Abstract
Maize is sensitive to salinity stress, which has adverse effects on plant growth and yield. In this study, two Egyptian white maize hybrids, single cross 131 (SC131) and single cross 132 (SC132), were exposed to 100 mM NaCl stress for 12 days in a hydroponic culture and physiological and biochemical parameters, and gene expression for some Na+ and K+ transporters were evaluated. The results revealed that the total dry weight of SC131 was greater than that of SC132. The root growth was also better for SC131 than SC132. The Na+ concentration in leaves and stems, and H2O2 were significantly lower in SC131 than in SC132, while the proline concentration was higher in the leaf of SC131 than in SC132 under salt stress. Moreover, catalase and ascorbate peroxidase activities increased with salinity in SC131 leaves compared to catalase and GR in SC132. Salt stress slightly induced the expression of ZmHKT1;5 (for Na+ exclusion) in SC132, but repressed it in SC131. On the other hand, the expression of ZmHKT2 gene (for K+ exclusion) was highly induced by salt stress in SC132, but was not detected in SC131. The salt increased the expression of ZmNHX1 (for vacuolar Na+ sequestration) in SC132, but repressed it in SC131. Taken together, these results suggest that the maize hybrid SC131 is more tolerant to salinity than SC132, thanks to a more efficient leaf Na+ exclusion mechanism, that is yet to be investigated, and to a better antioxidant defense system. Thus, SC131 could constitute a new hybrid worthy of consideration in maize breeding programs for enhanced productivity on salt-affected soils.
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References
AbdElgawad H, Zinta G, Hegab MM, Pandy R, Asard H, Abuelsoud W (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Sci 7:1–11
Adhikari T, Sarkar D, Mashayekhi H, Xing B (2016) Growth and enzymatic activity of maize (Zea mays L.) plant: Solution culture test for copper dioxide nano particles. J Plant Nutr 39:99–115
Anschütz U, Becker D, Shabala S (2014) Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. J Plant Physiol 171:670–687. https://doi.org/10.1016/j.jplph.2014.01.009
Arora N, Renu B, Priyanka S, Arora HK (2008) 28-Homobrassinolide alleviates oxidative stress in salt-treated maize (Zea mays L.) plants. Braz J Plant Physiol 20:153–157
Assaha DV, Mekawy AM, Ueda A, Saneoka H (2015) Salinity-induced expression of HKT may be crucial for Na+ exclusion in the leaf blade of huckleberry (Solanum scabrum Mill.), but not of eggplant (Solanum melongena L.). Biochem Biophys Res Commun 460:416–421. https://doi.org/10.1016/j.bbrc.2015.03.048
Assaha DV, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW (2017) The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front Physiol 8:1–19. https://doi.org/10.3389/fphys.2017.00509
Assaha DVM, Liu L, Ueda A, Nagaoka T, Saneoka H (2016) Effects of drought stress on growth, solute accumulation and membrane stability of leafy vegetable, huckleberry (Solanum scabrum Mill.). J Environ Biol 37:107–114
Banu MNA, Hoque MA, Watanabe-Sugimoto M, Matsuoka K, Nakamura Y, Shimoishi Y, Murata Y (2009) Proline and glycinebetaine induce antioxidant defense gene expression and suppress cell death in cultured tobacco cells under salt stress. J Plant Physiol 166:146–156. https://doi.org/10.1016/j.jplph.2008.03.002
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil. https://doi.org/10.1007/bf00018060
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Bohnert HJ, Gensen RJ (1996) Strategies for engineering water-stress tolerance in plants. Trends Biotechnol 14:89–97
Cao Y, Liang X, Yin P, Zhang M, Jiang C (2019) A domestication-associated reduction in K+-preferring HKT transporter activity underlies maize shoot K+ accumulation and salt tolerance. New Phytol 222:301–317. https://doi.org/10.1111/nph.15605
Carden DE, Walker DJ, Flowers TJ, Miller AJ (2003) Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiol 131:676–683. https://doi.org/10.1104/pp.011445
Chance B, Maehly AC (1955) The assay of catalases and peroxidases. Methods Enzymol 2:764–775
Chuamnakthong S, Nampei M, Ueda A (2019) Characterization of Na+ exclusion mechanism in rice under saline-alkaline stress conditions. Plant Sci 287:110171
Esfandiari E, Gohari G (2017) Response of ROS-scavenging systems to salinity stress in two different wheat (Triticum aestivum L.) cultivars. Not Bot Horti Agrobo 45:287–291. https://doi.org/10.15835/nbha45110682
Farooq M, Mubshar H, Abdul W, Kadambot HMS (2015) Salt stress in maize: effects, resistance mechanisms, and management. A review. Agron Sustain Dev 35:461–481
Fortmeier R, Schubert S (1995) Salt tolerance of maize (Zea mays L.): the role of sodium exclusion. Plant Cell Environ 18:1041–1047
Fricke W, Akhiyarova G, Veselov D, Kudoyarova G (2004) Rapid and tissue-specific changes in ABA and in growth rate in response to salinity in barley leaves. J Exp Bot 55:1115–1123
Garciadeblás B, Senn ME, Bañuelos MA, Rodríguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J 34:788–801. https://doi.org/10.1046/j.1365-313x.2003.01764.x
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
Golldack D, Quigley F, Michalowski CB, Kamasani UR, Bohnert HJ (2003) Salinity stress-tolerant and -sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Mol Biol 51:71–81. https://doi.org/10.1023/a:1020763218045
Gondim FA, Gomes-Filho E, Lacerda F, Prisco JT (2010) Pretreatment with H2O2 in maize seeds: effects on germination and seedling acclimation to salt stress. Braz J Plant Physiol 22:103–112
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 Physiol 25:251–260
Hanks RJ, Ashcroft GL, Rasmussen VP, Wilson GD (1978) Corn production as influenced by irrigation and salinity-Utah studies. Irrigation Sci 1:47–59
Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ 33:552–565. https://doi.org/10.1111/j.1365-3040.2009.02056.x
Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651. https://doi.org/10.1016/j.bbrc.2006.04.140
Jiang C, Zu C, Lu D, Zheng Q, Shen J, Wang H, Li D (2017) Effect of exogenous selenium supply on photosynthesis, Na+ accumulation and antioxidative capacity of maize (Zea mays L.) under salinity stress. Sci Rep 7:42039. https://doi.org/10.1038/srep42039
Jiang Z et al (2018) Association analysis and identification of ZmHKT1;5 variation with salt-stress tolerance. Front Plant Sci 9:1485. https://doi.org/10.3389/fpls.2018.01485
Köşkeroğlu S, Tuna AL (2010) The investigation on accumulation levels of proline and stress parameters of the maize (Zea mays L.) plant under salt and water stress. Acta Physiol Plant 32:541–549
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lv BS, Ma HY, Li XW, Wei LX, Lv HY, Yang HY, Jiang CJ, Liang ZW (2015) Proline accumulation is not correlated with saline-alkaline stress tolerance in rice seedlings. Agron J 107:51–60. https://doi.org/10.2134/agronj14.0327
Maas EV, Hoffman GJ, Chaba GD, Poss JA, Shannon MC (1983) Salt sensitivity of corn at various growth stages. Irrigation Sci 4:45–57
Mekawy AM, Assaha DV, Yahagi H, Tada Y, Ueda A, Saneoka H (2015) Growth, physiological adaptation, and gene expression analysis of two Egyptian rice cultivars under salt stress. Plant Physiol Biochem 87:17–25. https://doi.org/10.1016/j.plaphy.2014.12.007
Mekawy AMM, Abdelaziz MN, Ueda A (2018a) Apigenin pretreatment enhances growth and salinity tolerance of rice seedlings. Plant Physiol Biochem 130:94–104. https://doi.org/10.1016/j.plaphy.2018.06.036
Mekawy AMM, Assaha DVM, Munehiro R, Kohnishi E, Nagaoka T, Ueda A, Saneoka H (2018b) Characterization of type 3 metallothionein-like gene (OsMT-3a) from rice, revealed its ability to confer tolerance to salinity and heavy metal stresses. Environ Exp Bot 147:157–166. https://doi.org/10.1016/j.envexpbot.2017.12.002
Mekawy AMM, Assaha DVM, Ueda A (2020) Differential salt sensitivity of two flax cultivars coincides with differential sodium accumulation, biosynthesis of osmolytes and antioxidant enzyme activities. J Plant Growth Regul 39:1127–1129. https://doi.org/10.1007/s00344-020-10140-1
Munns R (1993) Physiological processes limiting plant growth in saline soils: some Dogmas and hypotheses. Plant Cell Environ 16:15–24
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663. https://doi.org/10.1111/j.1469-8137.2005.01487.x
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Munns R et al (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30:360–364. https://doi.org/10.1038/nbt.2120
Munns R et al (2020a) Energy costs of salt tolerance in crop plants. New Phytol 225:1072–1090. https://doi.org/10.1111/nph.15864
Munns R, Passioura JB, Colmer TD, Byrt CS (2020b) Osmotic adjustment and energy limitations to plant growth in saline soil. New Phytol 225:1091–1096. https://doi.org/10.1111/nph.15862
Nieves-Cordones M, Martínez V, Benito B, Rubio F (2016) Comparison between arabidopsis and rice for main pathways of K+ and Na+ uptake by roots. Front Plant Sci 7:992. https://doi.org/10.3389/fpls.2016.00992
Pardo JM (2010) Biotechnology of water and salinity stress tolerance. Curr Opin Biotechnol 21:185–196. https://doi.org/10.1016/j.copbio.2010.02.005
Pitann B, Mohamed AKH, Neubert AB, Schubert S (2013) Tonoplast Na+/H+ antiporters of newly developed maize (Zea mays) hybrids contribute to salt resistance during the second phase of salt stress. J Plant Nutr Soil Sci 176:148–156
Ren ZH et al (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146. https://doi.org/10.1038/ng1643
Rhee SG, Chang TC, Jeong W, Kang D (2010) Methods for detection and measurement of hydrogen peroxide inside and outside of cells. Mol Cells 29:539–549. https://doi.org/10.1007/s10059-010-0082-3
Shavrukov Y (2013) Salt stress or salt shock: which genes are we studying? J Exp Bot 64:119–127
Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochem 28:1057–1060. https://doi.org/10.1016/0031-9422(89)80182-7
Suzuki K et al (2016) OsHKT1;4-mediated Na+ transport in stems contributes to Na+ exclusion from leaf blades of rice at the reproductive growth stage upon salt stress. BMC Plant Biol 16:22. https://doi.org/10.1186/s12870-016-0709-4
Takagi H, Yamada S (2013) Roles of enzymes in anti-oxidative response system on three species of chenopodiaceous halophytes under NaCl-stress condition. Soil Sci Plant Nutr 59:603–611. https://doi.org/10.1080/00380768.2013.809600
Ueda A et al (2013) Comparative physiological analysis of salinity tolerance in rice. Soil Sci Plant Nutr 59:896–903. https://doi.org/10.1080/00380768.2013.842883
van Bezouw RFHM et al (2019) Shoot sodium exclusion in salt stressed barley (Hordeum vulgare L.) is determined by allele specific increased expression of HKT1;5. J Plant Physiol 241:153029. https://doi.org/10.1016/j.jplph.2019.153029
Vass I, Rehman AU (2018) The activity of proline as singlet oxygen and superoxide scavenger. Free Radic Biol Med 120:S75–S76. https://doi.org/10.1016/j.freeradbiomed.2018.04.250
Venema K, Quintero FJ, Pardo JM, Donaire JP (2002) The arabidopsis Na+/H+ exchanger AtNHX1 catalyzes low affinity Na+ and K+ transport in reconstituted liposomes. J Biol Chem 277:2413–2418. https://doi.org/10.1074/jbc.M105043200
Wangsawang T, Chuamnakthong S, Kohnishi E, Sripichitt P, Sreewongchai T, Ueda A (2018) A salinity tolerant japonica cultivar has Na+ exclusion mechanism at leaf sheaths through the function of a Na+ transporter OsHKT1;4 under salinity stress. J Agron Crop Sci 204:274–284. https://doi.org/10.1111/jac.12264
Zörb C et al (2005) Does H+ pumping by plasmalemma ATPase limit leaf growth of maize (Zea mays) during the first phase of salt stress? J Plant Nutr Soil Sci 168:550–557
Zhang J et al (2016) Increased abscisic acid levels in transgenic maize overexpressing AtLOS5 mediated root ion fluxes and leaf water status under salt stress. J Exp Bot 67:1339–1355. https://doi.org/10.1093/jxb/erv528
Zhang M et al (2018) A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize. New Phytol 217:1161–1176. https://doi.org/10.1111/nph.14882
Acknowledgements
This research was supported by JSPS KAKENHI Grant Numbers 15KK0283, 16K07643 to AU and Ministry of Higher Education and Scientific Research in Egypt to MSR.
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The authors have made the following declarations about their contributions: Conception and design the experiments: MSR, AU, and AMMM; Performing the experiments and collecting data: MSR, SC, and AU; Analysis and data processing: MSR, AMMM, NES, and AU; Writing and manuscript processing: MSR, DVMA, AMMM, NES, and AU.
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Rizk, M.S., Mekawy, A.M.M., Assaha, D.V.M. et al. Regulation of Na+ and K+ Transport and Oxidative Stress Mitigation Reveal Differential Salt Tolerance of Two Egyptian Maize (Zea mays L.) Hybrids at the Seedling Stage. J Plant Growth Regul 40, 1629–1639 (2021). https://doi.org/10.1007/s00344-020-10216-y
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DOI: https://doi.org/10.1007/s00344-020-10216-y