Effect of Drought Stress on Physio-biochemical Traits and Secondary Metabolites Production in the Woody Species Pinus Halepensis Mill. At a Juvenile Development Stage

References

• Abrams, M. D. (1988). Sources of variation in osmotic potentials with special reference to North American tree species. Forest Science, 34(4), 1030–1046 .
   Web of Science ®Google Scholar
• Abrams, M. D., Kubiske, M. E., & Steiner, K. C. (1990). Drought adaptations and responses in five genotypes of Fraxinus pennsylvanica Marsh.: Photosynthesis, water relations and leaf morphology. Tree Physiology, 6(3), 305–315. https://doi.org/10.1093/treephys/6.3.305
   PubMed Web of Science ®Google Scholar
• Agati, G., & Tattini, M. (2010). Multiple functional roles of flavonoids in photoprotection. New Phytologist, 186(4), 786–793. https://doi.org/10.1111/j.1469-8137.2010.03269.x
   PubMed Web of Science ®Google Scholar
• Aron, D. (1949). Copper enzymes isolated chloroplasts, polyphenoloxidase in Beta vulgaris. Plant Physiology, 24(1), 1–15. https://doi.org/10.1104/pp.24.1.1
   PubMed Web of Science ®Google Scholar
• Ayari, A., Moya, D., Rejeb, M. N., Ben Mansoura, A., Albouchi, A., De Las Heras, J., Fezzani, T., & Henchi, B. (2011). Geographical variation on cone and seed production of natural Pinus halepensis Mill. forests in Tunisia. Journal of Arid Environments, 75(5), 403–410. https://doi.org/10.1016/j.jaridenv.2011.01.001
   Web of Science ®Google Scholar
• Ayari, A., Zubizarreta-Gerendiain, A., Tome, M., Tome, J., Garchi, S., & Henchi, B. (2012). Stand, tree and crown variables affecting cone crop and seed yield of Aleppo pine forests in different bioclimatic regions of Tunisia. Forest Systems, 21(1), 128–140. https://doi.org/10.5424/fs/2112211-11463
   Web of Science ®Google Scholar
• Bachtobji, B. B., Khorchani, A., Guibal, F., El Aouni, M. H., & Khaldi, A. (2017). Dendroecological study of Pinus halepensis and Pinus pinea in northeast coastal dunes in Tunisia according to distance from the shoreline and dieback intensity. Dendrochronologia, 45, 62–72. https://doi.org/10.1016/j.dendro.2017.06.008
   Web of Science ®Google Scholar
• Bahreininejad, B., Razmjoo, J., & Mirza, M. (2014). Effect of water stress on productivity and essential oil content and composition of Thymus carmanicus. Journal of Essential Oil Bearing Plants, 17(5), 717–725. https://doi.org/10.1080/0972060X.2014.901605
   Web of Science ®Google Scholar
• Bates, 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. http://www.jstor.org/stable/42932378
   Web of Science ®Google Scholar
• Bistgani, Z. E., Siadat, S. A., Bakhshandeh, A., Pirbalouti, A. G., & Hashemi, M. (2017). Interactive effects of drought stress and chitosan application on physiological characteristics and essential oil yield of Thymus daenensis Celak. The Crop Journal, 5(5), 407–415. https://doi.org/10.1016/j.cj.2017.04.003
   Google Scholar
• Biswas, S., Koul, M., & Bhatnagar, A. K. (2011). Effect of salt, drought and metal stress on essential oil yield and quality in plants. Natural Product Communications, 6(10), 1559–1564. https://doi.org/10.1177/1934578X1100601036
   PubMed Web of Science ®Google Scholar
• Bongarten, B. C., & Teskey, R. O. (1986). Water relations of loblolly pine seedlings from diverse geographic origins. Tree Physiology, 1(3), 265–276. https://doi.org/10.1093/treephys/1.3.265
   PubMed Web of Science ®Google Scholar
• Borghetti, M., Leonardi, S., Raschi, A., Snyderman, D., & Tognetti, R. (1993). Ecotypic variation of xylem embolism, phenological traits, growth parameters and allozyme characteristics in Fagus sylvatica. Functional Ecology, 7(6), 713–720. https://doi.org/10.2307/2390193
   Web of Science ®Google Scholar
• Braatne, J. H., Hinckley, T. M., & Stettler, R. F. (1992). Influence of soil water on the physiological and morphological components of plant water balance in Populus trichocarpa, Populus deltoides and their F1 hybrids. Tree Physiology, 11(4), 325–339. https://doi.org/10.1093/treephys/11.4.325
   PubMed Web of Science ®Google Scholar
• Bradford, 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. https://doi.org/10.1016/0003-2697(76)90527-3
   PubMed Web of Science ®Google Scholar
• Cakmak, I., & Marschner, H. (1992). Magnesium Deficiency and High Light Intensity Enhance Activities of Superoxide Dismutase, Ascorbate Peroxidase, and Glutathione Reductase in Bean Leaves. Plant Physiology, 98(4), 1222–1227. https://doi.org/10.1104/pp.98.4.1222
   PubMed Web of Science ®Google Scholar
• Calamassi, R. (1986). Caractérisation de quelques provenances de Pinus halepensis sur la base de la structure anatomique et morphologique des aguilles. Annals of Forest Science, 43(3), 281–289. https://doi.org/10.1051/forest:19860301
   Google Scholar
• Caser, M., Demasi, S., Victorino, Í. M. M., Donno, D., Faccio, A., Lumini, E., Bianciotto, V., & Scariot, V. (2019). Arbuscular mycorrhizal fungi modulate the crop performance and metabolic profile of saffron in soilless cultivation. Agronomy, 9(5), 232. https://doi.org/10.3390/agronomy9050232
   Web of Science ®Google Scholar
• Chakroun, M. L. (1986). Le pin d’Alep en Tunisie. Le pin d’Alep et le pin brutia dans la sylviculture méditerranéenne. CIHEAM.
   Google Scholar
• Chaves, M. M., Maroco, J. P., & Pereira, J. S. (2003). Understanding plant responses to drought—from genes to the whole plant. Functional Plant Biology, 30(3), 239–264. https://doi.org/10.1071/FP02076
   PubMed Web of Science ®Google Scholar
• Cheikh-Rouhou, S., Hentati, B., Besbes, S., Blecker, C., Deroanne, C., & Attia, H. (2006). Chemical Composition and Lipid Fraction Characteristics of Aleppo Pine (Pinus halepensis Mill.) Seeds Cultivated in Tunisia. Food Science and Technology International, 12(5), 407–416. https://doi.org/10.1177/1082013206069910
   Web of Science ®Google Scholar
• Cherif, S., Ezzine, O., Khouja, M. L., & Nasr, Z. (2019). Hydraulic traits performances of three pine species in Tunisia. Journal of Agricultural Science, 11(13), 20–29. https://doi.org/10.5539/jas.v11n13p20
   Google Scholar
• Cochard, H. (1992). Vulnerability of several conifers to air embolism. Tree Physiology, 11(1), 73–83. https://doi.org/10.1093/treephys/11.1.73
   PubMed Web of Science ®Google Scholar
• Delauney, A. J., & Verma, D. P. S. (1990). A soybean gene encoding pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Molecular General Genetics, 221(3), 299–305. https://doi.org/10.1007/BF00259392
   PubMedGoogle Scholar
• Deligoz, A., & Gur, M. (2015). Morphological, physiological and biochemical responses to drought stress of stone pine (Pinus pinea L.) seedlings. Acta Physiologiae Plantarum, 37(11), 243. https://doi.org/10.1007/s11738-015-1998-1
   Web of Science ®Google Scholar
• Djeridane, A., Yousfi, M., Nadjemi, B., Boutassouna, D., Stocker, P., & Vidal, N. (2006). Antioxidant activity of some algerian medicinal plants extracts containing phenolic compounds. Food Chemistry, 97(4), 654–660. https://doi.org/10.1016/j.foodchem.2005.04.028
   Web of Science ®Google Scholar
• El Guemri, R., Jaouadi, W., Mechergui, K., Alsubeie, M., Naghmouchi, S., El Ouellani, S., & Khouja, M. L. (2019). Morphological characteristics and variation of wood, cone and seed productions in the reforestation of Aleppo pine in Northeastern Tunisia using terrestrial and spatial index approaches. Ekológia, 38(3), 273–291. https://doi.org/10.2478/eko-2019-0021
   Google Scholar
• Elaieb, M., Candelier, K., Pétrissans, A., Dumarçay, S., Gérardin, P., & Pétrissans, M. (2015). Heat treatment of Tunisian soft wood species: Effect on the durability, chemical modifications and mechanical properties. Maderas: Ciencia y tecnología, 17(4), 699–710. http://dx.doi.org/10.4067/S0718-221X2015005000061
   Web of Science ®Google Scholar
• Falusi, M., Calamassi, R., & Tocci, A. (1983). Sensitivity of seed germination and seedling root growth to moisture stress in four provenances of Pinus halepensis Mill. Silvae Genetica, 32(1–2), 4–9.
   Web of Science ®Google Scholar
• Fekih, N., Allali, H., Merghache, S., Chaïb, F., Merghache, D., El Amine, M., Djabou, N., Muselli, A., Tabti, B., & Costa, J. (2014). Chemical composition and antibacterial activity of Pinus halepensis Miller growing in West Northern of Algeria. Asian Pacific Journal of Tropical Disease, 4(2), 97. https://doi.org/10.1016/S2222-1808(14)60323-6
   Google Scholar
• Flexas, J., Bota, J., Loreto, F., Cornic, G., & Sharkey, T. D. (2004). Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology, 6(3), 269–279. https://doi.org/10.1055/s-2004-820867
   PubMed Web of Science ®Google Scholar
• Galmés, J., Medrano, H., & Flexa, F. (2007). Limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytologist, 175(1), 81–93. https://doi.org/10.1111/j.1469-8137.2007.02087.x
   PubMed Web of Science ®Google Scholar
• Gharibi, S., Tabatabaei, B. E., Saeidi, G., & Goli, S. A. (2016). Effect of drought stress on total phenolic, lipid peroxidation, and antioxidant activity of achillea species. Biotechnology and Applied Biochemistry, 178(4), 796–809. https://doi.org/10.1007/s12010-015-1909-3
   Web of Science ®Google Scholar
• Ghazghazi, H., Essghaier, B., Jawadi, I., Riahi, L., Ben Salem, R., & Rigane, G. (2021b). Effects of fruit maturity stages on GC-FID fatty acid profiles, phenolic contents, and biological activities of Eucalyptus marginata L. Journal of Food Quality, 2021, 5546969. https://doi.org/10.1155/2021/5546969
   Web of Science ®Google Scholar
• Ghazghazi, H., Fkiri, S., Zouaoui, R., El Aloui, M., & Nasr, Z. (2021a). Intraspecific variability to drought impacts In Pinus Halepensis Provenances Trials. Journal of Sustainable Forestry, 40(7), 721–732. https://doi.org/10.1080/10549811.2020.1813595
   Web of Science ®Google Scholar
• Grossnickle, S. C. (2012). Why seedlings survive: Influence of plant. attributes. New Forests, 43(5–6), 711–738. https://doi.org/10.1007/s11056-012-9336-6
   Web of Science ®Google Scholar
• Gur, A., Demirel, U., Ozden, M., Kahraman, A., & Copur, O. (2010). Diurnal gradual heat stress affects antioxidant enzymes, proline accumulation and some physiological components in cotton (Gossypium hirsutum L.). African Journal of Biotechnology, 9(7), 1008–1015. https://doi.org/10.5897/AJB09.1590
   Google Scholar
• Hameed, A., Goher, M., & Iqbal, N. (2012). Heat stress induced cell death, changes in antioxidants, lipid peroxidation and protease activity in wheat leaves. Journal of Plant Growth Regulation, 31(3), 283–291. https://doi.org/10.1007/s00344-011-9238-4
   Web of Science ®Google Scholar
• Hare, P. D., Cress, W. A., & Staden, J. V. (2002). Dissecting the roles of osmolyte accumulation during stress. Plant, Cell & Environment, 21(6), 535–553. https://doi.org/10.1046/j.1365-3040.1998.00309.x
   Google Scholar
• Hassanpour, H., Khavari-Nejad, R. A., Niknam, V., Razavi, K., & Najaf, F. (2014). Effect of penconazole and drought stress on the essential oil composition and gene expression of Mentha pulegium L. (Lamiaceae) at flowering stage. Acta Physiologiae Plantarum, 36(5), 1167–1175. https://doi.org/10.1007/s11738-014-1492-1
   Web of Science ®Google Scholar
• He, Y., & Huang, B. (2010). Differential responses to heat stress in activities and isozymes of four antioxidant enzymes for two cultivars of Kentucky bluegrass contrasting in heat tolerance. Journal of the American Society for Horticultural Science, 135(2), 116–124. https://doi.org/10.21273/JASHS.135.2.116
   Web of Science ®Google Scholar
• Jackson, G. E., Irvine, J., & Grace, J. (1995). Xylem cavitation in Scots pine and Sitka spruce saplings during water stress. Tree Physiology, 15(12), 783–790. https://doi.org/10.1093/treephys/15.12.783
   Web of Science ®Google Scholar
• Jeddi, K., & Chaieb, M. (2010). Soil properties and plant community in different aged Pinus halepensis Mill. plantations in arid Mediterranean areas: The case of Southern Tunisia. Land Degradation & Development, 21(1), 32–39. https://doi.org/10.1002/ldr.964
   Web of Science ®Google Scholar
• Jeddi, K., Cortina, J., & Chaieb, M. (2009). Acacia salicina, Pinus halepensis and Eucalyptus occidentalis improve soil surface conditions in arid southern Tunisia. Journal of Arid Environments, 73(11), 1005–1013. https://doi.org/10.1016/j.jaridenv.2009.05.005
   Web of Science ®Google Scholar
• Kaundun, S. S., Lebreton, P., & Fady, B. (1998). Geographical variability of Pinus halepensis Mill. as revealed by foliar flavonoids. Biochemical Systematics and Ecology, 26(1), 83–96. https://doi.org/10.1016/S0305-1978(97)00092-6
   Web of Science ®Google Scholar
• Kemble, A. R., & MacPherson, H. T. (1954). Liberation of amino acids in perennial rye grass during wilting. Biochemical Journal, 58(1), 46–49. https://doi.org/10.1042/bj0580046
   PubMed Web of Science ®Google Scholar
• Khalil, T. M., Ajmal, M., Zeb, I., & Khan, M. A. (2020). Estimating impact of salinity on soil water potential dynamics using a novel approach. Journal of Engineering and Applied Sciences, 39(2), 154–163. https://doi.org/10.17582/journal.jeas/39.2.154.163
   Google Scholar
• Kishor, P. B. K., Hong, Z., Miao, G. H., Hu, C. A. A., & Verma, D. P. S. (1995). Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiology, 108(4), 1387–1394. https://doi.org/10.1104/pp.108.4.1387
   PubMed Web of Science ®Google Scholar
• Kraus, T. E., Mckersie, B. D., & Fletcher, R. A. (1995). Paclobutrazole induced tolerance of wheat leaves to paraquat may involve antioxidant enzyme activity. Journal of Plant Physiology, 145(4), 570–576. https://doi.org/10.1016/S0176-1617(11)81790-6
   Web of Science ®Google Scholar
• Le Houérou, H. N. (2000). Restoration and rehabilitation of arid and semiarid Mediterranean ecosystems in North Africa andWest Asia: A review. Arid Soil Research and Rehabilitation, 14(1), 3–14. https://doi.org/10.1080/089030600263139
   Google Scholar
• Mafakheri, A. B., Siosemardeh, P. C., Bahramnejad, Y., Struik, T., & Sohrabi, S. (2010). Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Australian Journal of Crop Science, 4(8), 580–585.
   Web of Science ®Google Scholar
• Minervini, F., Missaoui, J., Celano, G., Calasso, M., Achour, L., Saidane, D., Gobbetti, M., & De Angelis, M. (2020). Use of Autochthonous Lactobacilli to Increase the Safety of Zgougou. Microorganisms, 8(1), 29. https://doi.org/10.3390/microorganisms8010029
   Web of Science ®Google Scholar
• Mohammadi, H., Akhondzadeh, M., Ghorbanpour, M., & Aghaee, A. (2020). Physiological responses and secondary metabolite ingredients in sage plants induced by 24-epibrassinolide foliar application under different water deficit regimes. Scientia Horticulturae, 263, 109139. https://doi.org/10.1016/j.scienta.2019.109139
   Web of Science ®Google Scholar
• Riahi, L., Chakroun, H., Klay, I., Masmoudi, A. S., Cherif, A., & Zoghlami, N. (2019). Metabolomic fingerprint of Mentha rotundifolia L. leaf tissues promotes this species as a potential candidate for sustainable production of biologically active molecules. Journal of Complementary & Integrative Medicine, 16(2), 20180048. https://doi.org/10.1515/jcim-2018-0048
   Google Scholar
• Riahi, L., Cherif, H., Miladi, S., Neifar, M., Bejaoui, B., Chouchane, H., Masmoudi, A. S., & Cherif, A. (2020). Use of plant growth promoting bacteria as an efficient biotechnological tool to enhance the biomass and secondary metabolites production of the industrial crop Pelargonium graveolens L’Hér. under semi-controlled conditions. Industrial Crops and Products, 154, 112721. https://doi.org/10.1016/j.indcrop.2020.112721
   Web of Science ®Google Scholar
• Saad, H., Khoukh, A., Ayed, N., Charrier, B., & Charrier-elbouhtoury, F. (2014). Characterization of Tunisian Aleppo pine tannins for a potential use in wood adhesive formulation. Industrial Crops and Products, 61, 517–525. https://doi.org/10.1016/j.indcrop.2014.07.035
   Web of Science ®Google Scholar
• Sangwan, N. S., Farooqi, A. H. A., Shabih, F., & Sangwan, R. S. (2001). Regulation of essential oil production in plants. Plant Growth Regulation, 34, 3–21. https://doi.org/10.1023/A:1013386921596
   Web of Science ®Google Scholar
• Sarke, U., & Oba, S. (2018). Drought stress effects on growth, ROS markers, compatible solutes, phenolics, flavonoids, and antioxidant activity in Amaranthus tricolor. Applied Biochemistry and Biotechnology, 186(4), 999–1016. https://doi.org/10.1007/s12010-018-2784-5
   PubMed Web of Science ®Google Scholar
• Shumway, D. L., Steiner, K. C., & Abrams, M. D. (1991). Effects of drought stress on hydraulic architecture of seedlings from five populations of green ash. Canadian Journal of Botany, 69(10), 2158–2164. https://doi.org/10.1139/b91-270
   Google Scholar
• Singleton, V. L., & Rosi, J. A. (1965). Colorimetry of total phenolics with phosphomolybdic–phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16(3), 144–158.
   Google Scholar
• Smirnoff, N. (1993). The role of active oxygen in the response of plants to water deficit and desiccation. New Phytology, 125(1), 27–58. https://doi.org/10.1111/j.1469-8137.1993.tb03863.x
   PubMed Web of Science ®Google Scholar
• Srinivas, N., Rashmi, K., & Raghavarao, K. (1999). Extraction and purification of a plant peroxidase by aqueous two-phase extraction coupled with gel filtration. Process Biochemistry, 35(1–2), 43–48. https://doi.org/10.1016/S0032-9592(99)00030-8
   Web of Science ®Google Scholar
• Sultan, M. A. R. F., Hui, L., Yang, L. J., & Xian, Z. H. (2012). Assessment of drought tolerance of some Triticum L. species through physiological indices. Czech Journal of Genetics and Plant Breeding, 48(4), 178–184. https://doi.org/10.17221/21/2012-CJGPB
   Web of Science ®Google Scholar
• Sun, B., Ricardo-da-silva, J. M., & Spranger, I. (1998). Critical factors of vanillin assay for catechins and proanthocyanidins. Journal of Agricultural and Food Chemistry, 46(10), 4267–4274. https://doi.org/10.1021/jf980366j
   Web of Science ®Google Scholar
• Szabados, L., & Savouré, A. (2010). Proline: A multifunctional amino acid. Trends in Plant Science, 15(2), 89–97. https://doi.org/10.1016/j.tplants.2009.11.009
   PubMed Web of Science ®Google Scholar
• Taïbi, K., Del Campo, A. D., Aguado, A., & Mulet, J. M. (2015). The effect of genotype by environment interaction, phenotypic plasticity and adaptation on Pinus halepensis reforestation establishment under expected climate drifts. Ecological Engineering, 84, 218–228. https://doi.org/10.1016/j.ecoleng.2015.09.005
   Web of Science ®Google Scholar
• Taïbi, K., Del Campo, A. D., Mulet, J. M., Flors, J., & Aguado, A. (2014). Testing Aleppo pine seed sources response to climate change by using trial sites reflecting future conditions. New Forests, 45(5), 603–624. https://doi.org/10.1007/s11056-014-9423-y
   Web of Science ®Google Scholar
• Tsitsoni, T. K. (2009). Seed quality characteristics of Pinus halepensis – Seed germination strategy and early seedling growth. Web Ecology, 9(1), 72–76. https://doi.org/10.5194/we-9-72-2009
   Google Scholar
• Turner, N. C. (1981). Techniques and experimental approaches for the measurement of plant water status. Plant and Soil, 58(1–3), 339–366. https://doi.org/10.1007/BF02180062
   Web of Science ®Google Scholar
• Villar-Salvador, P., Peñuelas, J. L., Nicolás-Peragón, J. L., & Domínguez-Lerena, S. (2013). Is nitrogen fertilization in the nursery a suitable tool for enhancing the performance of Mediterranean oak plantations? New Forests, 44(5), 733–751. https://doi.org/10.1007/s11056-013-9374-8
   Web of Science ®Google Scholar
• Wang, J., Ives, N. E., & Lechowicz, M. J. (1992). The relation of foliar phenology to xylem embolism in trees. Functional Ecology, 6(4), 469–475. https://doi.org/10.2307/2389285
   Web of Science ®Google Scholar
• Wang, Z., Li, G., Sun, H., Ma, L., Guo, Y., Zhao, Z., Gao, H., & Mei, L. (2018). Effects of drought stress on photosynthesis and photosynthetic electron transport chain in young apple tree leaves. Biology Open, 7(11), bio035279. https://doi.org/10.1242/bio.035279
   PubMed Web of Science ®Google Scholar
• White, D. A., Turner, N. C., & Galbraith, J. H. (2000). Leaf water relations and stomatal behavior of four allopatric Eucalyptus species planted in Mediterranean southwestern Australia. Tree Physiology, 20(17), 1157–1165. https://doi.org/10.1093/treephys/20.17.1157
   PubMed Web of Science ®Google Scholar
• Xiong, L., & Zhu, J. K. (2002). Molecular and genetic aspects of plant responses to osmotic stress. Plant, Cell & Environment, 25(2), 131–139. https://doi.org/10.1046/j.1365-3040.2002.00782.x
   PubMed Web of Science ®Google Scholar
• Yemm, E. W., & Willis, A. J. (1954). The estimation of carbohydrates in plant extracts by anthrone. Biochemical Journal, 57(3), 508–514. https://doi.org/10.1042/bj0570508
   PubMed Web of Science ®Google Scholar
• Zahir, A., Abbasi, B. H., Adil, M., Anjum, S., Zia, & Ihsan-Ul-Haq, M. (2014). Synergistic effects of drought stress and photoperiods on phenology and secondary metabolism of Silybum marianum. Applied Biochemistry and Biotechnology, 174(2), 693–707. https://doi.org/10.1007/s12010-014-1098-5
   PubMed Web of Science ®Google Scholar