j.ecoenv.2020.111790
Dong Y, Silbermann M, Speiser A, Forieri I, Linster E, Poschet G, Allboje-Samami A, Watanabe M, Sticht C, Teleman AA, Deragon JM, Saito K, Hell R, Wirtz M (2017) Sulfur availability regulates plant growth via glucose-TOR signaling. Nat Commun 8:1174. https://doi.org/10.1038/s41467-017-01224-w
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/ac60111a017
El Kassis E, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian JC (2007) Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 143:1231–1241. https://doi.org/10.1104/pp.106.091462
Ekuma JN, Ma Y, Akpabli-Tsigbe NDK, Kwaw E, Ma S, Hu J (2021) Global soil distribution, dietary access routes, bioconversion mechanisms and the human health significance of selenium: A review. Food Biosci 41:100960. https://doi.org/10.1016/j.fbio.2021.100960
FAO, IFAD, UNICEF, WFP, WHO (2019) The State of Food Security and Nutrition in the World 2019. Safeguarding against Economic Slowdowns and Downturns. FAO, Rome
Gigolashvili T, Kopriva S (2014) Transporters in plant sulfur metabolism. Front Plant Sci 5:442. https://doi.org/10.3389/fpls.2014.00442
Ibañez TB, Satos LFM, Lapaz AM, Ribeiro IV, Ribeiro FV, Reis AR, Moreira A, Heinrichs R (2020) Sulfur modulates yield and storage proteins in soybean seeds. Sci Agric 78:1–9. https://doi.org/10.1590/1678-992x-2019-0020
Joy EJM, Broadley MR, Young SD, Black CR, Chilimba ADC, Ander EL, Barlow TS, Watts MJ (2015) Soil type influences crop mineral composition in Malawi. Sci Total Environ 505:587–595. https://doi.org/10.1016/j.scitotenv.2014.10.038
Jiang L, Strobbe S, Straeten DVD, Zhang C (2021) Regulation of plant vitamin metabolism: backbone of biofortification for the alleviation of hidden hunger. Mol Plant 14:40–60. https://doi.org/10.1016/j.molp.2020.11.019
Kopriva S, Talukdar D, Takahashi H, Hell R, Sirko A, Souza SFD, Talukdar T (2016) Editorial: frontiers of sulfur metabolism in plant growth, development, and stress response. Front Plant Sci 6:1120. https://doi.org/10.3389/fpls.2015.01220
Lanza MGDB, Silva VM, Montanha GS, Lavres J, Carvalho HWP, Reis AR (2021) Assessment of selenium spatial distribution using µ-XFR in cowpea (Vigna unguiculata (L.) Walp.) plants: Integration of physiological and biochemical responses. Ecotoxicol Environ Saf 207:111216. https://doi.org/10.1016/j.ecoenv.2020.111216
Lanza MGDB, Reis AR (2021) Roles of selenium in mineral plant nutrition: ROS scavenging responses against abiotic stresses. Plant Physiol Biochem 164:27–43. https://doi.org/10.1016/j.plaphy.2021.04.026
Lara TS, Lessa JHL, Souza KRD, Corguinha APB, Martins FAD, Lopes G, Guilherme LRG (2019) Selenium biofortification of wheat seed via foliar application and its effect on plant metabolism. J Food Compost Anal 81:10–18. https://doi.org/10.1016/j.jfca.2019.05.002
Leaneaertes B, Demont M (2021) The global burden of chronic and hidden hunger revisited: New panel data evidence spanning 1990–2017. Glob Food Sec 28:100480. https://doi.org/10.1016/j.gfs.2020.100480
Lidon FC, Oliveira K, Ribeiro MM, Pelica J, Paraco I, Ramalho JC, Leitão AE, Almeida AS, Campos PS, Ribeiro-Barros AI, Pais IP, Silva MM, Pessoa MF, Reboredo FH (2018) Selenium biofortification of rice seeds and implications on macronutrients quality. J Cereal Sci 81:22–29. https://doi.org/10.1016/j.jcs.2018.03.010
Liu X, Yang Y, Deng X, Li M, Zhang W, Zhao Z (2017) Effects of sulfur and sulfate on selenium uptake and quality of seeds in rapeseed (Brassica napus L.) treated with selenite and selenate. Environ Exp Bot 135:13–20. https://doi.org/10.1016/j.envexpbot.2016.12.005
Liu K, Chen F, Zhao Y, Gu Z, Yang H (2011) Selenium accumulation in protein fractions during germination of Se-enriched brown rice and molecular weights distribution of Se-containing proteins. Food Chem 127:1526–1531. https://doi.org/10.1016/j.foodchem.2011.02.010
Manzeke MG, Mtambenengwe F, Nezomba H, Watts MJ, Broadley MR, Mapfumo P (2017) Zinc fertilization increases productivity and seed nutritional quality of cowpea (Vigna unguiculata [L.] Walp.) under integrated soil fertility management. Field Crops Res 213:231–244. https://doi.org/10.1016/j.fcr.2017.08.010
Malavolta E, Vitti GC, Oliveira SA (1997) Avaliação do estado nutricional das plantas: princípios e aplicações. (In Portuguese.), 2nd edn. Potafos, Piracicaba, p 319
Mostofa MG, Hossain MA, Siddiqui MN, Fujita M, Tran LSP (2017) Phenotypical: physiological and biochemical analyses provide insight into selenium-induced phytotoxicity in rice plants. Chemosphere 178:212–223. https://doi.org/10.1016/j.chemosphere.2017.03.046
Najafi S, Razavi SM, Khoshkam M, Asadi A (2020) Effects of green synthesis of sulfur nanoparticles from Cinnamomum zeylanicum barks on physiological and biochemical factors of Lettuce (Lactuca sativa). Physiol Mol Biol Plants 26:1055–1066. https://doi.org/10.1007/s12298-020-00793-3
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. Environ Pollut 234:915–934. https://doi.org/10.1016/j.envpol.2017.12.019
Panduragan S, Sandercock M, Bayert R, Conn KL, Hou A, Marsolais F (2015) Differential response to sulfur nutrition of two common bean genotypes differing in storage protein composition. Front Plant Sci 6:92. https://doi.org/10.3389/fpls.2015.00092
Rayman MP (2000) The importance of selenium to human health. Lancet 356:233–41. https://doi.org/10.1016/S0140-6736(00)02490-9
Reis AR, El-Ramady H, Santos EF, Gratão PL, Schomburg L (2017) Overview of selenium deficiency and toxicity worldwide: affected areas, selenium-related health issues, and case studies. In: Pilon-Smits EAH, Winkel LHE, Lin ZQ (eds) Selenium in plants. Springer, Berlin, pp 209–230. https://doi.org/10.1007/978-3-319-56249-0_13
Reis HPG, Barcelos JPQ, Silva VM, Santos EF, Tavanti RFR, Putti FF, Young SD, Broadley MR, White PJ, Reis AR (2019) Agronomic biofortification with selenium impacts storage proteins in seeds of upland rice. J Sci Food Agric 100:1990–1997. https://doi.org/10.1002/jsfa.10212
Ren G, Ran X, Zeng R, Chen J, Wang Y, Mao C, Wang X, Feng Y, Yang G (2021) Effects of sodium selenite spray on apple production, quality, and sucrose metabolism-related enzyme activity. Food Chem 339:127883. https://doi.org/10.1016/j.foodchem.2020.127883
Schjoerring JK, Cakmak I, White PJ (2018) Plant nutrition and soil fertility: synergies for acquiring global green growth and sustainable development. Plant Soil 434:1–6. https://doi.org/10.1007/s11104-018-03898-7
Schiavon M, Pilon-Smits EAH (2017) The fascinating facets of plant selenium accumulation– biochemistry, physiology, evolution and ecology. New Phytol 213:1582–1596. https://doi.org/10.1111/nph.14378
Silva VM, Boleta EHM, Lanza MGDB, Lavres J, Martins JT, Santos EF, Santos FLM, Putti FF, Furlani Junior EF, White PJ, Broadley MR, Carvalho HWP, Reis AR (2018) Physiological, biochemical, and ultrastructural characterization of selenium toxicity in cowpea plants. Environ Exp Bot 150:172–182. https://doi.org/10.1016/j.envexpbot.2018.03.020
Silva VM, Boleta EHM, Martins JT, Dos Santos FLM, Silva ACR, Alcock TD, Wilson L, De Sá ME, Young SD, Broadley MR, White PJ, Reis AR (2019) Agronomic biofortification of cowpea with selenium: effects of selenate and selenite applications on selenium and phytate concentrations in seeds. J Sci Food Agric 99:5969–5983. https://doi.org/10.1002/jsfa.9872
Silva VM, Tavanti RR, Gratão PL, Alcock TD, Reis AR (2020) Selenate and selenite affect photosynthetic pigments and ROS scavenging through distinct mechanisms in cowpea (Vigna unguiculata (L.) walp) plants. Ecotoxicol Environ Saf 201:110777. https://doi.org/10.1016/j.ecoenv.2020.110777
Soil Survey Staff Keys to Soil Taxonomy (12th ed), USDA (2014) Natural Resources Conservation Service, Washington, DC
Teka TA, Retta N, Bultosa G, Admassu H, Astatkie T (2020) Protein fractions, in vitro protein digestibility and amino acid composition of select cowpea varieties grown in Ethiopia. Food Biosci 36:100634. https://doi.org/10.1016/j.fbio.2020.100634
Thomas CL, Alcock TD, Graham NS, Hayden R, Matterson S, Wilson L, Young SD, Dupuy LX, White PJ, Hammond JP, Danku JMC, Salt DE, Sweeney A, Bacroft I, Broadley MR (2016) Root morphology and seed and leaf ionomic traits in a Brassica napus L. diversity panel show wide phenotypic variation and are characteristic of crop habit. BMC Plant Biol 16:214. https://doi.org/10.1186/s12870-016-0902-5
Van Handel E (1968) Direct microdetermination of sucrose. Anal Biochem 22:280–283. https://doi.org/10.1016/0003-2697(68)90317-5
Van Raij B, De Andrade JC, Cantarella H, Quaggio JA (1997) Análise Química Para Avaliação da Fertilidade de Solos Tropicais. Instituto Agronômico de Campinas – IAC. Campinas – SP, p 285
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
White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182:49–84
White PJ (2016) Selenium accumulation by plants. Ann Bot 117:217–235. https://doi.org/10.1093/aob/mcv180
White PJ (2018) Selenium in soil and crops. In: Michalke B (ed) Molecular and Integrative Toxicology: Selenium. Springer International Publishing, Cham, pp 29–50. https://doi.org/10.1007/978-3-319-95390-8_2
Yang JYF, Fu Z, Fu Y, Liu S, Chen M, Li Y, Sun Q Chang H, Zhou W, Wang X, Zhang L (2019) Pathway and driving forces of selenite absorption in wheat leaf blades. Plant Soil Environ 65:609–614. https://doi.org/10.17221/542/2019-PSE
Yemm EW, Cocking EC, Ricketts RE (1955) The determination of amino-acids with ninhydrin. Analyst 80:209–214. https://doi.org/10.1039/AN9558000209
Funding
To São Paulo State Research Support Foundation (FAPESP) for VMS doctoral research with financial resources (process number 18/18936-6).
Author information
Authors and Affiliations
Contributions
André Rodrigues dos Reis idealized the study and provided supervision to the project. Vinicius Martins Silva performed the field experiment, lab analysis and wrote the first manuscript draft. Lolita Wilson and Scott D, Young provided technical support and background on lab analysis and results interpretation. Martin R. Broadley and Philip J. White provided intellectual background and support in the project idealization. All authors read and commented previous versions of the manuscript to improve it. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Kadambot Hamsa.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 4.36 MB)
Rights and permissions
About this article
Cite this article
Silva, V.M., Wilson, L., Young, S.D. et al. Interaction between sulfur and selenium in agronomic biofortification of cowpea plants under field conditions. Plant Soil 486, 69–85 (2023). https://doi.org/10.1007/s11104-022-05480-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05480-8