2 research outputs found
Genetic Relationships and Reproductive Traits of Romanian Populations of Silver Fir (Abies alba): Implications for the Sustainable Management of Local Populations
No full text[EN] Assessment of the diversity of reproductive traits and genetic variation is of great relevance to the conservation of genetic resources and management of silver fir (Abies alba) populations. We have evaluated reproductive characteristics associated with female cones and seed morphology, as well as seed germination after subjecting seeds to five storage methods, in nine Romanian populations of A. alba. The genetic diversity of the populations was assessed with 12 polymorphic simple sequence repeat (SSR) markers. We detected significant differences between populations for all reproductive traits and considerable differences in seed germination and storage methods; seed storage in wet sand was the method resulting in the highest germination in all populations. Genomic SSRs (gSSRs) were more informative on average than expressed sequence tag SSRs (EST-SSRs) in the populations studied. The nine populations were genetically diverse, with an average number of alleles (N) per SSR locus between 3.50 and 4.83. The observed heterozygosity (Ho) in the nine populations was always lower than the expected heterozygosity (He), which resulted in values of the inbreeding coefficient (Fis) between 0.261 and 0.709. Genetic distances between populations ranged between 0.077 and 0.410. The cluster analysis based on genetic distances did not group accessions according to their geographical proximity, and despite a positive trend, the correlation between geographic and genetic distances was non-significant. The results of an analysis of molecular variance (AMOVA) revealed that only 9.1% of the total molecular variance is attributable to differences between populations. This low degree of genetic differentiation between populations is confirmed by the intermingling of individuals of different populations in a principal coordinate analysis (PCoA). We found evidence of a positive relationship between He and germination, as well as a negative one between Fis and germination, suggesting that populations with low diversity and high consanguinity may have a reduced fitness and long-term viability. The results are relevant for the conservation and management of local genetic resources and populations, as well as for reforestation programmes of silver fir.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. The first author (I.M.T.M.) is thankful to UPV (Valencia) and the Erasmus+ mobility programme, financed by the European Commission, for her scholarship in UPV. The research was partially supported by the Advanced Horticultural Research Institute of Transylvania (ICHAT), University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca (USAMVCN), and Polytechnic University of Valencia (UPV). Mariola Plazas is grateful to Generalitat Valenciana and Fondo Social Europeo for a post-doctoral grant (APOSTD/2018/014).Todea Morar, IM.; Rensen, S.; Vilanova Navarro, S.; Boscaiu, M.; Holonec, L.; Sestras, AF.; Vicente, O.... (2020). Genetic Relationships and Reproductive Traits of Romanian Populations of Silver Fir (Abies alba): Implications for the Sustainable Management of Local Populations. Sustainability. 12(10):1-15. https://doi.org/10.3390/su12104199S1151210Dering, M., Sękiewicz, K., Boratyńska, K., Litkowiec, M., Iszkuło, G., Romo, A., & Boratyński, A. (2014). Genetic diversity and inter-specific relations of western Mediterranean relic Abies taxa as compared to the Iberian A. alba. Flora - Morphology, Distribution, Functional Ecology of Plants, 209(7), 367-374. doi:10.1016/j.flora.2014.03.011Tinner, 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:10.1890/12-2231.1Dobrowolska, 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:10.1080/13416979.2017.1386021Todea (Morar), I. M., González-Orenga, S., Boscaiu, M., Plazas, M., Sestras, A. F., Prohens, J., … Sestras, R. E. (2020). Responses to Water Deficit and Salt Stress in Silver Fir (Abies alba Mill.) Seedlings. Forests, 11(4), 395. doi:10.3390/f11040395TODEA (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/nbha47411348Schutz, J.-P. (2002). Silvicultural tools to develop irregular and diverse forest structures. Forestry, 75(4), 329-337. doi:10.1093/forestry/75.4.329PLESA, I., DAN, C., TRUȚA, A., HOLONEC, L., SESTRAS, A. F., BOSCAIU, M., & SESTRAS, R. E. (2017). Spruce Trees Growth and Forest Landscape Depending on Microstational Factors and Ecological Conditions. Notulae Scientia Biologicae, 9(4), 582-588. doi:10.15835/nsb9410217SESTRAS, P., BONDREA, M. V., CETEAN, H., SĂLĂGEAN, T., BILAŞCO, Ş., NAȘ, S., … CÎMPEANU, S. M. (2018). Ameliorative, Ecological and Landscape Roles of Făget Forest, Cluj-Napoca, Romania, and Possibilities of Avoiding Risks Based on GIS Landslide Susceptibility Map. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 46(1), 292-300. doi:10.15835/nbha46110866Bončina, A., Simončič, T., & Rosset, C. (2019). Assessment of the concept of forest functions in Central European forestry. Environmental Science & Policy, 99, 123-135. doi:10.1016/j.envsci.2019.05.009Skrzyszewska, K., & Chłanda, J. (2009). A study on the variation of morphological characteristics of silver fir (Abies alba Mill.) seeds and their internal structure determined by X-ray radiography in the Beskid Sądecki and Beskid Niski mountain ranges of the Carpathians (southern Poland). Journal of Forest Science, 55(No. 9), 403-414. doi:10.17221/48/2008-jfsGradečki-Poštenjak, M. (2016). The influence of crown defoliation on the variability of some physiological and morphological properties of silver fir (Abies alba) seeds in the seed zone of Dinaric beech-fir forests in Croatia. Periodicum Biologorum, 117(4), 479-492. doi:10.18054/pb.2015.117.4.3428Gömöry, D., Paule, L., Krajmerová, D., Romšáková, I., & Longauer, R. (2012). Admixture of genetic lineages of different glacial origin: a case study of Abies alba Mill. in the Carpathians. Plant Systematics and Evolution, 298(4), 703-712. doi:10.1007/s00606-011-0580-6Postolache, D., Leonarduzzi, C., Piotti, A., Spanu, I., Roig, A., Fady, B., … Vendramin, G. G. (2013). Transcriptome versus Genomic Microsatellite Markers: Highly Informative Multiplexes for Genotyping Abies alba Mill. and Congeneric Species. Plant Molecular Biology Reporter, 32(3), 750-760. doi:10.1007/s11105-013-0688-7De Luca, D., Menale, B., Caputo, P., & Cennamo, P. (2016). Population genetics analysis in a relic population of silver fir (Abies alba Mill.) in southern Italy: A comparison with microsatellites and reference data. Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, 151(4), 567-573. doi:10.1080/11263504.2016.1186124Belletti, P., Ferrazzini, D., Ducci, F., De Rogatis, A., & Mucciarelli, M. (2017). Genetic diversity of Italian populationsof Abies alba. Dendrobiology, 77, 147-159. doi:10.12657/denbio.077.012Popovic, V., Lucic, A., Rakonjac, L., Milovanovic, J., Mladenovic-Drinic, S., & Ristic, D. (2019). Application of SSR markers for assessment of genetic differentiation of silver fir (Abies alba Mill.) originating from Javor mountain. ABI Genetika, 51(3), 1103-1112. doi:10.2298/gensr1903103pPopovic, V., Lucic, A., Rakonjac, L., Cvjetkovic, B., Mladenovic-Drinic, S., & Ristic, D. (2017). Assessment of genetic diversity of silver fir (Abies alba Mill.) in Serbia using SSR markers. ABI Genetika, 49(3), 979-988. doi:10.2298/gensr1703979pDonohue, K., Rubio de Casas, R., Burghardt, L., Kovach, K., & Willis, C. G. (2010). Germination, Postgermination Adaptation, and Species Ecological Ranges. Annual Review of Ecology, Evolution, and Systematics, 41(1), 293-319. doi:10.1146/annurev-ecolsys-102209-144715Slate, J., David, P., Dodds, K. G., Veenvliet, B. A., Glass, B. C., Broad, T. E., & McEwan, J. C. (2004). Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity, 93(3), 255-265. doi:10.1038/sj.hdy.6800485Caudullo, G., Welk, E., & San-Miguel-Ayanz, J. (2017). Chorological maps for the main European woody species. Data in Brief, 12, 662-666. doi:10.1016/j.dib.2017.05.007HANSEN, O. K., VENDRAMIN, G. G., SEBASTIANI, F., & EDWARDS, K. J. (2005). Development of microsatellite markers in Abies nordmanniana (Stev.) Spach and cross-species amplification in the Abies genus. Molecular Ecology Notes, 5(4), 784-787. doi:10.1111/j.1471-8286.2005.01062.xCREMER, E., LIEPELT, S., SEBASTIANI, F., BUONAMICI, A., MICHALCZYK, I. M., ZIEGENHAGEN, B., & VENDRAMIN, G. G. (2006). Identification and characterization of nuclear microsatellite loci in Abies alba Mill. Molecular Ecology Notes, 6(2), 374-376. doi:10.1111/j.1471-8286.2005.01238.xPeakall, R., & Smouse, P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research--an update. Bioinformatics, 28(19), 2537-2539. doi:10.1093/bioinformatics/bts460Jombart, T., & Ahmed, I. (2011). adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics, 27(21), 3070-3071. doi:10.1093/bioinformatics/btr521Kamvar, Z. N., Tabima, J. F., & Grünwald, N. J. (2014). Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2, e281. doi:10.7717/peerj.281Schliep, K., Potts, A. J., Morrison, D. A., & Grimm, G. W. (2017). Intertwining phylogenetic trees and networks. Methods in Ecology and Evolution, 8(10), 1212-1220. doi:10.1111/2041-210x.12760Nei, M. (1972). Genetic Distance between Populations. The American Naturalist, 106(949), 283-292. doi:10.1086/282771Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131(2), 479-491. doi:10.1093/genetics/131.2.479Verdú, M., & Traveset, A. (2005). EARLY EMERGENCE ENHANCES PLANT FITNESS: A PHYLOGENETICALLY CONTROLLED META-ANALYSIS. Ecology, 86(6), 1385-1394. doi:10.1890/04-1647Sorensen, F. C. (1999). RELATIONSHIP BETWEEN SELF-FERTILITY, ALLOCATION OF GROWTH, AND INBREEDING DEPRESSION IN THREE CONIFEROUS SPECIES. Evolution, 53(2), 417-425. doi:10.1111/j.1558-5646.1999.tb03777.xRajora, O. P., & Mosseler, A. (2001). Euphytica, 118(2), 197-212. doi:10.1023/a:1004150525384Kaliniewicz, Z., Markowski, P., Anders, A., Jadwisieńczak, K., Żuk, Z., & Krzysiak, Z. (2019). Physical Properties of Seeds of Eleven Fir Species. Forests, 10(2), 142. doi:10.3390/f10020142Cremer, E., Ziegenhagen, B., Schulerowitz, K., Mengel, C., Donges, K., Bialozyt, R., … Liepelt, S. (2012). Local seed dispersal in European silver fir (Abies alba Mill.): lessons learned from a seed trap experiment. Trees, 26(3), 987-996. doi:10.1007/s00468-012-0676-9Carles, S., Lamhamedi, M. S., Beaulieu, J., Stowe, D. C., Colas, F., & Margolis, H. A. (2009). Genetic Variation in Seed Size and Germination Patterns and their Effect on White Spruce Seedling Characteristics. Silvae Genetica, 58(1-6), 152-161. doi:10.1515/sg-2009-0020Bussotti, F., Pollastrini, M., Holland, V., & Brüggemann, W. (2015). Functional traits and adaptive capacity of European forests to climate change. Environmental and Experimental Botany, 111, 91-113. doi:10.1016/j.envexpbot.2014.11.006Teodosiu, M., Mihai, G., Fussi, B., & Ciocîrlan, E. (2019). Genetic diversity and structure of Silver fir (Abies alba Mill.) at the south-eastern limit of its distribution range. Annals of Forest Research, 62(2), 139. doi:10.15287/afr.2019.1436Pandey, M. K., Gautami, B., Jayakumar, T., Sriswathi, M., Upadhyaya, H. D., Gowda, M. V. C., … Varshney, R. K. (2011). Highly informative genic and genomic SSR markers to facilitate molecular breeding in cultivated groundnut (Arachis hypogaea). Plant Breeding, 131(1), 139-147. doi:10.1111/j.1439-0523.2011.01911.xMartin, M. A., Mattioni, C., Cherubini, M., Taurchini, D., & Villani, F. (2010). Genetic diversity in European chestnut populations by means of genomic and genic microsatellite markers. Tree Genetics & Genomes, 6(5), 735-744. doi:10.1007/s11295-010-0287-9Muñoz-Falcón, J. E., Vilanova, S., Plazas, M., & Prohens, J. (2011). Diversity, relationships, and genetic fingerprinting of the Listada de Gandía eggplant landrace using genomic SSRs and EST-SSRs. Scientia Horticulturae, 129(2), 238-246. doi:10.1016/j.scienta.2011.03.034Nandha, P. S., & Singh, J. (2013). Comparative assessment of genetic diversity between wild and cultivated barley using gSSR and EST-SSR markers. Plant Breeding, 133(1), 28-35. doi:10.1111/pbr.12118VILCAN (TRUTA), A., MIHALTE (CRISAN), L., SESTRAS, A. F., HOLONEC, L., & SESTRAS, R. E. (2017). Genetic variation and potential genetic resources of several Romanian larch populations. TURKISH JOURNAL OF AGRICULTURE AND FORESTRY, 41, 82-91. doi:10.3906/tar-1610-57GRAMAZIO, P., PLESA, I. M., TRUTA, A. M., SESTRAS, A. F., VILANOVA, S., PLAZAS, M., … SESTRAS, R. E. (2018). Highly informative SSR genotyping reveals large genetic diversity and limited differentiation in European larch (Larixdecidua) populations from Romania. TURKISH JOURNAL OF AGRICULTURE AND FORESTRY, 42(3), 165-175. doi:10.3906/tar-1801-4
Responses to Water Deficit and Salt Stress in Silver Fir (Abies alba Mill.) Seedlings
No full text[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
