بررسی تغییرات میزان رنگیزه‌های فتوسنتزی، قندهای محلول، ترکیبات فلاونوئیدی و آنتوسیانینی در دو گیاه هالوفیت Salsola dendroides Pall. وLimonium reniforme (Girard) Lincz. در فصول مختلف
محورهای موضوعی : ژنتیک
سپیده بخشی
1
,
حسین عباس پور
2
,
سکینه سعیدی سار
3
1 - گروه زیست‌شناسی، واحد دامغان، دانشگاه آزاد اسلامی، دامغان، ایران
2 - گروه زیست‌شناسی، واحد دامغان، دانشگاه آزاد اسلامی، دامغان، ایران
3 - گروه زیست‌شناسی، واحد دامغان، دانشگاه آزاد اسلامی، دامغان، ایران
کلید واژه: شوری, تنش, تغییرات فصلی, هالوفیت, مکانیسم بردباری,
چکیده مقاله :
در گیاهان مکانیسم‌های بیوشیمیایی و مولکولی متعددی برای مقابله با تنش شوری ایجاد شده است که می‌توان به تغییر محتوای اسمولیت‌ها، افزایش میزان ترکیبات فنلی و حمایت از فعالیت فتوسنتزی اشاره کرد. این مکانیسم‌ها منجر به محصولات و فرایندهایی می‌گردد که تحمل به شوری را بهبود می‌بخشند. لذا نظر به اینکه کار تحقیقاتی قابل توجهی در زمینه مکانیسم‌های مقاومتی گونه‌های Salsola dendroides pall وLimonium reniforme (Girard)Lincz. انجام نشده است، برای پی بردن به مکانیسم فیزیولوژیکی بردباری این گیاهان تحت تنش اعمال شده به صورت طبیعی در فصول مختلف برخی از تغییرات فیزیولوژیکی گیاهان فوق مورد بررسی قرار گرفت. بدین منظور، گونه‌های مورد مطالعه از منطقه اینچه‌برون واقع در شمال گرگان به صورت کاملاً تصادفی با چهار تکرار در سه فصل بهار، تابستان و پاییز جمع‌آوری شدند. نتایج نشان داد که با افزایش دما و شوری در فصل تابستان محتوای رنگیز‌های کلروفیلی در هر دو گونه به صورت معنی‌داری کاهش یافت. میزان قندهای محلول در اندام هوایی وریشه گیاه S. dendroides در فصل بهار نسبت به دو فصل دیگر و در گیاهL. reniformeدرفصل تابستان نسبت به فصل بهار افزایش معنی‌داری داشت. در تابستان نیز میزان ترکیبات فلاونوئیدی در اندام هوایی و ریشه گیاهان مورد مطالعه به صورت معنی‌داری در مقایسه با سایر فصول افزایش نشان داد. میزان آنتوسیانینی نیز به صورت معنی‌داری با تغییر فصل تغییر یافت، به‌طوری‌که بیشترین میزان تجمع آنتوسیانین‌ها در اندام هوایی و ریشه گیاه S. dendroides در فصل پاییز و در گیاه L. reniforme در فصل تابستان مشاهده شد که اغلب این تغییرات در ارتباط با فعالسازی فرایندهای فیزیولوژیکی و بیوشیمیایی که به گیاه امکان سازگاری تحت شرایط شوری را می‌دهد.
Numerous biochemical and molecular mechanisms have been developed in plants to fight against salt stress namely, change in the content of osmolytes, enhancement of phenolic compounds, and supporting photosynthetic activity. These mechanisms lead to products and processes which improve the tolerance to salinity. Since there is no significant research on the resistance mechanisms of the species Salsola dendroides pall and Limonium reniforme (Girard) Lincz., some of these physiological changes in the aforementioned plants were investigated under natural stresses during different seasons to study their tolerance mechanism. To this end, plants were randomly collected from Incheboron area, north of Gorgan with four replicates during spring, summer, and autumn. Results showed that with increased temperature and salinity in summer, chlorophyll pigment contents significantly decreased in both Salsola dendroides and Limonium reniforme species. Soluble sugars content significantly increased in shoots and roots of Salsola dendroides in spring compared with other seasons while soluble sugars content in Limonium reniforme was higher in summer in comparison with spring. In summer, flavonoid contents significantly increased in shoots and roots of both species compared with other seasons. Anthocyanin content significantly changed with the change in seasons, while the highest anthocyanin contents were observed in shoots and roots of Salsola dendroides and Limonium reniforme in summer and autumn, respectively. Most of these changes were associated with activation of physiological and biochemical processes which allow the plants to adapt to saline conditions.
Anderson, O.M. and Jordheim, M. (2006). The anthocyanins. In: Flavonoids: Chemistry, biochemistry and applications. CRC Press, Taylor and Francis Group, Boca Raton. 471–551.
Anjum, S.A., Xie, X, Wang, L., Saleem, M.F., Man, C. and Lei, W. (2011). Morphological, physiological and biochemical responses of plants to drought stress. African Journal of Agricultural Research. 6(9): 2026-2032.
Ashraf, M. and Harris, P.J.C. (2013). Photosynthesis under stressful environments. Photosynthetica. 51 (2): 163-190.
Barnes, J.D., Balaguer, L., Manrique, E., Elvira, S. and Davison, A.W. (1992). A reappraisal of the use of DMSO for the extraction and determination of chlorophyll a and b in lichens and higher plants. Environmental and Experimental Botany. 32(2): 85-90.
Bhattacharjee, S. (2008). Calcium-dependent signaling pathway in the heat induced oxidative injury in Amaranthus lividus L. Biologia Plantarum.52: 137-140.
Chalker-Scott, L. (1999). Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology. 70(1): 1-9.
Chang, C.C., Yang, M.H., Wen, H.M. and Chern, J.Ch. (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis. 10(3): 178-182.
Chaves, M.M., Flexas, J. and Pinheiro, C. (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany. 103: 551–560.
Devmalkar, V.S., Murumkar, C.V., Salunkhe, S.M. and Chavan, S.J. (2014). Studies on pigment chlorophyll isolation and estimation of different bryophytes for their biochemical properties. Journal of Natural Product and Plant Resources. 4 (2): 56-61
Din, J., Khan, S.U., Ali, I. and Gurmani, A.R. (2011). Physiological and agronomic response of canola varieties to drought stress. Journal of Animal and Plant Sciences. 21(1): 78-82
Eckardt, N.A. (2009). A new chlorophyll degradation pathway. Plant Cell. 21: 700
El-Tayeb, M.A. (2005). Response of barley grain to the interactive effect of salinity and salicylic acid. Plant Growth Regulation. 42: 215-224.
Fardus, S., Wahid, A., Javed, F. and Sadia, B. (2014). Changes in leaf phenolics concentrations determine the survival of evening primrose (Oenothera biensis) in various seasons. International Journal of Agriculture and Biology.16: 819-824
Farooq, M., Wahid, A., Kobayashi, N., Fujita, D. and Basra, S.M.A. (2009). Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development. 29: 185-212
Flexas, J., Bota, J., Loreto, F., Cornic, G. and Sharkey, T.D.( 2004). Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Journal of Plant Biology. 6: 269-279.
Gehlot, M., Kasera, P. and Hussain, Sh. (2012).Seasonal variations in phytochemical parameters of Withania coagulans.Annals of Arid Zone. 51(1): 43-45.
Ghorbanli, M., Dasturani, M., Bonyadi, R. and Allahverdi Mamaghani, B. (2015). Effects seasonal changes of antioxidant enzymes activities, water and osmolyte in four halophyte species. Iranian Journal of Plant Physiology. 5 (2): 1297-1309.
Gonza´lez-Salvatierra, C., Andrade, J. L., Escalante-Erosa, F., Garcı´a-Sosa, K. and Pen -Rodrı´guez, L.M. ( 2010.). Antioxidant content in two CAM bromeliad species as a response to seasonal light changes in a tropical dry deciduous forest. Journal of Plant Physiology. 167(10):792-799
Gould, K. (2004). Nature's Swiss Army Knife: The diverse protective roles of anthocyanins in leaves. Journal of Biomedicine and Biotechnology. 5: 314–320.
Gupta, C. and Mishra, V. (2010). Effect of seasonal variation in photosynthetic pigments of few medicinal plants species of Jhansi. International Journal of Plant Sciences.5 (2): 676-678.
Huseynova, I.M., Suleymanov, S.Y., Rustamova, S.M. and Aliyev, J.A. (2009). Drought-induced changes in photosynthetic membranes of two wheat (Triticum aestivum L.) cultivars. Biochemistry. 74(8):903-909.
Imlay, J.A. (2008). Cellular defenses against superoxide and hydrogen peroxide. Annual Review of Biochemistry.77: 755–776.
Jaleel, C.A., Kishorekumar, P., Manivannan, A., Sankar, B., Gomathinayagam, M. and Panneerselvam, R. (2008). Salt stress mitigationby calcium chloride in Phyllanthusamarus. Acta Botanica Croatica. 67: 53-62.
Jenkins, S., Edward, G., Lennard, B. and Rengel, Z. (2010). Impacts of waterlogging and salinity on Puccinellia (Puccinellia ciliate) and wheat grass (Thinopgru mponticum) zonation on salt land with a shallow-water table, plant growth and Na+ and K+ concentrations in the leaves. Plant Soil. 329: 91-104.
Jouve, L., Hoffmann, L. and Hausman, J.F. (2004) .Polyamine, carbohydrate, and proline content changes during salt stress exposure of Aspen (Populus tremula L.): involvement of oxidation and osmoregulation metabolism. Plant Biology. 6(1): 74-80.
Kannan, N.D. and Kulandaivelu, G. (2011). Drought induced changes in physiological, biochemical and phytochemical properties of Withania somnifera Dun. Journal of Medicinal Plants Research. 5(16): 3929-3935.
Kheira, K., benchaben, H., adiba, B.D, Nadira, A. and Abbassia, A. (2015). Seasonal variations of ballotahirsutabenth flavonoids of tessala mount of the prefecture of SidiBel-Abbes (Western Algeria). Biochemistry and Molecular Biology Letters. 1(1): 001-006.
Kovacik, J., Klejdus, B., Hedbavny, J., Stork, F. and Backor, M. (2009). Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants. Plant and Soil. 320: 231-242.
Koyro, H.W., Khan, M. A. and Lieth, H. (2011). Halophytic crops: a resource for the future to reduce the water crisis?” Emirates Journal of Food and Agriculture. 23(1): 1–16.
Lineberger, D.R. and Steponkus, P. (1980). Cryoprotection by glucose, sucrose and raffinose to chloroplast thylakoids. Plant Physiology. 65(2): 298-304.
Mafakheri, A., Siosemardeh, A., Bahramnejad, B., Struik, P.C. and Sohrabi, E. (2010). Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Australian Journal of Crop Science. 4(8): 580-585.
Masukasu, H., Karin, O. and Kyoto, H. (2003). Enhancement of anthocyanin biosynthesis by sugar in radish (Raphanus sativus) hypocotyls. Plant Science. 164( 2): 259 - 265.
Morsy, A.A., Youssef, A.M., Mosallam, H.A.M. and Hashem, A.M. (2008). Assessment of selected species along Al-Alamein-Alexandria international desert road, Egypt. Journal of Applied Sciences Research. 4(10): 1276-1284.
MoselyArany, A., Hakimzadeh, M.A. and Ghobadpour, R. (2013). Comparison of changes in proline, soluble sugar and ion content of Atriplex lentiformis, Halostachys belangeriana and Tamarix rammossma over various times and natural salinity conditions. Iranian Scientific Association of Desert Management and Control. 2: 59-68
Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell and Environment. 25(2): 239-250.
Quideau, S., Deffieux, D., Douat-Casassus, C. and Pouységu, L. (2011). Plant polyphenols: Chemical properties, biological activities and synthesis. Angewandte Chemie International Edition. 50(3): 586–621.
Rahnama, A., Poustini, K., Tavakkol-Afshari, R. and Tavakoli, A. (2010). Growth and stomatal responses of bread wheat genotypes in tolerance to salt stress. International Journal of Biological Sciences. 6: 216-221.
Rezai-keneti, H. and Ghorbanli, M. (2015). Study of variation phytochemical and antioxidant activityof Frankenia hirsuta Desf. and Climacopte raturcomanica (Litw.) Aerial parts under harvest seasonin Sofikom regions of Golestan province. Journal of Iranian Plant Ecophysiological Research. 10(40): 51-61.
Rice-Evans, C., Miller, N. and Paganga, G. (1997). Antioxidant properties of phenolic compounds. Trends in Plant Science. 2(4): 152–159.
Sadasivam, S., and Manickam A. (1992). In: Biochemical methods for agricultural sciences, Wiley Eastern Limitetd. New Delhi. pp. 193-194.
Saibo, N.J.M., Lourenço, T. and Oliveira, M.M. (2009). Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Annals of Botany. 103: 609-623.
Shichijo, C., Hamada, T., Hiraoka, M., Johnson, C. B. and Hashimoto, T. (1993). Enhancement of red-light-induced anthocyanin synthesis in sorghum first internodes by moderate low temperature given in the pre-irradiation culture period. Planta an International Journal of Plant Biology.191(2):238-245.
Smirnoff, N. and Cumbes, Q.T. (1989). Hydroxyl radicals scavenging activity of compatible isolates. Phytochemistry. 28: 1057–1060.
Teimouri, Z. Ghorbanli, M. and Satei, A. (2014). Comparison the contents of proline, glycine betaine, soluble sugar and antioxidant enzyme activity in two Halophyte species Suaeda altissima Pall and Frankenia hirsute L. in two different seasons. Journal of Iranian Plant Ecophysiological Research. 9 (36):34-46.
Verpoorte, R., Contin, A. and Memelink, J. (2002). Biotechnology for the production of plant secondary metabolites. Phytochemistry. 1: 13–25.
Walker, D.J., Romero, P., De Hoyos, A. and Correal, E. (2008). Seasonal changes in cold tolerance, water relations and accumulation of cations and compatible solutes in Atriplex halimus L. Journal Environmental and Experimental Botany. 64: 217–224.
Zhu, J.K. (2002). Salt and drought stress signal transduction in plants. Annual Review of Plant Physiology and Plant Molecular Biology.53: 247-273.
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Anderson, O.M. and Jordheim, M. (2006). The anthocyanins. In: Flavonoids: Chemistry, biochemistry and applications. CRC Press, Taylor and Francis Group, Boca Raton. 471–551.
Anjum, S.A., Xie, X, Wang, L., Saleem, M.F., Man, C. and Lei, W. (2011). Morphological, physiological and biochemical responses of plants to drought stress. African Journal of Agricultural Research. 6(9): 2026-2032.
Ashraf, M. and Harris, P.J.C. (2013). Photosynthesis under stressful environments. Photosynthetica. 51 (2): 163-190.
Barnes, J.D., Balaguer, L., Manrique, E., Elvira, S. and Davison, A.W. (1992). A reappraisal of the use of DMSO for the extraction and determination of chlorophyll a and b in lichens and higher plants. Environmental and Experimental Botany. 32(2): 85-90.
Bhattacharjee, S. (2008). Calcium-dependent signaling pathway in the heat induced oxidative injury in Amaranthus lividus L. Biologia Plantarum.52: 137-140.
Chalker-Scott, L. (1999). Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology. 70(1): 1-9.
Chang, C.C., Yang, M.H., Wen, H.M. and Chern, J.Ch. (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis. 10(3): 178-182.
Chaves, M.M., Flexas, J. and Pinheiro, C. (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany. 103: 551–560.
Devmalkar, V.S., Murumkar, C.V., Salunkhe, S.M. and Chavan, S.J. (2014). Studies on pigment chlorophyll isolation and estimation of different bryophytes for their biochemical properties. Journal of Natural Product and Plant Resources. 4 (2): 56-61
Din, J., Khan, S.U., Ali, I. and Gurmani, A.R. (2011). Physiological and agronomic response of canola varieties to drought stress. Journal of Animal and Plant Sciences. 21(1): 78-82
Eckardt, N.A. (2009). A new chlorophyll degradation pathway. Plant Cell. 21: 700
El-Tayeb, M.A. (2005). Response of barley grain to the interactive effect of salinity and salicylic acid. Plant Growth Regulation. 42: 215-224.
Fardus, S., Wahid, A., Javed, F. and Sadia, B. (2014). Changes in leaf phenolics concentrations determine the survival of evening primrose (Oenothera biensis) in various seasons. International Journal of Agriculture and Biology.16: 819-824
Farooq, M., Wahid, A., Kobayashi, N., Fujita, D. and Basra, S.M.A. (2009). Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development. 29: 185-212
Flexas, J., Bota, J., Loreto, F., Cornic, G. and Sharkey, T.D.( 2004). Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Journal of Plant Biology. 6: 269-279.
Gehlot, M., Kasera, P. and Hussain, Sh. (2012).Seasonal variations in phytochemical parameters of Withania coagulans.Annals of Arid Zone. 51(1): 43-45.
Ghorbanli, M., Dasturani, M., Bonyadi, R. and Allahverdi Mamaghani, B. (2015). Effects seasonal changes of antioxidant enzymes activities, water and osmolyte in four halophyte species. Iranian Journal of Plant Physiology. 5 (2): 1297-1309.
Gonza´lez-Salvatierra, C., Andrade, J. L., Escalante-Erosa, F., Garcı´a-Sosa, K. and Pen -Rodrı´guez, L.M. ( 2010.). Antioxidant content in two CAM bromeliad species as a response to seasonal light changes in a tropical dry deciduous forest. Journal of Plant Physiology. 167(10):792-799
Gould, K. (2004). Nature's Swiss Army Knife: The diverse protective roles of anthocyanins in leaves. Journal of Biomedicine and Biotechnology. 5: 314–320.
Gupta, C. and Mishra, V. (2010). Effect of seasonal variation in photosynthetic pigments of few medicinal plants species of Jhansi. International Journal of Plant Sciences.5 (2): 676-678.
Huseynova, I.M., Suleymanov, S.Y., Rustamova, S.M. and Aliyev, J.A. (2009). Drought-induced changes in photosynthetic membranes of two wheat (Triticum aestivum L.) cultivars. Biochemistry. 74(8):903-909.
Imlay, J.A. (2008). Cellular defenses against superoxide and hydrogen peroxide. Annual Review of Biochemistry.77: 755–776.
Jaleel, C.A., Kishorekumar, P., Manivannan, A., Sankar, B., Gomathinayagam, M. and Panneerselvam, R. (2008). Salt stress mitigationby calcium chloride in Phyllanthusamarus. Acta Botanica Croatica. 67: 53-62.
Jenkins, S., Edward, G., Lennard, B. and Rengel, Z. (2010). Impacts of waterlogging and salinity on Puccinellia (Puccinellia ciliate) and wheat grass (Thinopgru mponticum) zonation on salt land with a shallow-water table, plant growth and Na+ and K+ concentrations in the leaves. Plant Soil. 329: 91-104.
Jouve, L., Hoffmann, L. and Hausman, J.F. (2004) .Polyamine, carbohydrate, and proline content changes during salt stress exposure of Aspen (Populus tremula L.): involvement of oxidation and osmoregulation metabolism. Plant Biology. 6(1): 74-80.
Kannan, N.D. and Kulandaivelu, G. (2011). Drought induced changes in physiological, biochemical and phytochemical properties of Withania somnifera Dun. Journal of Medicinal Plants Research. 5(16): 3929-3935.
Kheira, K., benchaben, H., adiba, B.D, Nadira, A. and Abbassia, A. (2015). Seasonal variations of ballotahirsutabenth flavonoids of tessala mount of the prefecture of SidiBel-Abbes (Western Algeria). Biochemistry and Molecular Biology Letters. 1(1): 001-006.
Kovacik, J., Klejdus, B., Hedbavny, J., Stork, F. and Backor, M. (2009). Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants. Plant and Soil. 320: 231-242.
Koyro, H.W., Khan, M. A. and Lieth, H. (2011). Halophytic crops: a resource for the future to reduce the water crisis?” Emirates Journal of Food and Agriculture. 23(1): 1–16.
Lineberger, D.R. and Steponkus, P. (1980). Cryoprotection by glucose, sucrose and raffinose to chloroplast thylakoids. Plant Physiology. 65(2): 298-304.
Mafakheri, A., Siosemardeh, A., Bahramnejad, B., Struik, P.C. and Sohrabi, E. (2010). Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Australian Journal of Crop Science. 4(8): 580-585.
Masukasu, H., Karin, O. and Kyoto, H. (2003). Enhancement of anthocyanin biosynthesis by sugar in radish (Raphanus sativus) hypocotyls. Plant Science. 164( 2): 259 - 265.
Morsy, A.A., Youssef, A.M., Mosallam, H.A.M. and Hashem, A.M. (2008). Assessment of selected species along Al-Alamein-Alexandria international desert road, Egypt. Journal of Applied Sciences Research. 4(10): 1276-1284.
MoselyArany, A., Hakimzadeh, M.A. and Ghobadpour, R. (2013). Comparison of changes in proline, soluble sugar and ion content of Atriplex lentiformis, Halostachys belangeriana and Tamarix rammossma over various times and natural salinity conditions. Iranian Scientific Association of Desert Management and Control. 2: 59-68
Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell and Environment. 25(2): 239-250.
Quideau, S., Deffieux, D., Douat-Casassus, C. and Pouységu, L. (2011). Plant polyphenols: Chemical properties, biological activities and synthesis. Angewandte Chemie International Edition. 50(3): 586–621.
Rahnama, A., Poustini, K., Tavakkol-Afshari, R. and Tavakoli, A. (2010). Growth and stomatal responses of bread wheat genotypes in tolerance to salt stress. International Journal of Biological Sciences. 6: 216-221.
Rezai-keneti, H. and Ghorbanli, M. (2015). Study of variation phytochemical and antioxidant activityof Frankenia hirsuta Desf. and Climacopte raturcomanica (Litw.) Aerial parts under harvest seasonin Sofikom regions of Golestan province. Journal of Iranian Plant Ecophysiological Research. 10(40): 51-61.
Rice-Evans, C., Miller, N. and Paganga, G. (1997). Antioxidant properties of phenolic compounds. Trends in Plant Science. 2(4): 152–159.
Sadasivam, S., and Manickam A. (1992). In: Biochemical methods for agricultural sciences, Wiley Eastern Limitetd. New Delhi. pp. 193-194.
Saibo, N.J.M., Lourenço, T. and Oliveira, M.M. (2009). Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Annals of Botany. 103: 609-623.
Shichijo, C., Hamada, T., Hiraoka, M., Johnson, C. B. and Hashimoto, T. (1993). Enhancement of red-light-induced anthocyanin synthesis in sorghum first internodes by moderate low temperature given in the pre-irradiation culture period. Planta an International Journal of Plant Biology.191(2):238-245.
Smirnoff, N. and Cumbes, Q.T. (1989). Hydroxyl radicals scavenging activity of compatible isolates. Phytochemistry. 28: 1057–1060.
Teimouri, Z. Ghorbanli, M. and Satei, A. (2014). Comparison the contents of proline, glycine betaine, soluble sugar and antioxidant enzyme activity in two Halophyte species Suaeda altissima Pall and Frankenia hirsute L. in two different seasons. Journal of Iranian Plant Ecophysiological Research. 9 (36):34-46.
Verpoorte, R., Contin, A. and Memelink, J. (2002). Biotechnology for the production of plant secondary metabolites. Phytochemistry. 1: 13–25.
Walker, D.J., Romero, P., De Hoyos, A. and Correal, E. (2008). Seasonal changes in cold tolerance, water relations and accumulation of cations and compatible solutes in Atriplex halimus L. Journal Environmental and Experimental Botany. 64: 217–224.
Zhu, J.K. (2002). Salt and drought stress signal transduction in plants. Annual Review of Plant Physiology and Plant Molecular Biology.53: 247-273.
