Skip to main content

Advertisement

SpringerLink
Log in

Growth and alkaloid production along with expression profiles of biosynthetic pathway genes in two contrasting morphotypes of prickly and prickleless Solanum viarum Dunal

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Growth and production kinetics of three important glycoalkaloids viz. α-solanine, solanidine, and solasodine in two contrasting prickly and prickleless plants of Solanum viarum Dunal were evaluated under in vitro conditions. The prickleless plants showed improved accumulation of total glycoalkaloid content [7.11 and 6.85 mg g−1 dry weight (DW)] and growth (GI = 11.08 and 19.26) after 45 and 50 days of culture cycle, respectively. For higher biomass (91.18 g l−1) as well as glycoalkaloid (52.56 mg l−1) recovery, the prickleless plants served as highly profitable platform. All the three studied glycoalkaloids were identified and quantified by mass spectrometry and HPLC. All the three studied glycoalkaloids accumulated in age-dependent manner. The presence of two constituents, i.e., solasodine and solanidine mainly contributed for higher accumulation of total glycoalkaloid content in the prickleless plants. However, the synthesis of α-solanine was highly age specific and could be detected after 4 to 5 weeks of culture cycle in both prickle containing as well as prickleless plants of S. viarum. The higher accumulation of glycoalkaloids in prickleless plants was also supported with the expression analysis of six key pathway enzymes viz. mevalonate kinase (MVK), 3-hydroxy-3-methyl-glutaryl coenzyme A reductase (HMGR), farnesyl diphosphate synthase (FPS), UDP-galactose/solanidine galactosyltransferase (SGT1), UDP-glucose/solanidine glucosyltransferase (SGT2), and cytochrome P450 monooxygenase (CYP). The results indicated that the plants harvested after 45 and 50 days of culture cycle accumulated maximum bioactive in-demand glycoalkaloids in the prickly and prickleless plants of S. viarum Dunal, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abe I, Rohmer M, Prestwich GD (1993) Enzymatic cyclization of squalene and oxidosqualene to sterols and triterpenes. Chem Rev 93:2189–2206

    Article  CAS  Google Scholar 

  • Alvarez MA (2014) Solasodine production in Solanum eleagnifolium in vitro cultures. In: Plant Biotechnology for Health. Springer, Cham

    Chapter  Google Scholar 

  • Bergenstråhle A, Borga P, Jonsson MV (1996) Sterol composition and synthesis in potato tuber discs in relation to glycoalkaloid synthesis. Phytochemistry 41:155–161

    Article  Google Scholar 

  • Bhatnagar P, Bhatnagar M, Nath AK, Sharma DR (2004) Production of solasodine by Solanum laciniatum using plant tissue culture technique. Ind J Exp Biol 42:1020–1023

    CAS  Google Scholar 

  • Cahill MG, Caprioli G, Vittori S, Jamesa KJ (2010) Elucidation of the mass fragmentation pathways of potato glycoalkaloids and aglycons using Orbitrap mass spectrometry. J Mass Spectrom 45:1019–1025

    Article  CAS  Google Scholar 

  • Cherkaoui S, Bekkouche K, Christen P, Veuthey JL (2001) Non-aqueous capillary electrophoresis with diode array and electrospray mass spectrometric detection for the analysis of selected steroidal alkaloids in plant extracts. J. Chromatogr. A 922:321–328

    Article  CAS  Google Scholar 

  • Dwivedi S, Alam A, Shekhawat GS (2016) Relative production and quantification of stevioside from in-vitro generated shoots, callus, suspension culture and synseeds of Stevia rebaudiana (Bertoni) Bertoni. Plant cell Biotechnol Mol Biol 17:155–166

    Google Scholar 

  • Eanes RC, Tek N, Kirsoy O, Frary A, Doganlar S, Almeida AE (2008) Development of practical HPLC methods for the separation and determination of eggplant steroidal glycoalkaloids and their aglycones. J Liq Chromatogr Relat Technol 31:984–1000

    Article  CAS  Google Scholar 

  • Gbadamosi IT, Afolayan AJ (2016) In vitro anti-radical activities of extracts of Solanum nigrum (L.) from South Africa. J Appl Biosci 98:9240–9251

    Article  Google Scholar 

  • Ginzberg I, Tokuhisa JG, Veilleux RE (2009) Potato steroidal glycoalkaloids: biosynthesis and genetic manipulation. Potato Res 52:1–15

    Article  CAS  Google Scholar 

  • Ginzberg I, Thippeswamy M, Fogelman E, Demirel U, Mweetwa AM, Tokuhisa J, Veilleux RE (2012) Induction of potato steroidal glycoalkaloid biosynthetic pathway by overexpression of cDNA encoding primary metabolism HMG-CoA reductase and squalene synthase. Planta 235:1341–1353

    Article  CAS  Google Scholar 

  • Jacob A, Malpathak N (2004) Green hairy root cultures of Solanum khasianum Clarke—a new route to in vitro solasodine production. Curr Sci 87:1442–1447

    CAS  Google Scholar 

  • Jacob A, Malpathak N (2005) Plantlet regeneration enhances solasodine productivity in hairy root cultures of Solanum khasianum Clarke. In Vitro Cell Dev Biol-Plant 41:291–295

    Article  CAS  Google Scholar 

  • Jayakumar K, Murugan K (2016) Solanum alkaloids and their pharmaceutical roles: a review. J Anal Pharm Res 3:75

    Google Scholar 

  • Khanna KR, Singh SP (1985) Harvesting Solanum viarum Dunal as a spineless crop. Sci culture 51:25

    Google Scholar 

  • Kittipongpatana N, Hock RS, Porter JR (1998) Production of solasodine by hairy root, callus and cell suspension cultures of Solanum aviculare Forst. Plant Cell Tiss Organ Cult 52:133–143

    Article  CAS  Google Scholar 

  • Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange BM (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6866–6871

    Article  CAS  Google Scholar 

  • Loc NH, Thanh LTH (2011) Solasodine production from cell culture of Solanum hainanense Hance. Biotech Bioprocess Eng 16:581–586

    Article  CAS  Google Scholar 

  • Maiti PC, Mookerjea S, Mathew R (1965) Solasodine from Solanum khasianum. J Pharm Sci 54:1828–1829

    Article  CAS  Google Scholar 

  • Mathur S, Shekhawat GS (2013) Establishment and characterization of Stevia rebaudiana (Bertoni) cell suspension culture: an in vitro approach for production of stevioside. Acta Physiol Plant 35:931–939

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum 15:473–497

    Article  CAS  Google Scholar 

  • Ohnishi T, Yokota T, Mizutani M (2009) Insights into the function and evolution of P450s in plant steroid metabolism. Phytochemistry 70:1918–1929

    Article  CAS  Google Scholar 

  • Padmashree A, Sharma GK, Semwal AD, Mahesh C (2014) Antioxygenic activity of Solanum nigrum L. leaves in sun flower oil model system and its thermal stability. Food Nutr Sci 5:1022–1029

    Google Scholar 

  • Pandey S, Goel R, Bhardwaj A, Asif MH, Sawant SV, Misra P (2018) Transcriptome analysis provides insight into prickle development and its link to defense and secondary metabolism in Solanum viarum Dunal. Sci Rep 8:17092

    Article  Google Scholar 

  • Patel K, Singh RB, Patel DK (2013) Medicinal significance, pharmacological activities, and analytical aspects of solasodine: a concise report of current scientific literature. J Acute Dis. 2:92–98

    Article  Google Scholar 

  • Prasad A, Mathur A, Singh M, Gupta MM, Uniyal GC, Lal RK, Mathur AK (2012) Growth and asiaticoside production in multiple shoot cultures of a medicinal herb, Centella asiatica (L.) Urban, under the influence of nutrient manipulations. J Nat Med 66(2):383–387

    Article  Google Scholar 

  • Putalun W (2011) Technology of compact MAb and its application for medicinal plant breeding named as missile type molecular breeding. Curr Drug Discov Technol 8:24–31

    Article  CAS  Google Scholar 

  • Singh RK, Chaudhary BD (1979) Biometrical methods in quantitative genetic analysis. Kalyani Publishers, New Delhi

    Google Scholar 

  • Singh S, Khanna K, Sudhir S (1998) Breeding of Solanum viarum: current status as steroid bearing plant. J Med Arom Plant Sci 20:423–431

    CAS  Google Scholar 

  • Srivastava M, Sharma S, Misra P (2016) Elicitation based enhancement of secondary metabolites in Rauwolfia serpentina and Solanum khasianum hairy root cultures. Phcog Mag 12:315–320

    Article  CAS  Google Scholar 

  • Sun Y, Zhao Y, Wang L, Lou H, Cheng A (2012) Cloning and expression analysis of squalene synthase, a key enzyme involved in antifungal steroidal glycoalkaloids biosynthesis from Solanum nigrum. Drug Discov Ther 6:242–248

    CAS  PubMed  Google Scholar 

  • Tambe NM (2013) Studies on in vitro callus culture of Solanum khasianum Clarke. Inter J Recent Trends Sci Technol 5:111–112

    Google Scholar 

  • Uddin A, Chaturvedi H (1979) Solasodine in somatic tissue cultures of Solanum khasianum. Planta Med 37:90–92

    Article  CAS  Google Scholar 

  • Umemoto N, Nakayasu M, Ohyama K, Yamashita MY, Mizutani M, Seki H, Saito K, Muranaka T (2016) Two cytochrome P450 monooxygenases catalyze early hydroxylation steps in the potato steroid glycoalkaloid biosynthetic pathway. Plant Physiol 171:2458–2467

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu XF, Shi HP, Tsang P, Keung E (2008) Induction and in vitro culture of hairy roots of Solanum nigrum L. var. pauciflorum Liou and its solasodine production. J Mol Cell Biol 41:183–191

    Google Scholar 

  • Wu JJ, Gao R, Shi Y, Tian WS (2015) Facile synthesis of solasodine based on a mild halogenation-ring opening reaction of spiroketals in steroidal sapogenins. Tetrahedron Lett 56:1215–1217

    Article  CAS  Google Scholar 

  • Zelezniak A, Sheridan S, Patil KR (2014) Contribution of network connectivity in determining the relationship between gene expression and metabolite concentration changes. PLOS Comput Biol 10:e1003572

    Article  Google Scholar 

  • Zha XM, Sun H, Hao J, Zhang Y (2007) Efficient synthesis of solasodine, O-acetylsolasodine, and soladulcidine as anticancer steroidal alkaloids. Chem Biodivers 4:25–31

    Article  CAS  Google Scholar 

  • Zhang GP, Shen SD, Lei M, Hu LH (2011) A facile and efficient method for the synthesis of solasodine from diosgenin. Tetrahedron 67:5894–5896

    Article  CAS  Google Scholar 

  • Zywicki B, Catchpole G, Draper J, Fiehn O (2005) Comparison of rapid liquid chromatography-electrospray ionization-tandem mass spectrometry methods for determination of glycoalkaloids in transgenic field-grown potatoes. Anal Biochem 336:178–186

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Director Council of Scientific and Industrial Research - NBRI, Lucknow for providing the necessary facilities. The senior author AP also acknowledges the award of NPDF with grant no. DST-PDF/2016/000922 to Science and Engineering Research Board, Department of Science and Technology, New Delhi (India).

Author information

Authors and Affiliations

  1. Department of Plant Biotechnology, Council of Scientific and Industrial Research-National Botanical Research Institute, Rana Pratap Marg, Lucknow, 226001, India

    Archana Prasad, Preeti Patel, Shatrujeet Pandey & Pratibha Misra

  2. Central Instrumentation Facility, Council of Scientific and Industrial Research - National Botanical Research Institute, Lucknow, 226001, India

    Abhishek Niranjan

Authors
  1. Archana Prasad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Preeti Patel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shatrujeet Pandey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abhishek Niranjan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pratibha Misra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pratibha Misra.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Peter Nick

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prasad, A., Patel, P., Pandey, S. et al. Growth and alkaloid production along with expression profiles of biosynthetic pathway genes in two contrasting morphotypes of prickly and prickleless Solanum viarum Dunal. Protoplasma 257, 561–572 (2020). https://doi.org/10.1007/s00709-019-01446-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-019-01446-3

Keywords

Search

Navigation