Abstract
Salinity causes massive loss of economic crops due to the build-up of toxic salts in shoot. Rosmarinic acid (RA) has been known to prevent the inevitable damage to vital biological molecules under stress. There is an increasing interest, therefore, in the use of polyphenols in crop stress physiology studies. An in vitro regeneration protocol was established using explants of the potato cultivar White Desiree to assess tolerance to salinity at a morphological, cellular, and biochemical level. Additionally, we examined the potential ameliorative effects of RA on growth in salt-stressed potato explants. Based on our observations, we propose a model for the ameliorative effects of a caffeic acid conjugate of α-hydroxyhydrocaffeic acid. Explants of White Desiree showed differential responses to salt and RA supplementation. Salt-stressed and control explants grown in RA-supplemented media showed a pronounced expansion of leaf area, suggesting direct effects of RA on cell elongation in potato explants. Root elongation was less affected by salinity in comparison to shoot elongation. Moderate levels of RA resulted in stimulatory effects on growth. The microscopic examination of leaves and stems indicated the presence of unique trichomes at the early stages of explant growth under RA supplementation, which varied considerably in size, shape, and distribution in response to stress. Our data indicated that RA significantly decreased osmolyte content under stress. Salinity resulted in the biosynthesis of high levels of free proline, carbohydrates, and malondialdehyde (MDA). However, the lower contents of MDA in salt-stressed explants treated with RA indicate that RA possesses anti-lipid peroxidation properties. Our observations provide evidence for the stimulatory effects of RA on cellular growth and the protection of membranes from ion toxicity.
Similar content being viewed by others
References
Abeles FB, Morgan PW, Saltveit ME Jr (2012) Ethylene in plant biology. Academic Press, London
Adedeji O, Ajuwon O, Babawale O (2007) Foliar epidermal studies, organographic distribution and taxonomic importance of trichomes in the family Solanaceae. Int J Botany 3:276–282
Ahmad HH, Hamza AH, Hassan AZ, Sayed AH (2013) Promising therapeutic role of Rosmarinus officinalis successive methanolic fraction against colorectal cancer. Int J Pharm Pharm Sci 5:164–170
Anjum SA, Farooq M, Xie X, Liu X, Ijaz MF (2012) Antioxidant defense system and proline accumulation enables hot pepper to perform better under drought. Sci Hort 140:66–73
Ashraf M (2002) Salt tolerance of cotton: some new advances. CRC Crit Rev Plant Sci 21:1–30
Bai J-P, Gao H-J, Yang H-Y, Lou Y, Zhang J-L, Wang D, Zhang J-L (2016) Comparison of ultrastructural and physiological changes of potato (Solanum tuberosum L.) plantlets subjected to salt and modeling drought stresses. Acta Physiol Plant 38:1–9
Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Bayuelo-Jimenez JS, Craig R, Lynch JP (2002) Salinity tolerance of species during germination and early seedling growth. Crop Sci 42:1584–1594
Brown C (2005) Antioxidants in potato. Am J Potato Res 82:163–172
Cai-Hong P, Su-Jun Z, Zhi-Zhong G, Bao-Shan W (2005) NaCl treatment markedly enhances H2O2-scavenging system in leaves of halophyte Suaeda salsa. Physiol Plant 125:490–499
Costa P, Gonçalves S, Andrade PB, Valentão P, Romano A (2011) Inhibitory effect of Lavandula viridis on Fe2+-induced lipid peroxidation, antioxidant and anti-cholinesterase properties. Food Chem 126:1779–1786
Ehsanpour A, Jones M (2000) Evaluation of direct shoot regeneration from stem explants of potato (Solanum tuberosum L.) cv. Delaware by thidiazuron (TDZ). J Sci Technol Agric Natural Resour 4:47–54
Elaleem KGA, Modawi RS, Khalafalla MM (2009) Effect of plant growth regulators on callus induction and plant regeneration in tuber segment culture of potato (Solanum tuberosum L.) cultivar Diamant. Afr J Biotechnol 8:2529–2534
FAO (2015) World food and agriculture 2015. FAO, Rome
FAO (2016) The state of food and agriculture. Climate change, agriculture and food security. Food and Agriculture Organization of the United Nations, Rome (ISBN 978-92-5-109374-0)
Fernández-Segura E, Canizares FJ, Cubero MA, Warley A, Campos A (1999) Changes in elemental content during apoptotic cell death studied by electron probe X-ray microanalysis. Exp Cell Res 253:454–462
Fry W (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9:385–402
Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254
Fu Q, Yang R, Wang H, Zhao B, Zhou C, Ren S, Guo Y-D (2013) Leaf morphological and ultrastructural performance of eggplant (Solanum melongena L.) in response to water stress. Photosynthetica 51:109–114
Furtado RA, Oliveira BR, Silva LR, Cleto SS, Munari CC, Cunha WR, Tavares DC (2015) Chemopreventive effects of rosmarinic acid on rat colon carcinogenesis. Eur J Cancer Prev 24:106–112
Gelmesa D, Dechassa N, Mohammed W, Gebre E, Monneveux P, Bündig C, Winkelmann T (2017) In vitro screening of potato genotypes for osmotic stress tolerance. Open Agric 2:308–316
González-Vallinas M, Reglero G, Ramirez de Molina A (2015) Rosemary (Rosmarinus officinalis L.) extract as a potential complementary agent in anticancer therapy. Nutr Cancer 67:1223–1231
Gustavsson J, Cederberg C, Sonesson U, Emanuelsson A (2013) The methodology of the FAO study: “Global Food Losses and Food Waste-extent, causes and prevention”-FAO, 2011. Gӧteborg, Sweden
Guyer A, De Vrieze M, Bӧnisch D, Gloor R, Musa T, Bodenhausen N, Bailly A, Weisskopf L (2015) The anti-Phytophthora effect of selected potato-associated Pseudomonas strains: from the laboratory to the field. Front Microbiol 6(1309):1–13
Hakkim F, Kalyani S, Essa M, Girija S, Song H (2011) Production of rosmarinic acid in Ocimum sanctum (L.) cell suspension cultures by the influence of growth regulators. Int J Biol Med Res 2:1158–1161
Hansen J, Nielsen B, Nielsen SV (1999) In vitro shoot regeneration of Solanum tuberosum cultivars: interactions of medium composition and leaf, leaflet, and explant position. Potato Res 42:141–151
Hao W, Guo H, Zhang J, Hu G, Yao Y, Dong J (2014) Hydrogen peroxide is involved in salicylic acid-elicited rosmarinic acid production in Salvia miltiorrhiza cell cultures. Sci World J 2014:1–7
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant System and O2−/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831
Horton D, Sawyer RL (1985) The potato as a world food crop, with special reference to developing areas. In: Li PH (ed) Potato physiology. Academic Press, London, pp 1–34
Huttunen P, Kärkkäinen K, Løe G, Rautio P, Ågren J (2010) Leaf trichome production and responses to defoliation and drought in Arabidopsis lyrata (Brassicaceae). Ann Bot Fenn 47:199–207
James J, Alder N, Mühling K, Läuchli A, Shackel K, Donovan L, Richards J (2006) High apoplastic solute concentrations in leaves alter water relations of the halophytic shrub, Sarcobatus vermiculatus. J Exp Bot 57:139–147
Jamil M, Lee CC, Rehman SU, Lee DB, Ashraf M, Rha ES (2005) Salinity (NaCl) tolerance of Brassica species at germination and early seedling growth. Electron J Environ Agric Food Chem 4:970–976
Jin B-R, Chung K-S, Cheon S-Y, Lee M, Hwang S, Hwang SN, Rhee K-J, An H-J (2017) Rosmarinic acid suppresses colonic inflammation in dextran sulphate sodium (DSS)-induced mice via dual inhibition of NF-\kappa B and STAT3 activation. Sci Rep 7:1–11
Khatun N, Bari M, Islam R, Huda S, Siddque N, Rahman M, Mullah M (2003) Callus induction and regeneration from nodal segment of potato cultivar Diamant. J Biol Sci 3:1101–1106
Kim H-J, Seo E-Y, Kim J-H, Cheong H-J, Kang B-C, Choi D-I (2012) Morphological classification of trichomes associated with possible biotic stress resistance in the genus Capsicum. Plant Pathol J 28:107–113
Kissoudis C, van de Wiel C, Visser RG, van der Linden G (2014) Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk. Front Plant Sci 5:1–20
Koca H, Ozdemir F, Turkan I (2006) Effect of salt stress on lipid peroxidation and superoxide dismutase and peroxidase activities of Lycopersicon esculentum and L. pennellii. Biol Plant 50:745–748
Latijnhouwers M, Ligterink W, Vleeshouwers VG, van West P, Govers F (2004) A Gɑ subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans. Mol Microbiol 51:925–936
Levy D, Veilleux RE (2007) Adaptation of potato to high temperatures and salinity—a review. Am J Potato Res 84:487–506
Lianes A, Bertazza G, Palacio G, Luna V (2013) Different sodium salts cause different solute accumulation in the halophyte Prosopis strombulifera. Plant Biol 15:118–125
Lichtenthaler HK (1987) [34] Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592
Margineanu A-M, Molnár I, Rakosy-Tican E (2014) Trichomes types analysis and their density in parental species Solanum tuberosum and S. chacoense and their derived somatic hybrids. Analele Stiintifice ale Universitatii “Al I Cuza” din Iasi 60:33
Martinez CA, Maestri M, Lani EG (1996) In vitro salt tolerance and proline accumulation in Andean potato (Solanum spp.) differing in frost resistance. Plant Sci 116:177–184
Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exper Bot 49:69–76
Mohamed AA, Matter MA, Saker MM (2010) Effect of salt stress on some defense mechanisms of transgenic and wild potato clones (Solanum tuberosum L.) grown in vitro. Nature 12:8
Moore J, Yousef M, Tsiani E (2016) Anticancer effects of rosemary (Rosmarinus officinalis L.) extract and rosemary extract polyphenols. Nutrients 8:731
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Murashige T, Skoog F (1962) Manipulation of organ initiation in plant tissue cultures. Bot Bull Acad Sin 18:1–24
Murshed R, Najla S, Albiski F, Kassem I, Jbour M, Al-Said H (2015) Using growth parameters for in vitro screening of potato varieties tolerant to salt stress. J Agric Sci Technol 17:483–494
Neumann PM (1995) Inhabitation of root growth by salinity stress: toxicity or an adaptive biophysical response. In: Baluska F, Ciamporova M, Gasparikova O, Barlow PW (eds) Structure and function of roots. Kluwer Academic, The Netherlands, pp 299–304
Ozturk H, Ozturk H, Terzi EH, Ozgen U, Duran A, Uygun I (2014) Protective effects of rosmarinic acid against renal ischaemia/reperfusion injury in rats. J Pak Med Assoc 64:260–265
Park WT, Arasu MV, Al-Dhabi NA, Yeo SK, Jeon J, Park JS, Lee SY, Park SU (2016) Yeast extract and silver nitrate induce the expression of phenylpropanoid biosynthetic genes and induce the accumulation of rosmarinic acid in Agastache rugosa cell culture. Molecules 21:426
Pearson D (1976) The chemical analysis of foods, 7th edn. Longman Group Ltd, Harlow, p xii
Rahman M, Islam R, Hossain M, Haider S (2008) Differential response of potato under sodium chloride stress conditions in vitro. J Biosci 16:79–83
Reginato MA, Castagna A, Furlán A, Castro S, Ranieri A, Luna V (2014) Physiological responses of a halophytic shrub to salt stress by Na2SO4 and NaCl: oxidative damage and the role of polyphenols in antioxidant protection. AoB Plants 6:plu042
Roomans GM (1988) Introduction to X-ray microanalysis in biology. J Electron Microsc Tech 9:3–17
Saeedipour S (2013) Relationship of grain yield, ABA and proline accumulation in tolerant and sensitive wheat cultivars as affected by water stress. Proc Natl Acad Sci India Sect B 83:311–315
Sahraroo A, Babalar M, Mirjalili MH, Moghaddam MRF, Ebrahimi SN (2014) In-vitro callus induction and rosmarinic acid quantification in callus culture of Satureja khuzistanica Jamzad (Lamiaceae). Iran J Pharm Res 13:1447
Sharmila R, Manoharan S (2012) Anti-tumor activity of rosmarinic acid in 7, 12-dimethylbenz (a) anthracene (DMBA) induced skin carcinogenesis in Swiss albino mice. Indian J Exp Biol 50:187
Shirin F, Hossain M, Kabir M, Roy M, Sarker S (2007) Callus induction and plant regeneration from internodal and leaf explants of four potato (Solanum tuberosum L.) cultivars. World J Agric Sci 3:01–06
Skepper JN, Karydis I, Garnett MR, Hegyi L, Hardwick SJ, Warley A, Mitchinson MJ, Cary NR (1999) Changes in elemental concentrations are associated with early stages of apoptosis in human monocyte-macrophages exposed to oxidized low-density lipoprotein: an X-ray microanalytical study. J Pathol 188:100–106
Tache A, Radu G-L, Litescu S-C (2012) Assessment of role of rosmarinic acid in preventing oxidative process of low density lipoproteins. Chem Pap 66:1166–1170
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction. Plant J 11:1187–1194
Toth J, Mrlianova M, Tekelova D, Koremova M (2003) Rosmarinic acid an important phenolic active compound of Lemon Balm (Melissa officinalis). Acta Fac Pharm Univ Comen 50:139–146
Tsedaley B (2014) Late blight of potato (Phytophthora infestans) biology, economic importance and its management approaches. J Biol Agric Healthc 25:215–226
Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132
Wang PJ, Hu CY (1985) Potato tissue culture and its application in agriculture. In: Li PH (ed) Potato physiology. Academic, London, pp 503–577
Warley A (1997) X-ray microanalysis for biologists. Ashgate Publishing, Farnham
Werner JE, Finkelstein RR (1995) Arabidopsis mutants with reduced response to NaCl and osmotic stress. Physiol Plant 93:659–666
Xu W, Yang F, Zhang Y, Shen X (2016) Protective effects of rosmarinic acid against radiation-induced damage to the hematopoietic system in mice. J Rad Res 57:356–362
Yemm E, Willis A (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508
Zaman MS, Ali GM, Muhammad A, Farooq K, Hussain I et al (2015) In vitro screening of salt tolerance in potato (Solanum tuberosum L.) varieties. Sarhad J Agric 31:106–113
Zhang J, Kirkham M (1996) Lipid peroxidation in sorghum and sunflower seedlings as affected by ascorbic acid, benzoic acid, and propyl gallate. J Plant Physiol 149:489–493
Zhang W, Roomans GM (1998) Volume-induced chloride transport in HT29 cells studied by X-ray microanalysis. Microsc Res Tech 40:72–78
Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6:66–71
Acknowledgements
Authors of this study would like to thank University of Isfahan for providing facilities for in vitro potato generation. We express our sincere thanks to Miss Ahlam Al-Kadi from the NanoScope Center at Kuwait University for her help in sample preparation, and Mr. Mohamed Rajab for SEM microscopy.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by M. Capuana.
Rights and permissions
About this article
Cite this article
Eskandari, H., Al-Mansour, N. & Ehsanpour, A.A. Rosmarinic acid ameliorates the negative effects of salinity in in vitro-regenerated potato explants (Solanum tuberosum L.). Acta Physiol Plant 40, 74 (2018). https://doi.org/10.1007/s11738-018-2622-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-018-2622-y