Effects of salicylic acid and heat acclimation on thermotolerance and withanolide accumulation under high temperature stress in the Cape gooseberry (Physalis peruviana L.)

Effects of salicylic acid and heat acclimation on thermotolerance and withanolide accumulation under high temperature stress in the Cape gooseberry (Physalis peruviana L.)

The adverse effects of high temperature stress can be alleviated by thermotolerance induced by exogenous application of plantgrowth regulators or by gradual application of temperature stress. Physalis peruviana L., commonly known as the Cape gooseberry,is a source of a variety of phytocompounds such as withanolides (withanone, withaferin A, and withanolide A). These withanolidesare potentially high-value drug candidates because of their various pharmacological properties. The production of withanolides viatraditional agriculture is commercially inadequate. In the present study, elicitation strategies were employed to improve the crop’sthermotolerance and accumulation of withanolides. For these purposes, the effects of heat acclimation (45 °C HA) or salicylic acid (150mM SA) treatments in inducing withanolide production and thermotolerance were tested in leaves of P. peruviana L. grown under hightemperature stress (55 °C). Considerable increases in the production of withanolides (up to 86.83 mg g–1 dry weight, dw) were observedwhen the cultures were exposed for 5 h to high temperature stress after pretreatment with SA. SA application and heat acclimationincreased the activity of superoxide dismutase (SOD; EC 1.15.1.1) and decreased the catalase activity (CAT; EC 1.11.1.6). Both SA andheat acclimation caused a significant increase in endogenous H2O2 and proline content. Changes in related antioxidants parallelingheat acclimation or SA treatment suggest that common mechanisms might be involved in thermotolerance induced by SA and heatacclimation.

___

  • Ali MB, Hahn EJ, Paek KY (2007). Methyl jasmonate and salicylic acid-induced oxidative stress and accumulation of phenolics in Panax ginseng bioreactor root suspension cultures. Molecules 12: 607-621. doi: 10.3390/12030607
  • Awate PD, Gaikwad DK (2014). Influence of growth regulators on secondary metabolites of medicinally important oil yielding plant Simarouba glauca DC. under water stress conditions. Journal of Stress Physiology and Biochemistry 10: 222-229.
  • Bartoli CG, Casalongue C, Simontacchi M, Marquez-Garcia B, Foyer CH (2012). Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environmental and Experimental Botany 94: 73-88. doi: 10.1016/j.envexpbot.2012.05.003
  • Bates L, Waldren R, Teare I (1973). Rapid determination of free proline for water stress studies. Plant and Soil 39: 205-207. doi: 10.1007/BF00018060
  • Brennan T, Frenkel C (1977). Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiology 59: 411-416.
  • Ben-Rejeb K, Lefebvre-De Vos D, Le Disquet I, Leprince AS, Bordenave M et al. (2015). Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytologist 208: 1138-1148. doi: 10.1111/nph.13550
  • Chen Z, Ricigliano JW, Klessig DF (1993). Purification and characterization of a soluble salicylic acid-binding protein from tobacco. Proceedings of the National Academy of Sciences of the United States of America 90: 9533-9537.
  • Chen CT, Chen LM, Lin CC, Kao CH (2001). Regulation of proline accumulation in detached rice leaves exposed to excess copper. Plant Science 160: 283-290. doi: 10.1016/S0168-9452(00)00393-9
  • Cingoz SG, Verma SK, Gürel E (2014). Hydrogen peroxide-induced antioxidant activities and cardiotonic glycoside accumulation in callus cultures of endemic Digitalis species. Plant Physiology and Biochemistry 82: 89-94. doi: 10.1016/j.plaphy.2014.05.008
  • Cingoz GS, Gurel E (2016). Effects of salicylic acid on thermotolerance and cardenolide accumulation under high temperature stress in Digitalis trojana Ivanina. Plant Physiology and Biochemistry 105: 145-149. doi: 10.1016/j.plaphy.2016.04.023
  • Clarke SM, Mur LA, Wood JE, Scott IM (2004). Salicylic acid dependent signalling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. The Plant Journal 38: 432-447. doi: 10.1111/j.1365-313X.2004.02054.x
  • Conrath U, Silva H, Klessig DF (1997). Protein dephosphorylation mediates salicylic acid-induced expression of PR-1 genes in tobacco. The Plant Journal 11: 747-757. doi: 10.1046/j.1365- 313X.1997.11040747.x
  • Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998). Parallel changes in H2 O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard plants. Plant Physiology 116: 1351-1357.
  • Fabro G, Kovacs I, Pavet V, Szabados L, Alvarez ME (2004). Proline accumulation and AtP5CS2 gene activation are induced by plant–pathogen incompatible interactions in Arabidopsis. Molecular Plant–Microbe Interactions 17: 343-350. doi: 10.1094/MPMI.2004.17.4.343
  • Fayez KA, Bazaid SA (2014). Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. Journal of the Saudi Society of Agricultural Sciences 13: 45-55. doi: 10.1016/j.jssas.2013.01.001
  • Fedina I, Georgieva K, Velitchkova M, Grigorova I (2006). Effect of pretreatment of barley seedlings with different salts on the level of UV-B induced and UV-B absorbing compounds. Environmental and Experimental Botany 56: 225-230. doi: 10.1016/j.envexpbot.2005.02.006
  • Foyer CH, Noctor G (2009). Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants and Redox Signaling 11: 861-905. doi: 10.1089/ ars.2008.2177
  • Grover A, Samuel G, Bisaria VS, Sundar D (2013). Enhanced withanolide production by overexpression of squalene synthase in Withania somnifera. Journal of Bioscience and Bioengineering 115: 680-685. doi: 10.1016/j.jbiosc.2012.12.011
  • Hassanien MFR (2011). Physalis peruviana: A rich source of bioactive phytochemicals for functional foods and pharmaceuticals. Food Reviews International 27: 259-273. doi: 10.1080/87559129.2011.563391
  • He YL, Liu YL, Chen Q, Bian AH (2002). Thermotolerance related to antioxidation induced by salicylic acid and heat hardening in tall fescue seedlings. Journal of Plant Physiology and Molecular Biology 28: 89-95.
  • Kawano T, Sahashi N, Takahashi K, Uozumi N, Muto S (1998). Salicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: the earliest events in salicylic acid signal transduction. Plant Cell Physiology 39: 721-730. doi: 10.1093/ oxfordjournals.pcp.a029426
  • Khan MIR, Asgher M, Khan NA (2014). Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycine betaine and ethylene in mung bean (Vigna radiata L.). Plant Physioloy and Biochemistry 80: 67-74. doi: 10.1016/j. plaphy.2014.03.026.
  • Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015). Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Frontiers in Plant Science 6: 462-472. doi: 10.3389/fpls.2015.00462
  • Kiddle GA, Doughty KJ, Wallsgrove RM (1994). Salicylic acidinduced accumulation of glucosinolates in oilseed rape (Brassica napus L.) leaves. Journal of Experimental Botany 45: 1343-1346. doi:10.1093/jxb/45.9.1343
  • Larkindale J, Hall JD, Knight MR, Verling E (2005). Heat stress phenotypes of Arabidopsis mutants simplicate multiple signalling pathways in the acquisition of thermotolerance. Plant Physiology 138: 882-897. doi: 10.1104/pp.105.062257
  • Larkindale J, Knight MR (2002). Protection against heat stressinduced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiology 128: 682-695. doi: 10.1104/pp.010320
  • Levitt J (1980). Responses of Plants to Environmental Stresses: Water, Radiation, Salt and Other Stresses, 2nd ed. New York, NY, USA: Academic Press.
  • Lopez-Delgado H, Dat JF, Foyer CH, Scott IM (1998). Induction of thermotolerance in potato microplants by acetylsalicylic acid and H2 O2 . Journal of Experimental Botany 49: 713-720. doi: 10.1093/jxb/49.321.713
  • Praveen N, Murthy HN (2010). Production of withanolide A from adventitious root cultures of Withania somnifera. Acta Physiologiae Plantarum 5: 1017-1022. doi: 10.1007/s11738- 010-0489-7
  • Rao MV, Paliyath G, Ormrod P, Murr DP, Watkins CB (1997). Influence of salicylic acid on H2 O2 production, oxidative stress and H2 O2 -metabolizing enzymes. Plant Physiology 115: 137- 149. doi:10.1104/pp.115.1.137
  • Raskin I, Skubatz H, Tang W, Meeuse BJD (1990). Salicylic acid in thermogenic and non-thermogenic plants. Annals of Botany 66: 369-373. doi: 10.1093/oxfordjournals.aob.a088037
  • Ruiz JM, Rivero RM, Lopez-Cantarero I, Romero L (2003). Role of Ca2+ in metabolism of phenolic compounds in tobacco leaves (Nicotiana tabacum L.). Plant Growth Regulation 41: 173-177. doi: 10.1023/A:102735842
  • Sivanandhan G, Arun M, Mayavan S, Rajesh M, Mariashibu TS et al. (2012). Chitosan enhances withanolides production in adventitious root cultures of Withania somnifera (L.) Dunal. Industrial Crops and Products 37: 124-129. doi: 10.1016/j. indcrop.2011.11.022
  • Sivanandhan G, Selvaraj N, Ganapathi A, Manickavasagam M (2014). An efficient hairy root culture system for Withania somnifera (L.) Dunal. African Journal of Biotechnology 13: 4141-4147. doi: 10.5897/AJB2014.14128
  • Takshak S, Agrawal SB (2014). Effect of ultraviolet-B radiation on biomass production, lipid peroxidation, reactive oxygen species, and antioxidants in Withania somnifera. Biologia Plantarum 58: 328-334. doi: 10.1007/s10535-014-0390-0
  • Tari I, Csiszar J, Szalai G, Horvath F, Pecsvaradi A et al. (2002). Acclimation of tomato plants to salinity stress after a salicylic acid pre-treatment. Acta Biologica Szegediensis 46: 55-56. Van Camp W, Montagu MV, Inze D (1998). H2 O2 and NO: redox signals in disease resistance. Trends in Plant Science 3: 330-334.
  • Wang LJ, Fan L, Loescher W, Duan W, Liu GJ et al. (2010). Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biology 10: 34-43. doi: 10.1186/1471-2229-10-34
  • Wang LJ, Li SH (2006). Thermotolerance and related antioxidant enzyme activities induced by heat acclimation and salicylic acid in grape (Vitis vinifera L.) leaves. Plant Growth Regulation 48: 137-144. doi: 10.1007/s10725-005-6146-2
  • Yücesan B, Mohammed A, Arslan M, Gürel E (2015). Clonal propagation and synthetic seed production from nodal segments of Cape gooseberry (Physalis peruviana L.), a tropical fruit plant. Turkish Journal of Agriculture and Forestry 39: 797-806. doi: 10.3906/tar-1412-86
  • Zhang Y, Xu S, Yang S, Chen Y (2015). Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through up-regulating antioxidant defence system in two melon cultivars (Cucumis melo L.). Protoplasma 252: 911-924. doi: 10.1007/s00709-014-0732-y
  • Zhang CS, Lu Q, Verma DPS (1995). Removal of feedback inhibition of P5CS, a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants. The Journal of Biological Chemistry 270: 20491-20496. doi: 10.1074/jbc.270.35.20491
Turkish Journal of Botany-Cover
  • ISSN: 1300-008X
  • Yayın Aralığı: 6
  • Yayıncı: TÜBİTAK
Sayıdaki Diğer Makaleler

Patryk MIZIA, Kamil MYSZCZYNSKI, Monika SLIPIKO, Katarzyna KRAWCZYK, Vitezslav PLÁSEK, Monika SZCZECINSKA, Jakub SAWICKI

Ming CHEN, Peipei QIAN, Zhankui WANG, Yingjie SHU, Yuan TAO, Liyan HUANG, Yilong WANG, Haihong ZHAO, Hao MA

İlhami TÜZÜN, Zeynep Elibol ÇAKMAK, Emmanuel YOUNG, Turgay ÇAKMAK

Fruit and seed macro- and micromorphologies of the genus Matthiola (Brassicaceae) in Turkey and their taxonomic value

Ayla KAYA, Abdurrahman SEFALI, Esra MARTİN, Murat ÜNAL

Comparative plastomes analysis reveals the first infrageneric evolutionary hotspots of Orthotrichum s.l. (Orthotrichaceae, Bryophyta)

Katarzyna KRAWCZYK, Patryk MIZIA, Kamil MYSZCZYNSKI, Vitezslav PLASEK, Monika SLIPIKO, Jakub SAWICKI, Monika SZCZECINSKA

Natural and anthropic forest fragments have distinct ecological behavior due to their different origin and landscape context

Rubens Manoel dos SANTOS, Paola Ferreira SANTOS, Polyanne Aparecida COELHO, Jean Daniel MOREL, Gisele Cristina de Oliveira MENINO, Aline Martins MOREIRA, Cleber Rodrigo de SOUZA

Silvia AGUILAR-RODRIGUEZ, Teresa TERRAZAS, Xicotencatl CAMACHO-CORONEL

Identification and functional analysis of soybean GmSBH1 gene promoter conferring high temperature- and humidity-induced expression

Zhankui WANG, Haihong ZHAO, Peipei QIAN, Yilong WANG, Ming CHEN, Yingjie SHU, Yuan TAO, Liyan HUANG, Hao MA

Effects of salicylic acid and heat acclimation on thermotolerance and withanolide accumulation under high temperature stress in the Cape gooseberry (Physalis peruviana L.)

Günce ŞAHİN

Ayla KAYA, Murat ÜNAL, Abdurrahman SEFALI, Esra MARTİN