The responses of potato cultivars to osmotic and temperature stresses under in vitro conditions

Subject Areas : Stress Physiology

Farnoosh Jafari ¹ , Jaber Panahandeh ² , Alireza Motallebi Azar ³ , Mousa Torabi Giglou ⁴

1 - Department. of Horticulture, Faculty of Agriculture, University of Tabriz. Iran
2 - Department. of Horticulture, Faculty of Agriculture, University of Tabriz. Iran
3 - Department. of Horticulture, Faculty of Agriculture, University of Tabriz. Iran
4 - Department. of Horticulture, Faculty of Agriculture, University of Mohaghegh Ardabili, Iran

Received: 2019-08-26 Accepted : 2019-08-26 Published : 2019-05-01

Keywords: in vitro, temperature, osmotic stress, PEG, Potato,

Abstract :

In order to investigate the responses of potato plantlets under in vitro conditions to osmotic and temperature stresses, a factorial experiment was carried out in a completely randomized design with three replications. Each replicate contained a glass jar with 5 explants grown in it. The first factor was water deficit at four levels of osmotic stress caused by polyethylene glycol 6000 including control, -0.5,-0.1, and -1.5 MPa and the second factor was temperature at three levels of 15, 25 and 35° C. Five potato cultivars, including 3 promising clones, 143, 301, and 306 as well as Marfona and Picasso cultivars were exposed to stresses in MS medium. Eight weeks after stress period, indicators such as fresh and dry weights of plantlets, electrolyte leakage, proline, catalase, phosphorus, and potassium concentrations were measured. The results of variance analysis indicated that the simple effects of factors as well as the interactions of the investigated factors at P≤0.01 had a significant effect on the study traits. Mean comparison showed that the temperature stress decreased the fresh and dry weights of plantlets and potassium concentration but increased electrolyte leakage, proline, catalase, and phosphorus concentration. On the other hand, osmotic stress reduced fresh and dry weight of plantlets, P and K, while proline, CAT, and electrolyte leakage increased. The combination of stresses lowered plantlets’ resistance to stresses because osmotic stress of -0.5 MPa and higher, in combination with 35° C caused the explants to dry. Finally, results showed that Marfona cultivar was more tolerant to stress conditions than other genotypes. This seems to be the result of accumulating more proline and high antioxidant activity. On the other hand, clone 306 was more susceptible to stress than other genotypes and the plantlets 306 experienced more damage and dried.

References:

Acar O, I. Türkan and F. Özdemir.2001. 'Superoxide dismutase and peroxidase activities in drought sensitive and resistant barley (Hordeum vulgare L.) varieties'. Acta Physiol Plant. 23(3): 351–356.

Ahuja I, RC de Vos, AM Bones and RD Hall. 2010. 'Plant molecular stress responses face climate change'. Trends Plant Sci. 15:664–74.

Alam S M. 1999. 'Nutrient uptake by plants under stress condition', In: M. Pessaraki (ed.), Handbook of plant and crop stress, Marcel Dekker Inc., pp. 285-315.

Aebi H. 1984. 'Catalase in vitro'. Methods in Enzymology.105, 121-126.

Amini F. M. Askari and M. Haghir. 2017. 'Changes in protein and antioxidant system of Cucumis sativus cv. Isfahani in response to drought stress'. Journal of Cell & Tissue. 7(4):375-385. (In persian).

Amoubeigi M. and R. Razavizadeh .2013. 'Effect of drought stress and paclobutrazol on the accumulation of flavonoids and minerals nutrition under in vitro conditions in rapeseed (Brassica napus L.)'. Iranian Journal of Plant Echo-physiology. 31, 8 (3): 12-22. (In Persian)

Anjum SA.  LC. Wang, M. Farooq, M. Hussain,LL. Xue and CM. Zou. 2011. 'Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange'. Journal of Agronomy and Crop Science.197(3): 177-185.

Anjum NA., C. Arena and S. Singhgill. 2014. 'Reactive Oxygen species and response of antioxidants as ROS scavengers during environmental stress in plant'. Frontiers in Environmental Science. 2:1-13.

Arndt SKK. SC. Clifford, W. Wanek, H.G. Jones and M. Popp. 2001. 'Physiological and morphological adaptations of the fruit tree Ziziphus rotundifolia in response to progressive drought stress'. Tree Physiology.21:705-715.

Ashraf M, and MR Foolad. 2007. 'Roles of glycine betaine and proline in improving plant abiotic stress tolerance'. Environmental and Experimental Botany. 59(1): 206-216.

 

Ashraf, M., H.R., Athar, P.J.C., Harris, and T.R. Kwon, 2008. 'Some prospective strategies for improving crop salt tolerance'. Advances in Agronomy. 97, 45-110.

Awasthi R, N Kaushal, V Vadez, NC Turner, J Berger, and KHM Siddique. 2014. 'Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea'. Functional Plant Biology 41(11):1148-1167

Barber, S. A. 1995. 'Soil Nutrient Bioavailability': A Mechanistic Approach, 2nd Edn. New York, NY: Wiley.

Bates LS. RP Waldern and ID Tears. 1973 'Rapid determination of free proline for water-stress studies'. Plant and Soil, 39: 205-207. 

Benavides MP, PL Marconi, SM Gallego, ME Comba, and ML Tomaro. 2000. 'Relationship between antioxidant defense system and salt tolerance in Solanum tuberosum'.  Australian journal of plant physiology 27(3):273-278.

Bewley JD. 1979. 'Physiological aspects of desiccation tolerance'. Annual Review of Plant Physiology. 30:195-238.

Birch P.R.J., G. Bryan, B.Fenton, E.M.Gilroy, I.Hein, J.T. Jones, A. Prashar, M.A Taylor, L.Torrance,  and IK Toth .2012. 'Crops that feed the world 8: Potato: are the trends of increased global production sustainable?' Food Security.4(4,12):477-508.

Blume A. and A. Ebercon. 1981. 'Cell membrane stability as a Measure of Drought and Heat Tolerance in wheat'.  Crop Science. 21(1): 43-47.

Bohnert HJ, and RG Jensen. 1996. 'Metabolic engineering for increased salt tolerance. The next step'. Australian Journal of Plant Physiology 23(5) 661 – 667

 Bohenert HJ. and B. Shen .1999.'Transformation and compatible solutes'. Scientia Horticulturae. 78: 237-260. 

Bor, M. F. Ozdemir, and I. Turkan. 2003. 'The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L and wild beet Beta maritima L'. Plant Sci. 164:77–84.

Bowler C., MV Montagu, and D. Inze. 1992. 'Superoxide dismutase and stress tolerance'. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:83– 116.

Brown C.R. 2005. 'Antioxidants in potato'. Am. J. Potato Res. 82(2): 163-172

Caballero JI, CV Verduzco , J Galan , and ESD Jimenz. 2005. 'Proline accumulation as a symptom of drought stress in maize: A tissue differentiation requirement'. Journal of Experimental Botany .39 (7): 889-897

Cakmak I. 2005. 'The role of potassium in alleviating detrimental effects of abiotic stresses in plants'. J. Plant Nutrition and Soil Science. 168:521-530.

Carr MKV. 1989. 'Potato quality control with irrigation'. Water Irrigation Review. 9: 28-29.

Chaves, M.M., J.P. Maroco, and J.S. Pereira. 2003. 'Understanding plant responses to drought-from genes to the whole plant', Functional Plant Biology ,30: 239–264.

Chew YH, and KJ Halliday. 2011. 'A stress-free walk from Arabidopsis to crops'. Current Opinion in Biotechnology. 22(2):281-286.

Deikman J., M. Petracek, and JE Heard. 2012. 'Drought tolerance through biotechnology: improving translation from the laboratory to farmers’ fields'. Current Opinion in Biotechnology. 23(2):243-250.

Delauney, A. J., and DPS Verma. 1993. 'Proline biosynthesis and osmoregulation in plants'. Plant J. 4: 215-223.

Ding X, Y Jiang, T Hao , H Jin , H Zhang  and L He .2016. 'Effects of heat shock on photosynthetic properties, antioxidant enzyme activity, and downy mildew of cucumber'. PLOS ONE, 11;11(4): e0152429.

Dulai S, I Molnar, J Pronay, A Csernak, R Tarnai and M Molnar-Lang. 2006. 'Effects of drought on photosynthetic parameters and heat stability of PSII in wheat and in Aegilops species originating from dry habitats'. Acta Biologica Szegediensis 50(1-2):11-17.

Fageria, N.K., VC Baligar and R B Clark. 2002. 'Micronutrient in crop production'. Adv. Agron. 77:185-268.

 

Farooq, M., T Aziz, SMA Basra, MA Cheema, and H Rehman. 2008. 'Chilling tolerance in hybrid maize induced by seed priming with salicylic acid'. J. Agron. Crop Sci. 194, 161–168.

Farooq M., A Wahid, M Kobayashi,D Fujita and SMA Basra. 2009. 'Plant drought stress: effects, mechanisms and management'. Agron.Sustain.Dev. 29:185-212.

Fernando M., J. Mehroke and ADM Glass. 1992. 'De novo synthesis of plasma membrane and tonoplast polypeptides of barley roots during short-term K deprivation. In search of the high-affinity K transport system'. Plant Physiol.100:1269–1276.

 Fumis, T.F. and J. F. Pedras. 2002. 'Proline, diamine and polyamines accumulation in wheat cultivars submitted to water deficits'. Pesquisa Agropecuaria Brasileira. 37(4):449-459

Garg BK .2003. 'Nutrient uptake and management under drought: Nutrient-moisture interaction'. Curr. Agric. 27:1-8.

Gelmesa, D., N. Dechassa, W. Mohammed, E. Gebre, Ph. Monneveux, Ch. Bundig and T. Winkelmenn. 2017.'In vitro screening of potato genotypes for osmotic stress tolerance'.Open Agriculture, 2: 308–316.

Gholipour S. and A. Ebadie. 2017. ' Study change compatibility metabolites and antioxidant enzyme activities of wheat cultivars under water stress'. Journal of process and Function, 6 (19):219-232. (In Persian)

Gimmenz C. and E. Freres .1986. 'Genetic variability in sunflower cultivars under drought II. Growth and water relations'. Australian Journal of Agricultural Research, 37(6) 583 – 597. 

Golen H., E. Turhan and A. Eris. 2006.' Changes in peroxidase activities and soluble proteins in strawberry varieties under salt stress'. Acta Physiologiae Plantarum, 28(2): 109-116.

Golestani Kermani S., MR Nouri Emamzade’i, M. Shayannejad, A. Shah Nazari and A. Mohammadkhani. 2014. 'Effects of water stress on quantitative and qualitative properties of potato crop (Agria c.v.) in deficit irrigation and partial root zone drying techniques '. Journal of Irrigation Science and Engineering, 37 (3): 135-123.(In Persian)

Gregory, P.J. and L.P. Simmonds. 1992. 'Water relations and growth of potatoes'. p. 214–246. In P.M. Harris (ed.) The potato crop: The scientific basis for improvement. 2nd ed. Chapman and Hall, London.

Hadidi A. 1999. 'Germination and early growth of tea common bean cultivars as affected by water stress and seed size'. Direct Agricultural Science, 26: 23-25.

Hao, H.P., C. D.  Jiang, S. R. Zhang, Y. D. Tang and L. Shi. 2012.  'Enhanced thermal-tolerance of photosystem II by elevating root zone temperature in Prunus mira Koehne seedlings'. Plant Soil, 353:367–378.

Hare, P. D. and W. A. Cress. 1997. 'Metabolic implications of stress-induced proline accumulation in plants'. Plant Growth Regulat, 21:79–102.

Hassandokht MR. M. Bigdelo, F. Soltani and R.  Salehi Mohammadi .2017. 'Evaluation of drought stress tolerance and its effects on growth characteristics in some accessions of colocynth (Citrullus colocynthis (L.) Schrad'). Iranian Journal of Horticultural Science, 48(2):275-284. (In Persian)

Hassani Moghadam E., M. Esna-Ashari and A. H. Rezainejad .2015.' Effect of drought stress on some physiological characteristics in six commercial iranian pomegranate (Punica granatum L.) cultivars'. Plant Production Technology, 7(1):1-11. (In Persian)

Hasanuzzaman, M, K Nahar,SS Gill and M. Fujita.2013. 'Drought stress responses in plants, oxidative stress, and antioxidant defense (eds).' Climate Change and Plant Abiotic Stress Tolerance.Wiley-VCH Verlag GmbH & Co. KGaA: Germany 209-249.

Hemantaranjan A, AN Bhanu, MN Singh, DK Yadav, PK Patel, R Singh and D Katiyar. 2014. 'Heat stress responses and thermos tolerance.' Adv Plants Agric Res,1(3):62‒70.

Hernandez, J A, E Olmos, F J Corpas, F Sevilla and L A del Rio. 1995. 'Salt induced oxidative stress in chloroplast of pea plants'.Plant Sci. 105:151–167.

Hokmabadi H., S. Noorian bigdeli, R.  Narimani and M. Moghaddam. 2017. 'Study of beet bagasse effect on biochemical characteristics, photosynthetic pigments and antioxidant activity of leaf extracts of peppermint (Mentha piperita L.) under drought stress conditions'.Journal of Science and Technology of Greenhouse Culture, 8 (1) :135-145. (In Persian)

Hopkins WG and NPA Huner. 2009. 'Introduction to plant physiology'. Fourth Edition, John Wiley & Sons, Inc., New York, USA, pp.503.

Howarth C.J. 2005. 'Genetic improvements of tolerance to high temperature. In: Abiotic Strsses Plant Resistance Through Breeding and Molecular Approaches (Eds M. Ashraf, P.J.C. Harris)'. Howarth Press, New York, USA.

Huang, B., S.  Rachmilevitch and J. Xu. 2012. 'Root carbon and protein metabolism associated with heat tolerance'. J. Exp. Bot. 63:3455–3465.

Jaleel C.A., P. Manivannan, A.  Wahid, M.  Farooq, R. Somasundaram and R. Panneerselvam. 2009. 'Drought stress in plants: a review on morphological characteristics and pigments composition'. International Journal of Agriculture and Biology, 11(1): 100–105.

Javadi T., K. Arzani and H. Ebrahimzadeh. 2004. 'Evaluation of soluble carbohydrate content and proline in 9 genotypes of Asian pear (Pyrus serotina Rehd) under drought stress'. Iranian Journal of Plant Biology, 17(3):369-378. (In Persian)

Jiang Y and B. Hung. 2001. 'Drought and heat stress injury to two cool-season turf grasses in relation to antioxidant metabolism lipid peroxidation'. Crop Science ,41: 436-442.

Juenger,T. E. 2013. 'Natural variation and genetic constraints on drought tolerance'. Current Opinion in Plant Biology,  16(3):274-81.

Kafi M., A. Borzouii, M. Salehi, A. Kamandi , A. Masoumi and J. Nabati. 2010. 'Physiology of environmental stresses in plants'. Mashhad University Press.502 pp. (In Persian)

Karimi S. A. Yadollahi and K.  Arzani. 2013. 'Response of almond genotypes to osmotic stress induced in vitro.' Journal of Nuts, 4(4):1-7.

Kishor, P.B.K., S. Sangama, R.N. Amrutha, P.S. Laxmi, K.R. Naidu and K.S. Rao. 2005. 'Regulation of proline biosynthesis degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance'. Current Science, 88: 424-438.

Kozlowska M. 2007. Plant Physiology'. From theory to applied sciences (in Polish). PWRiL, Warsaw, Poland.

Kulkarni JH, V Ravindra, VK Sojitra and DM Bhatt .1988. 'Growth, nodulation and N uptake of groundnut (Arachis hypogaea L.) as influenced by water deficits stress at different phenophase'. Oleagineus, 43: 415–419.

Levitt J. 1980. 'Response of plants to environmental stresses'. Vol 1, 2 Chilling, Freezing and High temperature Stresses. Academic Press, New York

LIMA, M. G. S., N. F. LOPES, M. A. BACARIN, and C. R. MENDES. 2004. 'Efeito do estresse salino sobre a concentração de pigmentos e prolina em folhas de arroz'. Bragantia, v. 63, n. 3, p. 335-340.

Lipiec J, C Doussan, A Nosalewicz and K Kondracka. 2013. 'Effect of drought and heat stresses on plant growth and yield: a review'. Int Agrophys, 27:463–77.

Liu X. and B. Huang. 2000. 'Heat stress injury in relation to membrane lipid peroxidation in creeping bent grass'. Crop Sci. 40: 503-510.

Lutts S, JM Kinet and J Bouharmont. 1995. 'Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance'. Journal of Experimental Botany, 46 (12): 1843-1852.

Mafakheri A., A. Siosemardeh, B.  Bahramnejad and PC Struik. 2011. 'Effect of drought stress and subsequent recovery on protein, carbohydrate contents, catalase and peroxidase activities in three chickpeas (Cicer arietinum) cultivars'. Australian Journal of Crop Science, 5 (10):1255-60.

Marschner H.1995. 'Mineral Nutrition of Higher Plants'.2nd ed. Academic Press, London, UK.

Masoudi Sadaghiani, F. and M. Amini Dehaghi .2016. 'Changes in some osmolytes and photosynthetic pigments accumulation and antioxidant enzymes activity in potato under water stress in greenhouse conditions'. Iranian Journal of Horticultural Science and Technology, 17 (1) :29-38. (In Persian)

Masoumi A, M. Kafi, HR Khazaei and K Davari. 2010. 'Effect of drought stress on water status, electrolyte leakage and enzymatic antioxidants of Kochia (Kochia scoparia) under saline conditions'. Pakistan Journal of Botany,42 (5): 3517-3524.

 Mehri, H.R.,S. Ghobadi, B.  Baninasab, P. Ehsanzadeh and M.  Gholami. 2015.'Evaluation of some physiological and morphological responses of four Iranian grapevine (Vitis vinifera L.) cultivars to drought stress under in vitro conditions'. Journal of Plant Process and Function,  3(10): 115-126. (In Persian)

Michel BE. and MR Kaufmann. 1973. 'The osmotic potential of polyethylene glycol 6000'. Plant Physiology. 51:914-916.

Mittler R. 2002. 'Oxidative stress, antioxidant and stress tolerance'. Annual Review of Plant Science, 7: 405-415.

Mittler R. 2006. 'Abiotic stress, the field environment and stress combination'. Trends Plant Sci.11:15–9.

Monneveux P., D. A. Ramirez and M. T. Pino .2013. 'Drought tolerance in potato (Solanum tuberosum L.): Can we learn from drought tolerance research in cereals?' Plant Sci.205:76-86.

Moussa, H.R and S. M.  Abdel-Aziz. 2008. 'Comparative response of drought tolerant and drought sensitive maize genotypes to water stress'. Australian Journal of Crop Science, 1(1):31-36.

Munns R. 2002. 'Comparative physiology of salt and water stress'. Plant, Cell and Environment ,25: 239-250.

Munns R and RA James. 2003. 'Screening methods for salinity tolerance: a case study with tetraploid wheat'. Plant and Soil, 253: 201-218.

NajafZadeh S. and A.  Ehsanpour.2012.' Effect of drought stress on some physiological parameters of two potato cultivars (Kenebec and Concord) under in vitro culture condition'. Journal of Aridbiom,2(1) :70-82.(In Persian)

Nasibi F. 2011. 'Effect of different concentrations of sodium nitroprusside (SNP) pretreatment on oxidative damages induced by drought stress in tomato plant'. Iranian Journal of Plant Biology, 3(9) :63-74. (In Persian)

Navari-Izzo, F. and N. Rascio. N.1999. 'Plant response to water-deficit conditions'. in: M. Pessarakli (Ed.),  andbook of Plant and Crop Stress, Marcel Dekker, New York. pp. 231–270.

Nazari Nasi H.  F. Jabari, MR. Azimi and M. Norouzian .2012. 'Evaluation of drought stress on cell membrane stability, photosynthesis rate, relative water content and grain yield of four maize bean cultivars'. Journal of Iranian Crop Science, 43 (3): 499-491. (In Persian)

Nematollahi A., AR Jafari and AR. Bagheri.2013. 'Effect of drought stress and salicylic acid on photosynthetic pigments and nutrient uptake of sunflower cultivars (Helianthus annuus L.)'. Plant Ecophysiology,5 (12): 37-51. (In Persian)

Nouri A., A. Nezami. M. Kafi and D. Hassanpanah. 2016. 'Evaluation of water deficit tolerance of 10 potato cultivars based on some physiological traits and (Solanum tuberosum L.) tuber yield in Ardabil region'. Journal of Crop Ecophysiology,10(1):243-268. (In Persian)

Pirzad A., MR. Shakiba, S. Zehtab-Salmasi and SA Mohammadi.2015.' Effects of water stress on some nutrients uptake in Matricaria chamomilla L.' Agronomy Journal, (Pajouhesh & Sazandegi). 106:1-7. (In Persian)

Ranjbarfordoei, A., R. Samson, P.V. Damne and R. Le-meur. 2000. 'Effects of drought stress induced by polyethylene glycol on pigment content and photosynthetic gas ex-change of Pistacia khinjuk and P mutica.' Photosynthetica, 38(3): 443-447.

Rasheed, R. , A. Wahid, M. Farooq,I. Hussain, M. Shahzad and A. Basra.2011.' Role of proline and glycine betaine pretreatments in improving heat tolerance of sprouting sugarcane (Saccharum sp.) buds'. Plant Growth Regulation, 65(1): 35-45.

Razavizadeh R. and E. Shahriari. 2017. 'Comparative study of drought stress effects on physiological and defense parameters of some varieties of sorghum under in vitro culture'. Journal of process and Function, 6 (19):163-180. (In Persian)

Sairam RK, KV Rao and GC Srivastava.  2002. 'Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration'. Plant Science, 163:1037–1046

Sanchez-Rodriguez E. M. Rubio-Wilhelmi, LM Cervilla, B. Blasco, JJ Rios, MAS Rosale , L. Romero and JM Ruiz.2010.'Genotypic differences in some physiological parameters symptomatic for oxidative stress under moderate drought in tomato plants'. Plant Science,178: 30-40.

Sariri R. , M. Galvani, R. Fotouhi Ghazvini and V. Jafarian.2011. 'The effect of cold temperature stress on antifreeze protein production and lipid peroxidation in two citrus species'. Iranian Journal of Plant Biology, 3(7), 97-102. (In Persian)

Sgherri, C.L.M., C.  Pinzino and F. Navari-Izzo. 1996.'Sunflower seedlings subjected to stress by water deficit changes in O₂ production related to the composition of thylakoid membranes', Physiol. Plant, 96:446–452.

Shalata, A., V. Mittova, M. Volokita, M. Guy and M. Tal. 2001. 'Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system'. Physiol. Plant., 112 (4):487–494.

Sharma, S.S and K.J. Dietz. 2006. 'The significance of amino acids and amino-acid derived molecules in plant responses and adaptation to heavy metal stress'. Journal of Experimental Botany, 57: 711-726.

Siddiqui MH, MY Al-Khaishany, MA Al-Qutami, MH Al-Whaibi, A Grover and HM Ali. 2015. 'Morphological and physiological characterization of different genotypes of faba bean under heat stress'. Saudi J Biol Sci. 22:656–63.

Singh DK and PWG Sale. 2000. 'Growth and potential conductivity of white clover roots in dry soil with increasing phosphorus supply and defoliation frequency'. Agron J., 92: 868–874.

Singh, N.P., P.K. Pal and S. K. Vaishali. 2014. 'Morpho-physiological characterization of Indian wheat genotypes and their evaluation under drought condition'. African Journal of Biotechnology, 13 (20).2022-2027.  

Sivritep N., U. Erturk, C. Yarlikaya, I. Turkan, M. Bor and F. Ozdemir. 2008.'Response of the cherry rootstock to water stress induced in vitro'. Biologia Plantarum, 52: 573-576.

Smirnoff, N. 1993. 'The role of active oxygen in the response of plants to water deficit and desiccation'. New Phytologist, 125:27-58.

Smirnoff, N.1996.'The function and metabolism of ascorbic acid in plants'. Ann. Bot. 78: 661–669.

Suzuki N, RM Rivero, V Shulaev, E Blumwald and R Mittler. 2014. 'Abiotic and biotic stress combinations'. New Phytol. 203(1):32-43.

Szabados, L. and A.  Savoure. 2010. 'Proline: a multifunctional amino acid'. Trends Plant Sci. 15: 89–97. 

Taiz L and E.  Zeiger. 2006.'Plant physiology'. 4th edn. Sinauer Associates Inc, Sunderland, Massachusetts

Taji A. and P.  KumarLackshmanan.2008.' In Vitro plant breeding, Food Production Press'. Binghamton. New York. USA. P: 167.

Tanguilig, V.C., E. B. Yambao, J. C. O’toole and S. K. De Datta. 1987.' Water stress effects on leaf elongation, leaf water potential, transpiration, and nutrient uptake of Rice, Maize, and Soybean'. Plant and Soil, 103, 155-168. 

Tarahomi G., M. Lahooti ​​and F. Abbasi. 2010. 'Effects of drought stress on changes in soluble sugars, chlorophyll content and potassium in Salvia leriifolia benth'. Journal of Biological Sciences 3 (2): 1-7. (In Persian)

Turkan, I., M.  Bor, F. Ozdemir and H. Koca. 2005. 'Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius Gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress'. Plant Science ,168: 223-231.

Umar, S. 2006. 'Alleviating adverse effects of water stress on yield of sorghum, mustard and groundnut by potassium application'. Pak J Bot ,38: 1373–1380.

 Vendruscolo ACG., I.Schuster, M. Pileggi, CA. Scapim, HBC. Molinari, CJ Marur and LGC Vieira. 2007. 'Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat'. Journal of PlantPhysiology,164:1367-1376.

Verbruggen N and C Hermans. 2008. 'Proline accumulation in plants: a review'. Amino Acids,35:753–759.

Wahid A, S. Gelani, M. Ashraf and MR Foolad. 2007. 'Heat tolerance in plants: An overview'. Environmental and Experimental Botany, 61:199-223.

Wahid, A. and E.  Rasul. 2007. 'Photosynthesis in leaf, stem, flower and fruit'. in: Pessarakli M. (Ed.), Handbook of Photosynthesis, 2^nd ed. CRC Press: Florida, 479–497.

Waraich E.A.,R. Ahmad, A. Halim and  T. Aziz. 2012. 'Alleviation of temperature stress by nutrient management in crop plants: a review'. J. Soil Sci. Plant Nutrition, 12(2):221-244.

Wind W., M. Arend and J. Fromm.2004. 'Potassium-dependent cambial growth in poplar'. Plant Biology, 6:30–37. 

Winston, G.W.1990. 'Physiochemical basis for free radical formation in cells: production and defenses'. in: R.G. Alscher, J.R. Cumming (Eds.), Stress Responses in Plants: Adaptation and Acclimation Mechanisms, Wiley-Liss, New York. pp. 57–86.

 

 

Zhang, Y. and D. J. Donnwelly. 1997. 'In vitro bioassays for salinity tolerance screening of potato'. Potato Research. 40 :285- 295.

Zhang J.-H., W. D. Huang, Y. P. Liu and Q. H. Pan. 2005. 'Effects of temperature acclimation pretreatment on the ultrastructure of mesophyll cells in young grape plants (Vitis vinifera L. cv. Jingxiu) under cross-temperature stresses'. J. Integr. Plant Biol. 47:959-970.

Zhou R, X. Yu, KH Kjær, E. Rosenqvist, CO Ottosen and Z Wu. 2015. 'Screening and validation of tomato genotypes under heat stress using Fv/Fm to reveal the physiological mechanism of heat tolerance'. Environ Exp Bot. 118:1–11.

Zlatev Z. and F. C. Lidon. 2012. 'An overview on drought induced changes in plant growth, water relations and photosynthesis'. Emir. J. Food Agric.,24:57-72.

Zokaii Khosro Shahi MR., M. Esna Ashari, A. Ershadi and A. Imani.2014. 'Physiological responses of five almond Species to PEG-induced drought stress'. Plant Production Technology. 5(2):73-88. (In Persian)