Abstract
Developing salt-tolerant plants has emerged as a highly efficient approach to cope with salinity damage on crop growth and productivity. This study aimed to elucidate the mechanisms of salt acclimation in cowpea plants [Vigna unguiculata (L.) Walp] and screen salt-tolerant potential genotypes during the early vegetative stage. Seven cowpea genotypes (Epace, Juruá, Maratauã, Milagroso, Pitiúba, Sempre verde, and TVU) were irrigated for 24 days with saline solutions of electrical conductivity 0.8 (control), 4.0 (moderate stress), and 8.0 dS m−1 (severe stress). Growth, water status, membrane damage, and variables related to photosynthetic machinery efficiency were evaluated. Biomass accumulation dramatically decreased with salinity, and the reductions were intensified by increasing the salt level. Nevertheless, under moderate salinity, Pitiúba plants showed less reductions in growth than other genotypes. Under moderate stress, Pitiúba plants exhibited maintenance of osmotic potential and photosynthetic pigments, which was consistent with unaltered membrane and elevated leaf succulence, resulting in improved photochemical performance. Conversely, although TVU, Juruá, and Milagroso plants had activated responses against moderate salinity, including reduced leaf osmotic potential and improved stomatal conductance, these responses were not sufficient to mitigate salt injury. The findings clearly show that the Pitiúba genotype activates coordinated responses to mitigate moderate salt damage, constituting an alternative for cultivating cowpea plants in saline environments.
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References
Agarwal PK, Sheel P, Gupta K, Jha B (2013) Bioengineering for salinity tolerance in plants: state of the art. Mol Biotechnol 54:102–123. https://doi.org/10.1007/s12033-012-9538-3
Araújo GS, Miranda RS, Mesquita RO, Paula SO, Prisco JT, Gomes-Filho E (2018) Nitrogen assimilation pathways and ionic homeostasis are crucial for photosynthetic apparatus efficiency in salt-tolerant sunflower genotypes. Plant Growth Regul 86(3):375–388. https://doi.org/10.1007/s10725-018-0436-y
Bao AK, Wang YW, Xi JJ, Liu C, Zhang JL, Wang SM (2014) Co-expression of xerophyte Zygophyllum xanthoxylum ZxNHX and ZxVP1-1 enhances salt and drought tolerance in transgenic Lotus corniculatus by increasing cations accumulation. Funct Plant Biol 41(2):203–214. https://doi.org/10.1071/fp13106
Bargaz A, Nassar RMA, Rady MM, Gaballah MS, Thompson SM, Brestic M, Schmidhalter U, Abdelhamid MT (2016) Improved salinity tolerance by phosphorus fertilizer in two Phaseolus vulgaris recombinant inbred lines contrasting in their P-efficiency. J Agron Crop Sci 202(6):497–507. https://doi.org/10.1111/jac.12181
Batista VCV, Pereira IMC, Paula-Marinho SO, Canuto KM, Pereira RCA, Rodrigues THS, Daloso DM, Gomes-Filho E, Carvalho HH (2019) Salicylic acid modulates primary and volatile metabolites to alleviate salt stress-induced photosynthesis impairment on medicinal plant Egletes viscosa. Environ Exp Bot 167:103870. https://doi.org/10.1016/j.envexpbot.2019.103870
Bernardo S, Soares AA, Mantovani EC (2008) Manual de irrigação, 8th edn. Viçosa, UFV
Bulgari R, Trivellini A, Ferrante A (2019) Effects of two doses of organic extract-based biostimulant on greenhouse lettuce grown under increasing NaCl concentrations. Front Plant Sci 9:1870. https://doi.org/10.3389/fpls.2018.01870
Cabello JV, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotech 26:62–70. https://doi.org/10.1016/j.copbio.2013.09.011
Causin HF, Bordón DAE, Burrieza H (2020) Salinity tolerance mechanisms during germination and early seedling growth in Chenopodium quinoa Wild. genotypes with different sensitivity to saline stress. Environ Exp Bot 172:103995. https://doi.org/10.1016/j.envexpbot.2020.103995
Chang B, Yang L, Cong W, Zu Y, Tang Z (2014) The improved resistance to high salinity induced by trehalose is associated with ionic regulation and osmotic adjustment in Catharanthus roseus. Plant Physiol Bioch 77:140–148. https://doi.org/10.1016/j.plaphy.2014.02.001
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103(4):551–560. https://doi.org/10.1093/aob/mcn125
Coelho DG, Miranda RS, Paula-Marinho SO, Carvalho HH, Prisco JT, Gomes-Filho E (2020) Ammonium nutrition modulates K and N uptake, transport and accumulation during salt stress acclimation of sorghum plants. Arch Agron Soil Sci 66(14):1991–2004. https://doi.org/10.1080/03650340.2019.1704736
Costa PHA, Silva JV, Bezerra MA, Enéas-Filho J, Prisco JT, Gomes-Filho E (2003) Crescimento e níveis de solutos orgânicos e inorgânicos em cultivares de Vigna unguiculata submetidos à salinidade. Rev Bras Bot 26(3):289–297. https://doi.org/10.1590/S0100-84042003000300002
Doubnerová V, Ryšlavá H (2011) What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Sci 180(4):575–583. https://doi.org/10.1016/j.plantsci.2010.12.005
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 Physiol Bioch 137:144–153. https://doi.org/10.1016/j.plaphy.2019.02.004
Fan H-F, Du C-X, Guo S-R (2013) Nitric oxide enhances salt tolerance in cucumber seedlings by regulating free polyamine content. Environ Exp Bot 86:52–59. https://doi.org/10.1016/j.envexpbot.2010.09.007
FAO (2020) Salt-affected soils. http://www.fao.org/soils-portal/soil-management/management-of-some-problem-soils/salt-affected-soils/more-information-on-salt-affected-soils/en/. Accessed 20 May 2020
Farooq M, Gogoi N, Hussain M, Barthakur S, Paul S, Bharadwaj N, Migdadi HM, Alghamdi SS, Siddique KHM (2017) Effects, tolerance mechanisms and management of salt stress in grain legumes. Plant Physiol Biochem 118:199–217. https://doi.org/10.1016/j.plaphy.2017.06.020
Flexas JA, Diaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30(10):1284–1298. https://doi.org/10.1111/j.1365-3040.2007.01700.x
Freitas VS, Miranda RS, Costa JH, Oliveira DF, Paula SO, Miguel EC, Freire RS, Prisco JT, Gomes-Filho E (2018) Ethylene triggers salt tolerance in maize genotypes by modulating polyamine catabolism enzymes associated with H2O2 production. Environ Exp Bot 145:75–86. https://doi.org/10.1016/j.envexpbot.2017.10.022
Freitas PAF, Carvalho HH, Costa JH, Miranda RS, Saraiva KDC, Oliveira FDB, Coelho DG, Prisco JT, Gomes-Filho E (2019) Salt acclimation in sorghum plants by exogenous proline: physiological and biochemical changes and regulation of proline metabolism. Plant Cell Rep 38(3):403–416. https://doi.org/10.1007/s00299-019-02382-5
Gondim FA, Miranda RS, Gomes-Filho E, Prisco JT (2013) Enhanced salt tolerance in maize plants induced by H2O2 leaf spraying is associated with improved gas exchange rather than with non-enzymatic antioxidant system. Theor Exp Plant Phys 25(4):251–260. https://doi.org/10.1590/S2197-00252013000400003
Hu M, Shi Z, Zhang Z, Zhang Y, Li H (2012) Effects of exogenous glucose on seed germination and antioxidant capacity in wheat seedlings under salt stress. Plant Growth Regul 68(2):177–188. https://doi.org/10.1007/s10725-012-9705-3
Huertas R, Olías R, Eljakaoui Z, Gálvez FJ, Li J, Morales AP, Belver A, Rodríguez-Rosales MP (2012) Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant Cell Environ 2:1–16. https://doi.org/10.1111/j.1365-3040.2012.02504.x
Huo T, Wang CT, Yu TF, Wang DM, Li M, Zhao D, Li XT, Fu JD, Xu ZS, Song XY (2021) Overexpression of ZmWRKY65 transcription factor from maize confers stress resistances in transgenic Arabidopsis. Sci Rep-UK 11(1):1–15. https://doi.org/10.1038/s41598-021-83440-5
Ismail AM, Horie T (2017) Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu Rev Plant Biol 68:405–434. https://doi.org/10.1146/annurev-arplant-042916-040936
Juneau P, Green BR, Harrison PJ (2005) Simulation of pulse amplitude-modulated (PAM) fluorescence: limitations of some PAM-parameters in studying environmental stress effects. Photosynthetica 43(1):75–83. https://doi.org/10.1007/s11099-005-5083-7
Kumar A, Lata C, Kumar P, Devi R, Singh K, Krishnamurthy SL, Kulshreshtha N, Yadav RK, Sharma SK (2016) Salinity and drought induced changes in gas exchange attributes and chlorophyll fluorescence characteristics of rice (Oryza sativa) varieties. Indian J Agr Sci 86(6):718–726
Li M, Chen R, Jiang Q, Sun X, Zhang H, Hu Z (2021) GmNAC06, a NAC domain transcription factor enhances salt stress tolerance in soybean. Plant Mol Biol 105(3):333–345. https://doi.org/10.1007/s11103-020-01091-y
Mann A, Kaur G, Kumar A, Sanwal SK, Singh J, Sharma PC (2019) Physiological response of chickpea (Cicer arietinum L.) at early seedling stage under salt stress conditions. Legume Res 42(5):625–632. https://doi.org/10.18805/LR-4059
Mantovani A (1999) A method to improve leaf succulence quantification. Braz Arch Biol Technol 42(1):9–14. https://doi.org/10.1590/S1516-89131999000100002
Miranda RS, Mesquita RO, Freitas NS, Prisco JT, Gomes-Filho E (2014) Nitrate:ammonium nutrition alleviates detrimental effects of salinity by enhancing photosystem II efficiency in sorghum plants. Rev Bras Eng Agr Amb 18(Suplement):8–12
Miranda RS, Gomes-Filho E, Prisco JT, Alvarez-Pizarro JC (2016) Ammonium improves tolerance to salinity stress in Sorghum bicolor plants. Plant Growth Regul 78(1):121–131. https://doi.org/10.1007/s10725-015-0079-1
Miranda RS, Mesquita RO, Costa JH, Alvarez-Pizarro JC, Prisco JT, Gomes-Filho E (2017) Integrative control between proton pumps and SOS1 antiporters in roots is crucial for maintaining low Na+ accumulation and salt tolerance in ammonium-supplied Sorghum bicolor. Plant Cell Physiol 58(3):522–536. https://doi.org/10.1093/pcp/pcw231
Mishra S, Behura R, Awasthi JP, Dey M, Sahoo D, Bhowmik SS, Panda SK, Sahoo L (2014) Ectopic overexpression of a mungbean vacuolar Na+/H+ antiporter gene (VrNHX1) leads to increased salinity stress tolerance in transgenic Vigna unguiculata L. Walp Mol Breeding 34(3):1345–1359. https://doi.org/10.1007/s11032-014-0120-5
Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol Biochem 54:17–26. https://doi.org/10.1016/j.plaphy.2012.02.003
Murillo-Amador B, Troyo-Diéguez E, García-Hernández JL, López-Aguilar R, Ávila-Serrano NY, Salgado SZ, Rueda-Puente EO, Kaya C (2006) Effect of NaCl salinity in the genotypic variation of cowpea (Vigna unguiculata) during early vegetative growth. Sci Hortic 108(4):423–431. https://doi.org/10.1016/j.scienta.2006.02.010
Poor P, Gemes K, Horvath F, Szepesi A, Simon ML, Tari I (2011) Salicylic acid treatment via the rooting medium interferes with stomatal response, CO2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. Plant Biol 13(1):105–114. https://doi.org/10.1111/j.1438-8677.2010.00344.x
Praxedes SC, Lacerda CF, DaMatta FM, Prisco JT, Gomes-Filho E (2010) Salt tolerance is associated with differences in ion accumulation, biomass allocation and photosynthesis in cowpea cultivars. J Agron Crop Sci 196:193–204. https://doi.org/10.1111/j.1439-037X.2009.00412.x
Praxedes SC, Lacerda CF, Ferreira TM, Prisco JT, DaMatta FM, Gomes-Filho E (2011) Salt tolerance is unrelated to carbohydrate metabolism in cowpea cultivars. Acta Physiol Plant 33:887–896. https://doi.org/10.1007/s11738-010-0615-6
Praxedes SC, Gomes-Filho E, Damatta FM, Lacerda CF, Prisco JT (2014) Salt stress tolerance in cowpea is poorly related to the ability to cope with oxidative stress. Acta Bot Croat 73(1):51–62. https://doi.org/10.2478/botcro-2013-0010
Rhoades JD, Kandiah A, Mashali AM (2000) Uso de águas salinas para produção agrícola. UFPB, Campina Grande
Silva ARA, Bezerra FML, Lacerda CF, Miranda RS, Marques EC (2018) Ion accumulation in young plants of the “green dwarf” coconut under water and salt stress. Rev Cienc Agron 49(2):249–258. https://doi.org/10.5935/1806-6690.20180028
Souza DMG, Lobato E (2014) Cerrado: correção do solo e adubação. Embrapa Informação Tecnológica, Brasília, p 416
Van Nguyen L, Bertero D, Nguyen LV (2020) Genetic variation in root development responses to salt stresses of quinoa. J Agron Crop Sci 206:538–547. https://doi.org/10.1111/jac.12411
Wang Q, Kang L, Lin C, Song Z, Tao C, Liu W, Sang T, Yan J (2019) Transcriptomic evaluation of Miscanthus photosynthetic traits to salinity stress. Biomass Bioenerg 125:123–130. https://doi.org/10.1016/j.biombioe.2019.03.005
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144(3):307–314. https://doi.org/10.1016/S0176-1617(11)81192-2
Yan K, Chen P, Shao H, Zhao S, Zhang L, Xu G, Sun J (2012) Responses of photosynthesis and photosystem II to higher temperature and salt stress in sorghum. J Agron Crop Sci 198(3):218–226. https://doi.org/10.1111/j.1439-037X.2011.00498.x
Yin Y, Li S, Liao W, Lu Q, Wen X, Lu C (2010) Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. J Plant Physiol 167(12):959–966. https://doi.org/10.1016/j.jplph.2009.12.021
Zahra J, Nazim H, Cai S, Han Y, Wu D, Zhang B, Haider SI, Zhang G (2014) The influence of salinity on cell ultrastructures and photosynthetic apparatus of barley genotypes differing in salt stress tolerance. Acta Physiol Plant 36:1261–1269. https://doi.org/10.1007/s11738-014-1506-z
Acknowledgements
The Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA), Fundação de Amparo à Pesquisa do Estado do Piauí (FAPEPI), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ) for financial support.
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This research was supported by the Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA) under grant number PVIG-02334/17; Fundação de Amparo à Pesquisa do Estado do Piauí (FAPEPI) under grant Edital PPP FAPEPI/MCT/CNPq/CT-INFRA n° 007/2018; and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) under grant number 427219/2018–3.
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de Souza Miranda, R., de Souza, F.I.L., Alves, A.F. et al. Salt-Acclimation Physiological Mechanisms at the Vegetative Stage of Cowpea Genotypes in Soils from a Semiarid Region. J Soil Sci Plant Nutr 21, 3530–3543 (2021). https://doi.org/10.1007/s42729-021-00625-7
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DOI: https://doi.org/10.1007/s42729-021-00625-7