Differential regulation of genes involved in root morphogenesis and cell wall modification is associated with salinity tolerance in chickpea

Salinity is a major constraint for intrinsically salt sensitive grain legume chickpea. Chickpea exhibits large genetic variation amongst cultivars, which show better yields in saline conditions but still need to be improved further for sustainable crop production. Based on previous multi-location physiological screening, JG 11 (salt tolerant) and ICCV 2 (salt sensitive) were subjected to salt stress to evaluate their physiological and transcriptional responses. A total of ~480 million RNA-Seq reads were sequenced from root tissues which resulted in identification of 3,053 differentially expressed genes (DEGs) in response to salt stress. Reproductive stage shows high number of DEGs suggesting major transcriptional reorganization in response to salt to enable tolerance. Importantly, cationic peroxidase, Aspartic ase, NRT1/PTR, phosphatidylinositol phosphate kinase, DREB1E and ERF genes were significantly up-regulated in tolerant genotype. In addition, we identified a suite of important genes involved in cell wall modification and root morphogenesis such as dirigent proteins, expansin and casparian strip membrane proteins that could potentially confer salt tolerance. Further, phytohormonal cross-talk between ERF and PIN-FORMED genes which modulate the root growth was observed. The gene set enrichment analysis and functional annotation of these genes suggests they may be utilised as potential candidates for improving chickpea salt tolerance

Leaf Eh and pH: A Novel Indicator of Plant Stress. Spatial, Temporal and Genotypic Variability in Rice (Oryza sativa L.)

A wealth of knowledge has been published in the last decade on redox regulations in plants. However, these works remained largely at cellular and organelle levels. Simple indicators of oxidative stress at the plant level are still missing. We developed a method for direct measurement of leaf Eh and pH, which revealed spatial, temporal, and genotypic variations in rice. Eh (redox potential) and Eh@pH7 (redox potential corrected to pH 7) of the last fully expanded leaf decreased after sunrise. Leaf Eh was high in the youngest leaf and in the oldest leaves, and minimum for the last fully expanded leaf. Leaf pH decreased from youngest to oldest leaves. The same gradients in Eh-pH were measured for various varieties, hydric conditions, and cropping seasons. Rice varieties differed in Eh, pH, and/or Eh@pH7. Leaf Eh increases and leaf pH decreases with plant age. These patterns and dynamics in leaf Eh-pH are in accordance with the pattern and dynamics of disease infections. Leaf Eh-pH can bring new insight on redox processes at plant level and is proposed as a novel indicator of plant stress/health. It could be used by agronomists, breeders, and pathologists to accelerate the development of crop cultivation methods leading to agroecological crop protection

Effects of Drought and Salinity on Two Commercial Varieties of Lavandula angustifolia Mill

[EN] Global warming is not only affecting arid and semi-arid regions but also becoming a threat to agriculture in Central and Eastern European countries. The present study analyzes the responses to drought and salinity of two varieties of Lavandula angustifolia cultivated in Romania. Lavender seedlings were subjected to one month of salt stress (100, 200, and 300 mM NaCl) and water deficit (complete withholding of irrigation) treatments. To assess the effects of stress on the plants, several growth parameters and biochemical stress markers (photosynthetic pigments, mono and divalent ions, and different osmolytes) were determined in control and stressed plants after the treatments. Both stress conditions significantly inhibited the growth of the two varieties, but all plants survived the treatments, indicating a relative stress tolerance of the two varieties. The most relevant mechanisms of salt tolerance are based on the maintenance of foliar K+ levels and the accumulation of Ca2+ and proline as a functional osmolyte in parallel with increasing external salinities. Under water stress, significant increases of Na+ and K+ concentrations were detected in roots, indicating a possible role of these cations in osmotic adjustment, limiting root dehydration. No significant differences were found when comparing the stress tolerance and stress responses of the two selected lavender varieties.This research was partially funded by the University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, granted to Z.S.-V, and by internal funds of Universitat Politecnica de Valencia. The publication was supported by funds from the National Research Development Projects to finance excellence (PFE)-37/2018-2020 granted by the Romanian Ministry of Research and Innovation.Szekely-Varga, Z.; González-Orenga, S.; Cantor, M.; Jucan, D.; Boscaiu, M.; Vicente, O. (2020). Effects of Drought and Salinity on Two Commercial Varieties of Lavandula angustifolia Mill. Plants. 9(5):1-20. https://doi.org/10.3390/plants9050637S1209

Molecular Aspects of Plant Salinity Stress and Tolerance

This book presents the advances in plant salinity stress and tolerance, including mechanistic insights revealed using powerful molecular tools and multi-omics and gene functions studied by genetic engineering and advanced biotechnological methods. Additionally, the use of plant growth-promoting rhizobacteria in the improvement of plant salinity tolerance and the underlying mechanisms and progress in breeding for salinity-tolerant rice are comprehensively discussed. Clearly, the published data have contributed to the significant progress in expanding our knowledge in the field of plant salinity stress and the results are valuable in developing salinity-stress-tolerant crops; in benefiting their quality and productivity; and eventually, in supporting the sustainability of the world food supply

Plant Oxidative Stress: Biology, Physiology and Mitigation

This Special Issue, “Plant Oxidative Stress: Biology, Physiology, and Mitigation”, published 11 original research works and 1 review article that discussed the various aspects of ROS Biology, metabolism, and the physiological mechanisms and approaches to mitigating oxidative stress. These types of research studies show further directions for the development of crop plants that are tolerant to abiotic stress in the era of climate change

A novel soybean intrinsic protein gene, GmTIP2;3, involved in responding to osmotic stress

Water is essential for plant growth and development. Water deficiency leads to loss of yield and decreased crop quality. To understand water transport mechanisms in plants, we cloned and characterized a novel tonoplast intrinsic protein (TIP) gene from soybean with the highest similarity to TIP2-type from other plants, thus designated GmTIP2;3. The protein sequence contains two conserved NPA motifs and six transmembrane domains. The expression analysis indicated that this gene was constitutively expressed in all detected tissues, with higher levels in the root, stem and pod, and the accumulation of GmTIP2;3 transcript showed a significant response to osmotic stresses, including 20% PEG6000 (polyethylene glycol) and 100 µM ABA (abscisic acid) treatments. The promoter-GUS (glucuronidase) activity analysis suggested that GmTIP2;3 was also expressed in the root, stem and leaf and preferentially expressed in the stele of root and stem, and the core promoter region was 1000 bp in length, located upstream of the ATG start codon. The GUS tissue and induced expression observations were consistent with the findings in soybean. In addition, subcellular localization showed that GmTIP2;3 was a plasma membrane-localized protein. Yeast heterologous expression revealed that GmTIP2;3 could improve tolerance to osmotic stress in yeast cells. Integrating these results, GmTIP2;3 might play an important role in response to osmotic stress in plants

A Novel Soybean Intrinsic Protein Gene, GmTIP2;3, Involved in Responding to Osmotic Stress

Water is essential for plant growth and development. Water deficiency leads to loss of yield and decreased crop quality. To understand water transport mechanisms in plants, we cloned and characterized a novel tonoplast intrinsic protein (TIP) gene from soybean with the highest similarity to TIP2-type from other plants, and thus designated GmTIP2;3. The protein sequence contains two conserved NPA motifs and six transmembrane domains. The expression analysis indicated that this gene was constitutively expressed in all detected tissues, with higher levels in the root, stem and pod, and the accumulation of GmTIP2;3 transcript showed a significant response to osmotic stresses, including 20% PEG6000 (polyethylene glycol) and 100 mu M ABA (abscisic acid) treatments. The promoter-GUS (glucuronidase) activity analysis suggested that GmTIP2;3 was also expressed in the root, stem, and leaf, and preferentially expressed in the stele of root and stem, and the core promoter region was 1000 bp in length, located upstream of the ATG start codon. The GUS tissue and induced expression observations were consistent with the findings in soybean. In addition, subcellular localization showed that GmTIP2;3 was a plasma membrane localized protein. Yeast heterologous expression revealed that Gm TIP2;3 could improve tolerance to osmotic stress in yeast cells. Integrating these results, Gm TIP2;3 might play an important role in response to osmotic stress in plants

Responses to Water Deficit and Salt Stress in Silver Fir (Abies alba Mill.) Seedlings

[EN] Forest ecosystems are frequently exposed to abiotic stress, which adversely affects their growth, resistance and survival. For silver fir (Abies alba), the physiological and biochemical responses to water and salt stress have not been extensively studied. Responses of one-year-old seedlings to a 30-day water stress (withholding irrigation) or salt stress (100, 200 and 300 mM NaCl) treatments were analysed by determining stress-induced changes in growth parameters and different biochemical markers: accumulation of ions, different osmolytes and malondialdehyde (MDA, an oxidative stress biomarker), in the seedlings, and activation of enzymatic and non-enzymatic antioxidant systems. Both salt and water stress caused growth inhibition. The results obtained indicated that the most relevant responses to drought are based on the accumulation of soluble carbohydrates as osmolytes/osmoprotectants. Responses to high salinity, on the other hand, include the active transport of Na+, Cl¿ and Ca2+ to the needles, the maintenance of relatively high K+/Na+ ratios and the accumulation of proline and soluble sugars for osmotic balance. Interestingly, relatively high Na+ concentrations were measured in the needles of A. alba seedlings at low external salinity, suggesting that Na+ can contribute to osmotic adjustment as a `cheap¿ osmoticum, and its accumulation may represent a constitutive mechanism of defence against stress. These responses appear to be efficient enough to avoid the generation of high levels of oxidative stress, in agreement with the small increase in MDA contents and the relatively weak activation of the tested antioxidant systems.This research was partially funded by Doctoral School from the University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, granted to I.M.T. The publication was supported by funds from the National Research Development Projects to finance excellence (PFE)-37/2018-2020 granted by the Romanian Ministry of Research and Innovation.Todea (morar), IM.; González-Orenga, S.; Boscaiu, M.; Plazas Ávila, MDLO.; Sestras, AF.; Prohens Tomás, J.; Vicente, O.... (2020). Responses to Water Deficit and Salt Stress in Silver Fir (Abies alba Mill.) Seedlings. Forests. 11(4):1-21. https://doi.org/10.3390/f11040395S121114Raza, A., Razzaq, A., Mehmood, S., Zou, X., Zhang, X., Lv, Y., & Xu, J. (2019). Impact of Climate Change on Crops Adaptation and Strategies to Tackle Its Outcome: A Review. Plants, 8(2), 34. doi:10.3390/plants8020034Zhou, S.-X., Prentice, I. C., & Medlyn, B. E. (2019). Bridging Drought Experiment and Modeling: Representing the Differential Sensitivities of Leaf Gas Exchange to Drought. Frontiers in Plant Science, 9. doi:10.3389/fpls.2018.01965Fita, A., Rodríguez-Burruezo, A., Boscaiu, M., Prohens, J., & Vicente, O. (2015). Breeding and Domesticating Crops Adapted to Drought and Salinity: A New Paradigm for Increasing Food Production. Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.00978Daliakopoulos, I. N., Tsanis, I. K., Koutroulis, A., Kourgialas, N. N., Varouchakis, A. E., Karatzas, G. P., & Ritsema, C. J. (2016). The threat of soil salinity: A European scale review. Science of The Total Environment, 573, 727-739. doi:10.1016/j.scitotenv.2016.08.177Cuevas, J., Daliakopoulos, I. N., del Moral, F., Hueso, J. J., & Tsanis, I. K. (2019). A Review of Soil-Improving Cropping Systems for Soil Salinization. Agronomy, 9(6), 295. doi:10.3390/agronomy9060295In Proceedings of the 5th Assessment Report, WGII, Climate Change 2014: Impacts, Adaptation, and Vulnerability http://www.ipcc.ch/report/ar5/wg2/Bartels, D., & Sunkar, R. (2005). Drought and Salt Tolerance in Plants. Critical Reviews in Plant Sciences, 24(1), 23-58. doi:10.1080/07352680590910410Tinner, W., Colombaroli, D., Heiri, O., Henne, P. D., Steinacher, M., Untenecker, J., … Valsecchi, V. (2013). The past ecology ofAbies albaprovides new perspectives on future responses of silver fir forests to global warming. Ecological Monographs, 83(4), 419-439. doi:10.1890/12-2231.1Vicario, F., Vendramin, G. G., Rossi, P., Liò, P., & Giannini, R. (1995). Allozyme, chloroplast DNA and RAPD markers for determining genetic relationships between Abies alba and the relic population of Abies nebrodensis. Theoretical and Applied Genetics, 90(7-8), 1012-1018. doi:10.1007/bf00222915Muller, S. D., Nakagawa, T., De Beaulieu, J.-L., Court-Picon, M., Carcaillet, C., Miramont, C., … Bruneton, H. (2007). Post-glacial migration of silver fir (Abies alba Mill.) in the south-western Alps. Journal of Biogeography, 34(5), 876-899. doi:10.1111/j.1365-2699.2006.01665.xRuosch, M., Spahni, R., Joos, F., Henne, P. D., van der Knaap, W. O., & Tinner, W. (2016). Past and future evolution of Abies alba forests in Europe - comparison of a dynamic vegetation model with palaeo data and observations. Global Change Biology, 22(2), 727-740. doi:10.1111/gcb.13075Dobrowolska, D., Bončina, A., & Klumpp, R. (2017). Ecology and silviculture of silver fir (Abies alba Mill.): a review. Journal of Forest Research, 22(6), 326-335. doi:10.1080/13416979.2017.1386021Flückiger, W., & Braun, S. (1981). Perspectives of reducing the deleterious effect of de-icing salt upon vegetation. Plant and Soil, 63(3), 527-529. doi:10.1007/bf02370056Schiop, S. T., Al Hassan, M., Sestras, A. F., Boscaiu, M., Sestras, R. E., & Vicente, O. (2015). Identification of Salt Stress Biomarkers in Romanian Carpathian Populations of Picea abies (L.) Karst. PLOS ONE, 10(8), e0135419. doi:10.1371/journal.pone.0135419Cailleret, M., Nourtier, M., Amm, A., Durand-Gillmann, M., & Davi, H. (2013). Drought-induced decline and mortality of silver fir differ among three sites in Southern France. Annals of Forest Science, 71(6), 643-657. doi:10.1007/s13595-013-0265-0Nourtier, M., Chanzy, A., Cailleret, M., Yingge, X., Huc, R., & Davi, H. (2012). Transpiration of silver Fir (Abies alba mill.) during and after drought in relation to soil properties in a Mediterranean mountain area. Annals of Forest Science, 71(6), 683-695. doi:10.1007/s13595-012-0229-9Gazol, A., Camarero, J. J., Gutiérrez, E., Popa, I., Andreu-Hayles, L., Motta, R., … Carrer, M. (2015). Distinct effects of climate warming on populations of silver fir (Abies alba) across Europe. Journal of Biogeography, 42(6), 1150-1162. doi:10.1111/jbi.12512TODEA (MORAR), I. M., GONZÁLEZ-ORENGA, S., PLAZAS, M., SESTRAS, A. F., PROHENS, J., VICENTE, O., … BOSCAIU, M. (2019). Screening for Salt and Water Stress Tolerance in Fir (Abies alba) Populations. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 47(4), 1063-1072. doi:10.15835/nbha47411348ZW, S., LK, R., JW, F., Li, Q., KJ, W., MM, G., … XN, L. (2016). Salt response of photosynthetic electron transport system in wheat cultivars with contrasting tolerance  . Plant, Soil and Environment, 62(No. 11), 515-521. doi:10.17221/529/2016-pseZhu, J.-K. (2016). Abiotic Stress Signaling and Responses in Plants. Cell, 167(2), 313-324. doi:10.1016/j.cell.2016.08.029LUGO-CRUZ, E., ZAVALA-GARCÍA, F., PICÓN-RUBIO, F. J., URÍAS-ORONA, V., RODRÍGUEZ-FUENTES, H., VIDALES-CONTRERAS, J. A., … NIÑO-MEDINA, G. (2016). Water Stress Effect on Cell Wall Components of Maize (Zea mays) Bran. Notulae Scientia Biologicae, 8(1), 81-84. doi:10.15835/nsb819710Battaglia, M., Olvera-Carrillo, Y., Garciarrubio, A., Campos, F., & Covarrubias, A. A. (2008). The Enigmatic LEA Proteins and Other Hydrophilins. Plant Physiology, 148(1), 6-24. doi:10.1104/pp.108.120725Zhang, D., Tong, J., He, X., Xu, Z., Xu, L., Wei, P., … Shao, H. (2016). A Novel Soybean Intrinsic Protein Gene, GmTIP2;3, Involved in Responding to Osmotic Stress. Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.01237FARDUS, J., MATIN, M. A., HASANUZZAMAN, M., HOSSAIN, M. S., NATH, S. D., HOSSAIN, M. A., … HASANUZZAMAN, M. (2017). Exogenous Salicylic Acid-Mediated Physiological Responses and Improvement in Yield by Modulating Antioxidant Defense System of Wheat under Salinity. Notulae Scientia Biologicae, 9(2), 219-232. doi:10.15835/nsb929998Flowers, T. J., & Colmer, T. D. (2008). Salinity tolerance in halophytes*. New Phytologist, 179(4), 945-963. doi:10.1111/j.1469-8137.2008.02531.xGriffith, M., & Yaish, M. W. F. (2004). Antifreeze proteins in overwintering plants: a tale of two activities. Trends in Plant Science, 9(8), 399-405. doi:10.1016/j.tplants.2004.06.007Slama, I., Abdelly, C., Bouchereau, A., Flowers, T., & Savouré, A. (2015). Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany, 115(3), 433-447. doi:10.1093/aob/mcu239Chen, T. H. H., & Murata, N. (2008). Glycinebetaine: an effective protectant against abiotic stress in plants. Trends in Plant Science, 13(9), 499-505. doi:10.1016/j.tplants.2008.06.007Szabados, L., & Savouré, A. (2010). Proline: a multifunctional amino acid. Trends in Plant Science, 15(2), 89-97. doi:10.1016/j.tplants.2009.11.009ESFANDIARI, E., & GOHARI, G. (2017). Response of ROS-Scavenging Systems to Salinity Stress in Two Different Wheat (Triticum aestivum L.) Cultivars. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 45(1), 287-291. doi:10.15835/nbha45110682Apel, K., & Hirt, H. (2004). REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction. Annual Review of Plant Biology, 55(1), 373-399. doi:10.1146/annurev.arplant.55.031903.141701Miller, G., Shulaev, V., & Mittler, R. (2008). Reactive oxygen signaling and abiotic stress. Physiologia Plantarum, 133(3), 481-489. doi:10.1111/j.1399-3054.2008.01090.xLICHTENTHALER, H. K., & WELLBURN, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11(5), 591-592. doi:10.1042/bst0110591Weimberg, R. (1987). Solute adjustments in leaves of two species of wheat at two different stages of growth in response to salinity. Physiologia Plantarum, 70(3), 381-388. doi:10.1111/j.1399-3054.1987.tb02832.xBates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205-207. doi:10.1007/bf00018060DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956). Colorimetric Method for Determination of Sugars and Related Substances. Analytical Chemistry, 28(3), 350-356. doi:10.1021/ac60111a017Hodges, D. M., DeLong, J. M., Forney, C. F., & Prange, R. K. (1999). Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta, 207(4), 604-611. doi:10.1007/s004250050524Blainski, A., Lopes, G., & de Mello, J. (2013). Application and Analysis of the Folin Ciocalteu Method for the Determination of the Total Phenolic Content from Limonium Brasiliense L. Molecules, 18(6), 6852-6865. doi:10.3390/molecules18066852Zhishen, J., Mengcheng, T., & Jianming, W. (1999). The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemistry, 64(4), 555-559. doi:10.1016/s0308-8146(98)00102-2Gil, R., Bautista, I., Boscaiu, M., Lidon, A., Wankhade, S., Sanchez, H., … Vicente, O. (2014). Responses of five Mediterranean halophytes to seasonal changes in environmental conditions. AoB PLANTS, 6(0), plu049-plu049. doi:10.1093/aobpla/plu049Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254. doi:10.1016/0003-2697(76)90527-3Beyer, W. F., & Fridovich, I. (1987). Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Analytical Biochemistry, 161(2), 559-566. doi:10.1016/0003-2697(87)90489-1Aebi, H. (1984). [13] Catalase in vitro. Oxygen Radicals in Biological Systems, 121-126. doi:10.1016/s0076-6879(84)05016-3Connell, J. P., & Mullet, J. E. (1986). Pea Chloroplast Glutathione Reductase: Purification and Characterization. Plant Physiology, 82(2), 351-356. doi:10.1104/pp.82.2.351Metsalu, T., & Vilo, J. (2015). ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Research, 43(W1), W566-W570. doi:10.1093/nar/gkv468Del Rio, D., Stewart, A. J., & Pellegrini, N. (2005). A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutrition, Metabolism and Cardiovascular Diseases, 15(4), 316-328. doi:10.1016/j.numecd.2005.05.003Zhu, J.-K. (2001). Plant salt tolerance. Trends in Plant Science, 6(2), 66-71. doi:10.1016/s1360-1385(00)01838-0Munns, R., & Tester, M. (2008). Mechanisms of Salinity Tolerance. Annual Review of Plant Biology, 59(1), 651-681. doi:10.1146/annurev.arplant.59.032607.092911GANANÇA, J. F. T., FREITAS, J. G. R., NÓBREGA, H. G. M., RODRIGUES, V., ANTUNES, G., GOUVEIA, C. S. S., … LEBOT, V. (2018). Screening for Drought Tolerance in Thirty Three Taro Cultivars. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 46(1), 65-74. doi:10.15835/nbha46110950Schiop, S. T., Al Hassan, M., Sestras, A. F., Boscaiu, M., Sestras, R. E., & Vicente, O. (2017). Biochemical responses to drought, at the seedling stage, of several Romanian Carpathian populations of Norway spruce (Picea abies L. Karst). Trees, 31(5), 1479-1490. doi:10.1007/s00468-017-1563-1Melo, H. F. de, Souza, E. R. de, & Cunha, J. C. (2017). Fluorescence of chlorophyll a and photosynthetic pigments in Atriplex nummularia under abiotic stresses. Revista Brasileira de Engenharia Agrícola e Ambiental, 21(4), 232-237. doi:10.1590/1807-1929/agriambi.v21n4p232-237Kumar, D., Al Hassan, M., Naranjo, M. A., Agrawal, V., Boscaiu, M., & Vicente, O. (2017). Effects of salinity and drought on growth, ionic relations, compatible solutes and activation of antioxidant systems in oleander (Nerium oleander L.). PLOS ONE, 12(9), e0185017. doi:10.1371/journal.pone.0185017Santos, C. V. (2004). Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Scientia Horticulturae, 103(1), 93-99. doi:10.1016/j.scienta.2004.04.009Plesa, I. M., Al Hassan, M., González-Orenga, S., Sestras, A. F., Vicente, O., Prohens, J., … Sestras, R. E. (2019). Responses to Drought in Seedlings of European Larch (Larix decidua Mill.) from Several Carpathian Provenances. Forests, 10(6), 511. doi:10.3390/f10060511Munns, R., & Gilliham, M. (2015). Salinity tolerance of crops – what is the cost? New Phytologist, 208(3), 668-673. doi:10.1111/nph.13519Tang, X., Mu, X., Shao, H., Wang, H., & Brestic, M. (2014). Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Critical Reviews in Biotechnology, 35(4), 425-437. doi:10.3109/07388551.2014.889080MF, G., Li, N., TY, S., XH, L., Brestič, M., HB, S., … rki, S. (2016). Accumulation capacity of ions in cabbage (Brassica oleracea L.) supplied with sea water  . Plant, Soil and Environment, 62(No. 7), 314-320. doi:10.17221/771/2015-pseBogemans, J., Neirinckx, L., & Stassart, J. M. (1989). Effect of deicing chloride salts on ion accumulation in spruce (Picea abies (L.) sp.). Plant and Soil, 113(1), 3-11. doi:10.1007/bf02181915RAVEN, J. A. (1985). TANSLEY REVIEW No. 2. New Phytologist, 101(1), 25-77. doi:10.1111/j.1469-8137.1985.tb02816.xManishankar, P., Wang, N., Köster, P., Alatar, A. A., & Kudla, J. (2018). Calcium signaling during salt stress and in the regulation of ion homeostasis. Journal of Experimental Botany, 69(17), 4215-4226. doi:10.1093/jxb/ery201Greenway, H., & Munns, R. (1980). Mechanisms of Salt Tolerance in Nonhalophytes. Annual Review of Plant Physiology, 31(1), 149-190. doi:10.1146/annurev.pp.31.060180.001053Rodrı́guez-Navarro, A. (2000). Potassium transport in fungi and plants. Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, 1469(1), 1-30. doi:10.1016/s0304-4157(99)00013-1Almeida, D. M., Oliveira, M. M., & Saibo, N. J. M. (2017). Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genetics and Molecular Biology, 40(1 suppl 1), 326-345. doi:10.1590/1678-4685-gmb-2016-0106KAVI KISHOR, P. B., & SREENIVASULU, N. (2013). Is proline accumulationper secorrelated with stress tolerance or is proline homeostasis a more critical issue? Plant, Cell & Environment, 37(2), 300-311. doi:10.1111/pce.12157Ditmarova, L., Kurjak, D., Palmroth, S., Kmet, J., & Strelcova, K. (2009). Physiological responses of Norway spruce (Picea abies) seedlings to drought stress. Tree Physiology, 30(2), 205-213. doi:10.1093/treephys/tpp116Taïbi, K., del Campo, A. D., Vilagrosa, A., Bellés, J. M., López-Gresa, M. P., Pla, D., … Mulet, J. M. (2017). Drought Tolerance in Pinus halepensis Seed Sources As Identified by Distinctive Physiological and Molecular Markers. Frontiers in Plant Science, 8. doi:10.3389/fpls.2017.01202Hayat, S., Hayat, Q., Alyemeni, M. N., Wani, A. S., Pichtel, J., & Ahmad, A. (2012). Role of proline under changing environments. Plant Signaling & Behavior, 7(11), 1456-1466. doi:10.4161/psb.21949Gil, R., Boscaiu, M., Lull, C., Bautista, I., Lidón, A., & Vicente, O. (2013). Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Functional Plant Biology, 40(9), 805. doi:10.1071/fp12359Van Breusegem, F., Vranová, E., Dat, J. F., & Inzé, D. (2001). The role of active oxygen species in plant signal transduction. Plant Science, 161(3), 405-414. doi:10.1016/s0168-9452(01)00452-6Ahmad, P., Jaleel, C. A., Salem, M. A., Nabi, G., & Sharma, S. (2010). Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Critical Reviews in Biotechnology, 30(3), 161-175. doi:10.3109/07388550903524243Chan, Z., Yokawa, K., Kim, W.-Y., & Song, C.-P. (2016). Editorial: ROS Regulation during Plant Abiotic Stress Responses. Frontiers in Plant Science, 7. doi:10.3389/fpls.2016.01536Shi, Q., & Zhu, Z. (2008). Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environmental and Experimental Botany, 63(1-3), 317-326. doi:10.1016/j.envexpbot.2007.11.003Ashraf, M. (2009). Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnology Advances, 27(1), 84-93. doi:10.1016/j.biotechadv.2008.09.003Huang, H., Ullah, F., Zhou, D.-X., Yi, M., & Zhao, Y. (2019). Mechanisms of ROS Regulation of Plant Development and Stress Responses. Frontiers in Plant Science, 10. doi:10.3389/fpls.2019.00800Tuna, A. L., Kaya, C., Dikilitas, M., & Higgs, D. (2008). The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environmental and Experimental Botany, 62(1), 1-9. doi:10.1016/j.envexpbot.2007.06.007Harinasut, P., Poonsopa, D., Roengmongkol, K., & Charoensataporn, R. (2003). ScienceAsia, 29(2), 109. doi:10.2306/scienceasia1513-1874.2003.29.109Ashraf, M., & Ali, Q. (2008). Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L.). Environmental and Experimental Botany, 63(1-3), 266-273. doi:10.1016/j.envexpbot.2007.11.008Yang, Y., Han, C., Liu, Q., Lin, B., & Wang, J. (2008). Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings. Acta Physiologiae Plantarum, 30(4), 433-440. doi:10.1007/s11738-008-0140-zBen Amor, N., Ben Hamed, K., Debez, A., Grignon, C., & Abdelly, C. (2005). Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity. Plant Science, 168(4), 889-899. doi:10.1016/j.plantsci.2004.11.002Kangasjärvi, S., Lepistö, A., Hännikäinen, K., Piippo, M., Luomala, E.-M., Aro, E.-M., & Rintamäki, E. (2008). Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochemical Journal, 412(2), 275-285. doi:10.1042/bj20080030Lee, D. H., & Lee, C. B. (2000). Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Science, 159(1), 75-85. doi:10.1016/s0168-9452(00)00326-5Keleş, Y., & Öncel, I. (2002). Response of antioxidative defence system to temperature and water stress combinations in wheat seedlings. Plant Science, 163(4), 783-790. doi:10.1016/s0168-9452(02)00213-3Vital, S. A., Fowler, R. W., Virgen, A., Gossett, D. R., Banks, S. W., & Rodriguez, J. (2008). Opposing roles for superoxide and nitric oxide in the NaCl stress-induced upregulation of antioxidant enzyme activity in cotton callus tissue. Environmental and Experimental Botany, 62(1), 60-68. doi:10.1016/j.envexpbot.2007.07.006Naya, L., Ladrera, R., Ramos, J., González, E. M., Arrese-Igor, C., Minchin, F. R., & Becana, M. (2007). The Response of Carbon Metabolism and Antioxidant Defenses of Alfalfa Nodules to Drought Stress and to the Subsequent Recovery of Plants. Plant Physiology, 144(2), 1104-1114. doi:10.1104/pp.107.099648Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M., & Zheng, B. (2019). Response of Phenylpropanoid Pathway and the Role of Polyphenols in Plants under Abiotic Stress. Molecules, 24(13), 2452. doi:10.3390/molecules24132452KEBBAS, S., BENSEDDIK, T., MAKHLOUF, H., & AID, F. (2018). Physiological and Biochemical Behaviour of Gleditsia triacanthos L. Young Seedlings Under Drought Stress Conditions. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 46(2), 585-592. doi:10.15835/nbha4621106