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Salt stress (NaCl) affects plant growth and branch pathways of carotenoid and flavonoid biosyntheses in Solanum nigrum

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Abstract

In this study, we set out to investigate the effect of sodium chloride (NaCl) on carotenoid and flavonoid production by the black nightshade (Solanum nigrum L.). The study was carried out under green chamber conditions using seedlings subjected to 0, 50, 100 and 150 mM NaCl for 3 weeks. The negative effect of NaCl on dry biomass production of roots and leaves were accompanied by a significant restriction in K+, Ca2+ and Mg2+ ion uptake and by an increase in Na+ ion concentrations, the effects of which were most pronounced at the highest NaCl level. Salt stress also induced oxidative stress, according to the amplified levels of thiobarbituric acid reactive substances and relative ion leakage ratio. Expression of some related carotenoid (phytoene synthase 2 and β-lycopene cyclase) and flavonoids genes (phenylalanine ammonialyase, chalcone synthase and flavonol synthase) were induced by NaCl, followed enhanced production of β-carotene, lutein, and quercetin 3-β-d-glucoside. At the highest NaCl level (150 mM NaCl), quercetin 3-β-d-glucoside synthesis came at the expense of reduced β-carotene and lutein, while salt stress treatment affected leaf antioxidant activities to a great extent relative to the control. Our data suggest that the potential antioxidant properties of carotenoids and flavonoids and their related key genes may be efficiently involved in the restriction of salt-induced oxidative damages.

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Abbreviations

NaCl:

Sodium chloride

ROS:

Reactive oxygen species

WC:

Water content

Chl:

Chlorophyll

TBARS:

Thiobarbituric acid reactive substances

RLR:

Relative ion leakage ratio

HPLC:

High performance liquid chromatography

TPC:

Total phenolic content

TFC:

Total flavonoid content

TAA:

Total antioxidant activity

PCR:

Polymerase chain reaction

Sn :

Solanum nigrum

PSY1:

Phytoene synthase 1

PSY2:

Phytoene synthase 2, β-LCY, β-lycopene cyclase

PAL:

Phenylalanine ammonialyase

CHS:

Chalcone synthase

FLS:

Flavonol synthase

References

  • Agati G, Biricolti S, Guidi L, Ferrini F, Fini A, Tattini M (2011) The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves. J Plant Physiol 168:204–212. doi:10.1016/j.jplph.2010.07.016

    Article  CAS  PubMed  Google Scholar 

  • Atanu FO, Ebiloma UG, Ajayi EI (2011) A review of the pharmacological aspects of Solanum nigrum Linn. Biotechnol Mol Biol Rev 6(1):1–7

    CAS  Google Scholar 

  • Cataldi TRI, Margiotta G, Del Fiore A, Bufo SA (2003) Ionic content in plant extracts determined by ion chromatography with conductivity detection. Phytochem Anal 14:176–183. doi:10.1002/pca.700

    Article  CAS  PubMed  Google Scholar 

  • Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 38:833–847. doi:10.1071/FP11192

    Article  CAS  Google Scholar 

  • Chan C, Lam HM (2013) A putative lambda class glutathione S-transferase enhances plant survival under salinity stress. Plant Cell Physiol 55(3):570–579. doi:10.1093/pcp/pct201

    Article  Google Scholar 

  • Chen X, Han H, Jiang P, Nie L, Bao H, Fan P, Lv S, Feng J, Li Y (2011) Transformation of β-lycopene cyclase genes from Salicornia europaea and Arabidopsis conferred salt tolerance in Arabidopsis and Tobacco. Plant Cell Physiol 52(5):909–921. doi:10.4238/2014

    Article  CAS  PubMed  Google Scholar 

  • Cheng YJ, Kim M-D, Deng XP, Kwak S-S, Chen W (2013) Enhanced salt stress tolerance in transgenic potato plants expressing IbMYB1, a sweet potato transcription factor. J Microbiol Biotechnol 23(12):1737–1746. doi:10.4014/jmb.1307.07024

    Article  CAS  PubMed  Google Scholar 

  • Dall’Osto L, Fiore A, Cazzaniga S, Giuliano G, Bassi R (2007) Different roles of alpha- and beta-branch xanthophylls in photosystem assembly and photoprotection. J Biol Chem 282:35056–35068. doi:10.1074/jbc.M704729200

    Article  PubMed  Google Scholar 

  • Dehghan S, Sadeghi M, Pöppel A, Fischer R, Lakes-Harlan R, Kavousi HR, Vilcinskas A, Rahnamaeian M (2014) Differential inductions of phenylalanine ammonia-lyase and chalcone synthase during wounding, salicylic acid treatment, and salinity stress in safflower, Carthamus tinctorius. Biosci Rep 34(3):273–282. doi:10.1042/BSR20140026

    Article  CAS  Google Scholar 

  • Dewanto V, Wu X, Adom KK, Liu RH (2002) Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agric Food Chem 50:3010–3014

    Article  CAS  PubMed  Google Scholar 

  • Fraser PD, Enfissi EMA, Halket JM, Truesdale MR, Yu D, Gerrish C, Bramley PM (2007) Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism. Plant Cell 19:3194–3211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García-Calderón M, Pons-Ferrer T, Mrázova A, Pal’ove-Balang P, Vilková M, Pérez-Delgado CM, Vega JM, Eliášová A, Repˇcák M, Márquez AJ, Betti M (2015) Modulation of phenolic metabolism under stress conditions in a Lotus japonicus mutant lacking plastidic glutamine synthetase. Front Plant Sci 6:760. doi:10.3389/fpls.2015.00760

    Article  PubMed  PubMed Central  Google Scholar 

  • Gou YJ, Felippes FF, Jun Liu C, Weigel D, Wei Wang J (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:1–18. doi:10.1155/2014/701596

    Article  Google Scholar 

  • Hajlaoui H, Denden M, El Ayed N (2009) Differential responses of two maize (Zea mays L.) varieties to salt stress: changes on polyphenols composition of foliage and oxidative damages. Ind Crop Prod 30:144–151. doi:10.1016/j.indcrop.2009.03.003

    Article  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322. doi:10.1104/pp.106.077073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han H, Li Y, Zhou S (2008) Overexpression of phytoene synthase gene from Salicornia europaea alters response to reactive oxygen species under salt stress in transgenic Arabidopsis. Biotechnol Lett 30:1501–1507. doi:10.1007/s10529-008-9705-6

    Article  CAS  PubMed  Google Scholar 

  • Han RM, Zhang JP, Skibsted LH (2012) Reaction dynamics of flavonoids and carotenoidsas antioxidants. Molecules 17:2140–2160. doi:10.3390/molecules17022140

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1940) The water culture method for growing plants without soil. Circular 347 College of Agriculture, University of California

  • Horie T, Karahara I, Katsuhara M (2012) Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants. Rice 5(11):1–18

    Google Scholar 

  • Hui-kun D, Yan Z, Dong-dong QI, Wen-long LI, Xue-jun H, Yong-xiu L, Xin D (2012) Comparative study on the expression of genes involved in carotenoid and ABA biosynthetic pathway in response to salt stress in tomato. J Integr Agric 11(7):1093–1102. doi:10.1016/S2095-3119(12)60102-6

    Article  Google Scholar 

  • Lichlenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  Google Scholar 

  • Lijuan C, Huiming G, Yi L, Hongmei C (2015) Chalcone synthase EaCHS1 from Eupatorium adenophorum functions in salt stress tolerance in tobacco. Plant Cell Rep 34:885–894. doi:10.1007/s00299-015-1751-7

    Article  PubMed  Google Scholar 

  • Lillo C, Lea US, Ruoff P (2008) Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant, Cell Environ 31:587–601. doi:10.1111/j.1365-3040.2007.01748.x

    Article  CAS  Google Scholar 

  • Mahmoudi H, Kaddour R, Huang J, Nasri N, Olfa B, M’Rah S, Hannoufa A, Lachaâl M, Ouerghi Z (2011) Varied tolerance to NaCl salinity is related to biochemical changes in two contrasting lettuce genotypes. Acta Physiol Plant 33:1613–1622. doi:10.1007/s11738-010-0696-2

    Article  CAS  Google Scholar 

  • Mansour MMF (2013) Plasma membrane permeability as an indicator of salt tolerance in plants. Biol Plant 57(1):1–10. doi:10.1007/s10535-012-0144

    Article  CAS  Google Scholar 

  • Maurya VK, Srinvasan R, Ramesh N, Anbalagan M, Gothandam KM (2015) Expression of carotenoid pathway genes in three Capsicum varieties under salt Stress. Asian J Crop Sci 7(4):286–294. doi:10.3923/ajcs.2015.286.294

    Article  Google Scholar 

  • Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113. doi:10.1093/jxb/erh113

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi:10.1146/annurev.arplant.59.032607.092911

    Article  CAS  PubMed  Google Scholar 

  • Nicot N, Hausman JF, Hoffmann L, le Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56(421):2907–2914. doi:10.1093/jxb/eri285

    Article  CAS  PubMed  Google Scholar 

  • Pandey A et al (2015) AtMYB12 expression in tomato leads to large scale differential modulation in transcriptome and flavonoid content in leaf and fruit tissues. Sci Rep 5:12412. doi:10.1038/srep12412

    Article  PubMed  PubMed Central  Google Scholar 

  • Payyavula RS, Navarre DA, Kuhl JC, Pantoja A, Pillai SS (2012) Differential effects of environment on potato phenylpropanoid and carotenoid expression. BMC Plant Biol 12(39):1–17. doi:10.1186/1471-2229-12-39

    Google Scholar 

  • Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269:337–341. doi:10.1006/abio.1999.4019

    Article  CAS  PubMed  Google Scholar 

  • Rajasekaran LR, Aspinall D, Paleg LG (2000) Physiological mechanism of tolerance of Lycopersicon spp. exposed to salt stress. Can J Plant Sci 80:151–159. doi:10.4141/P99-003

    Article  Google Scholar 

  • Raju M, Varakumar S, Lakshminarayana R, Krishnakantha PT, Baskaran V (2007) Carotenoids composition and vitamin A activity of medicinally important green leafy vegetables. Food Chem 101:1598–1605

    Article  CAS  Google Scholar 

  • Reginato MA, Castagna A, Furla´n 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 6:1–13. doi:10.1093/aobpla/plu042

    Article  Google Scholar 

  • Scattino C, Castagna A, Neugart SM, Chan H, Schreiner MH, Crisosto C, Tonutti P, Ranieri A (2014) Post-harvest UV-B irradiation induces changes of phenol contents and corresponding biosynthetic gene expression in peaches and nectarines. Food Chem 163:51–60. doi:10.1016/j.foodchem.2014.04.077

    Article  CAS  PubMed  Google Scholar 

  • Schmidt DD, Kessler A, Kessler D, Schmidt S, Lim M, Gase M, Baldwin IT (2004) Solanum nigrum: a model ecological expression system and its tools. Mol Ecol 13:981–995

    Article  CAS  PubMed  Google Scholar 

  • Shabala S, Cuin TA, Pang J, Percey W, Chen Z, Conn S, Eing C, Wegner LH (2010) Xylem ionic relations and salinity tolerance in barley. Plant J 61:839–853

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Xu X, Zhu H, Liu A, Liu L, Li J, Hua X (2010) Comparative transcriptomic profiling of salt tolerant wild tomato species and salt sensitive tomato cultivar. Plant Cell Physiol 51:997–1006

    Article  CAS  PubMed  Google Scholar 

  • Šutković J, Ler D, Abdel Gawwad MR (2011) In vitro production of solasodine alkaloid in Solanum nigrum under salt stress. J Phytol 3(1):43–49

    Google Scholar 

  • Tarchoune I, Degl’Innocenti E, Kaddour R, Guidi L, Lachaâl M, Navari-Izzo F, Ouerghi Z (2012) Effects of NaCl or Na2SO4 salinity on plant growth, ion content and photosynthetic activity in Ocimum basilicum L. Acta Physiol Plant 34:607–615

    Article  CAS  Google Scholar 

  • Valifard M, Mohsenzadeh S, Niazi A, Moghadam A (2015) Phenylalanine ammonia lyase isolation and functional analysis of phenylpropanoid pathway under salinity stress in Salvia species. AJCS 9(7):656–665

    Google Scholar 

  • Wang HC, Chung PJ, Wu CH, Lan KP, Yang MY, Wang CJ (2011) Solanum nigrum L. polyphenolic extract inhibits hepatocarcinoma cell growth by inducing G2/M phase arrest and apoptosis. J Sci Food Agric 91:178–185. doi:10.1002/jsfa.4170

    Article  CAS  PubMed  Google Scholar 

  • Welsch R, Wust F, Bar C, Al-Babili S, Beyer P (2008) A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of phytoene synthase genes. Plant Physiol 147:367–380. doi:10.1104/pp.108.117028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Sun J, Du L, Liu X (2012) Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytol 196:110–124

    Article  CAS  PubMed  Google Scholar 

  • Yin R, Messner B, Kessler TF, Hoffmann T, Schwab W, Hajirezaei MR, Saint Paul VV, Heller W, Schaffner AR (2012) Feedback inhibition of the general phenylpropanoid and flavonol biosynthetic pathways upon a compromised flavonol-3-O-glycosylation. J Exp Bot 16:1–14. doi:10.1093/jxb/err416

    Google Scholar 

  • Yu B, Lydiate DJ, Schafer UA, Hannoufa A (2007) Characterization of a β-carotene hydroxylase of Adonis aestivalis and its expression in Arabidopsis thaliana. Planta 226(1):181–192. doi:10.1007/s00425-006-0455-1

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was conducted as part of a Canada-Tunisia collaboration, supported by Ministry of Higher Education and Scientific Research of Tunisia and Agriculture and Agri-Food Canada.

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Authors and Affiliations

  1. Southern Crop Protection and Food Research Centre, Agriculture and Agri-Food Canada, 1391 Sandford Street, London, ON, N5V 4T3, Canada

    Saoussen Ben Abdallah, Banyar Aung, Lisa Amyot, Igor Lalin & Abdelali Hannoufa

  2. Unité de Physiologie et Biochimie de la Réponse des Plantes aux Contraintes Abiotiques, Faculté des Sciences de Tunis, Campus Universitaire, 2092, Tunis El Manar, Tunisia

    Saoussen Ben Abdallah, Mokhtar Lachâal & Najoua Karray-Bouraoui

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  1. Saoussen Ben Abdallah
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  2. Banyar Aung
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  3. Lisa Amyot
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  5. Mokhtar Lachâal
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Correspondence to Saoussen Ben Abdallah.

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Communicated by JV Jorrin-Novo.

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Ben Abdallah, S., Aung, B., Amyot, L. et al. Salt stress (NaCl) affects plant growth and branch pathways of carotenoid and flavonoid biosyntheses in Solanum nigrum . Acta Physiol Plant 38, 72 (2016). https://doi.org/10.1007/s11738-016-2096-8

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  • DOI: https://doi.org/10.1007/s11738-016-2096-8

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