Log in

Modulation of Picroside-I Biosynthesis in Grown Elicited Shoots of Picrorhiza kurroa In Vitro

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Elicitors are considered as biostimulants for growth improvement and enhancement of secondary metabolite content. To date, only seaweed extract (SWE) powder has been studied for its effect on picroside-I (P-I) production in in vitro grown Picrorhiza kurroa plants. However, little is known at the molecular level about P-I production in P. kurroa plants upon SWE treatment. Here, we investigated the relative effects of supplying different elicitors including methyl jasmonate (MeJa), sodium nitroprusside (SNP), and abscisic acid (ABA) with SWE on plant growth and P-I production in addition to their effects at the molecular level reflecting the metabolic status of P-I biosynthesis. Our results indicated that only SWE, ABA, and SNP stimulated P-I production by 2.60-, 2.01-, and 1.35-fold, respectively, whereas MeJa decreased P-I content. Interestingly, SWE modulated all four integrating secondary metabolic pathways, covering almost all critical steps in the methylerythritol phosphate (MEP), mevalonate (MVA), iridoid, and phenylpropanoid pathways to stimulate P-I biosynthesis. SNP targeted the MVA/MEP pathways in conjunction with the iridoid pathway, whereas ABA modulated the phenylpropanoid pathway to increase the P-I content in P. kurroa. This is apparently the first report on treatment of different elicitors in in vitro grown P. kurroa plants for eliciting P-I content and exploring the role of different elicitors at the molecular level.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Thailand)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bhandari P, Kumar N, Singh B, Kaul VK (2008) Simultaneous determination of sugars and picrosides in Picrorhiza kurroa species using ultrasonic extraction and high- performance liquid chromatography with evaporative light scattering detection. J Chromatogr 1194:257–261

    Article  CAS  Google Scholar 

  • Bhat WW, Dhar N, Razdan S, Rana S, Mehra R, Nargotra A, Dhar RS, Ashraf N, Vishwakarma R, Lattoo SK (2013) Molecular characterization of UGT94F2 and UGT86C4, two glycosyltransferases from Picrorhiza kurroa: comparative structural insight and evaluation of substrate recognition. PLoS ONE 8:e73804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhat WW, Razdan S, Rana S, Dhar N, Wani TA, Qazi P, Vishwakarma R, Lattoo SK (2014) A phenylalanine ammonia-lyase ortholog (PkPAL1) from Picrorhiza kurroa Royle ex. Benth: molecular cloning, promoter analysis and response to biotic and abiotic elicitors. Gene 547:245–256

    Article  CAS  PubMed  Google Scholar 

  • Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41

    Article  CAS  Google Scholar 

  • Craigie JS (2011) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393

    Article  CAS  Google Scholar 

  • du Jardin P (2015) Plant biostimulants: definition, concept, main categories and regulation. Sci Hortic 196:3–14

    Article  CAS  Google Scholar 

  • Fan D, Hodges DM, Critchley AT, Prithiviraj B (2013) A commercial extract of brown macroalga (Ascophyllum nodosum) affects yield and the nutritional quality of Spinach in vitro. Commun Soil Sci Plant Anal 44:1873–1884

    Article  CAS  Google Scholar 

  • Filippou P, Antoniou C, Yelamanchili S, Fotopoulos V (2012) NO loading: efficiency assessment of five commonly used application methods of sodium nitroprusside in Medicago truncatula plants. Plant Physiol Biochem 60:115–118

    Article  CAS  PubMed  Google Scholar 

  • Filippou P, Antoniou C, Fotopoulos V (2013) The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radic Biol Med 56:172–183

    Article  CAS  PubMed  Google Scholar 

  • Gahlan P, Singh HR, Shankar R, Sharma N, Kumari A, Chawla V, Ahuja PS, Kumar S (2012) De novo sequencing and characterization of Picrorhiza kurroa transcriptome at two temperatures showed major transcriptome adjustments. BMC Genomics 13:126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ganjewala D, Boba S, Raghavendra AS (2008) Sodium nitroprusside affects the level of anthocyanin and flavonol glycosides in pea (Pisum sativum L. cv. Arkel) leaves. Acta Biol Szeged 52:301–305

    Google Scholar 

  • Geu-Flores F, Sherden NH, Courdavault V, Burlat V, Glenn WS, Wu C, Nims E, Cui Y, O’Connor SE (2012) An alternative route to cyclic terpenes by reductive cyclization in iridoid biosynthesis. Nature 492:138–142

    Article  CAS  PubMed  Google Scholar 

  • Hurtado AQ, Joe M, Sanares RC, Fan D, Prithiviraj B, Critchley AT (2012) Investigation of the application of Acadian marine plant extract powder (AMPEP) to enhance the growth, phenolic content, free radical scavenging, and iron chelating activities of Kappaphycus Doty (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 24:601–611

    Article  CAS  Google Scholar 

  • Hussain MS, Fareed S, Ansari S, Rahman MA, Ahmad IZ, Saeed M (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 4:10–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ibrahim MH, Jaafar HZE (2013) Abscisic acid induced changes in production of primary and secondary metabolites, photosynthetic capacity, antioxidant capability, antioxidant enzymes and lipoxygenase inhibitory activity of Orthosiphon stamineus Benth. Molecules 18:7957–7976

    Article  CAS  PubMed  Google Scholar 

  • Jannin L, Arkoun M, Etienne P, Laıˆne´ P, Goux D, Garnica M, Fuentes M, Francisco SS, Baigorri R, Cruz F, Houdusse F, Garcia-Mina JM, Yvin JC, Ourry A (2013) Brassica napus growth is promoted by Ascophyllum nodosum (L.) Le Jol. seaweed extract: microarray analysis and physiological characterization of N, C, and S metabolisms. J Plant Growth Regul 32:31–52

    Article  CAS  Google Scholar 

  • Jiang Y, Joyce DC (2003) ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul 39:171–174

    Article  Google Scholar 

  • Kawoosa T, Singh H, Kumar A, Sharma SK, Devi K, Dutt S, Vats SK, Sharma M, Ahuja PS, Kumar S (2010) Light and temperature regulated terpene biosynthesis: hepatoprotective monoterpene picroside accumulation in Picrorhiza kurroa. Funct Integr Genomics 10:393–404

    Article  CAS  PubMed  Google Scholar 

  • Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM, Critchley AT, Craigie JS, Norrie P, Prithiviraj B (2009) Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 28:386–399

    Article  CAS  Google Scholar 

  • Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291

    Article  CAS  PubMed  Google Scholar 

  • Kumar V, Sood H, Sharma M, Chauhan RS (2013) A proposed biosynthetic pathway of picrosides linked through the detection of biochemical intermediates in the endangered medicinal herb Picrorhiza kurroa. Phytochem Anal 24:598–602

    Article  CAS  PubMed  Google Scholar 

  • Kumar V, Kumar V, Chauhan RS, Sood H, Tandon C (2015a) Cost effective quantification of picrosides in Picrorhiza kurroa by employing response surface methodology using HPLC-UV. J Plant Biochem Biotechnol 24:376–384

    Article  Google Scholar 

  • Kumar V, Sharma N, Shitiz K, Singh TR, Tandon C, Sood H, Chauhan RS (2015b) An insight into conflux of metabolic traffic leading to picroside-I biosynthesis by tracking molecular time course changes in a medicinal herb, Picrorhiza kurroa. Plant Cell Tissue Organ Cult 123:435–441

    Article  CAS  Google Scholar 

  • Kumar V, Shitiz K, Chauhan RS, Sood H, Tandon C (2015c) Tracking dynamics of enzyme activities and their gene expression in Picrorhiza kurroa with respect to picroside accumulation. J Plant Biochem Biotechnol. doi:10.1007/s13562-015-0317-7

    Google Scholar 

  • Lola-Luz T, Hennequart F, Gaffney M (2013) Enhancement of phenolic and flavonoid compounds in cabbage (Brassica oleraceae) following application of commercial seaweed extracts of the brown seaweed, (Ascophyllum nodosum). Agric Food Sci 22:288–295

    CAS  Google Scholar 

  • Miettinen K, Dong L, Navrot N, Schneider T, Burlat V, Pollier J, Woittiez L, van der Krol S, Lugan R, Ilc T, Verpoorte R, Oksman-Caldentey KM, Martinoia E, Bouwmeester H, Goossens A, Memelink J, Werck-Reichhart D (2014) The seco-iridoid pathway from Catharanthus roseus. Nat Commun 5:3606

    PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nayar MP, Sastri ARK (1990) Red data plants of India. CSIR Publication, New Delhi, p 271

    Google Scholar 

  • Pandit S, Shitiz K, Sood H, Chauhan RS (2013a) Differential biosynthesis and accumulation of picrosides in an endangered medicinal herb Picrorhiza kurroa. J Plant Biochem Biotechnol 22:335–342

    Article  CAS  Google Scholar 

  • Pandit S, Shitiz K, Sood H, Naik PK, Chauhan RS (2013b) Expression pattern of fifteen genes of non-mevalonate (MEP) and mevalonate (MVA) pathways in different tissues of endangered medicinal herb Picrorhiza kurroa with respect to picrosides content. Mol Biol Rep 40:1053–1063

    Article  CAS  PubMed  Google Scholar 

  • Panwar GS, Guru SK (2015) Stimulation of reserpine production in the whole plant culture of Rauwolfia serpentina L. by elicitors and precursor feeding. J Plant Biochem Biotechnol 24:49–55

    Article  CAS  Google Scholar 

  • Sah JN, Varshney VK (2013) Chemical constituents of Picrorhiza genus: a review. Am J Essent Oils Nat Prod 1:22–37

    Google Scholar 

  • Sharma N, Chauhan RS, Sood H (2015) Seaweed extract as a novel elicitor and medium for mass propagation and picroside-I production in an endangered medicinal herb Picrorhiza kurroa. Plant Cell Tissue Organ Cult 122:57–65

    Article  Google Scholar 

  • Sidiq T, Khajuria A, Suden P, Sharma R, Singh S, Suri KA, Satti NK, Johri RK (2010) Possible role of macrophages induced by an iridoid glycoside (RLJ-NE-299A) in host defense mechanism. Int Immunopharmacol 1:128–135

    Google Scholar 

  • Singh V, Banyal HS (2011) Antimalarial effects of Picrorhiza kurroa Royle Ex Benth extracts on Plasmodium berghei. Asian J Exp Biol Sci 2:529–532

    Google Scholar 

  • Singh H, Gahlan P, Kumar S (2013) Cloning and expression analysis of ten genes associated with picrosides biosynthesis in Picrorhiza kurroa. Gene 515:320–328

    Article  CAS  PubMed  Google Scholar 

  • Sood H, Chauhan RS (2009) High frequency callus induction and plantlet regeneration from different explants of Picrorhiza kurroa—a medicinal herb of Himalayas. Afr J Biotech 8:1965–1972

    CAS  Google Scholar 

  • Sood H, Chauhan RS (2010) Biosynthesis and accumulation of a medicinal compound, Picroside-I, in cultures of Picrorhiza kurroa Royle ex Benth. Plant Cell Tissue Organ Cult 100:113–117

    Article  CAS  Google Scholar 

  • Sung PH, Huang FC, Do YY, Huang PL (2011) Functional expression of geraniol 10-hydroxylase reveals its dual function in the biosynthesis of terpenoid and phenylpropanoid. J Agric Food Chem 59:4637–4643

    Article  CAS  PubMed  Google Scholar 

  • Wally OSD, Critchley AT, Hiltz D, Craigie JS, Han X, Zaharia LI, Abrams SR, Prithiviraj B (2013) Regulation of phytohormone biosynthesis and accumulation in Arabidopsis following treatment with commercial extract from the marine macroalga Ascophyllum nodosum. J Plant Growth Regul 32:324–339

    Article  CAS  Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotech Adv 23:283–333

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are thankful to the Jaypee University of Information Technology for providing the necessary research facilities and Department of Biotechnology, Ministry of Science and Technology, Govt. of India for providing research grant in the form of a programme support on high value medicinal plants to RSC and HS. We are also thankful to the Himalayan Forest Research Institute (HFRI), Manali, India for providing plant material of P. kurroa. The authors also gratefully acknowledge Sea6 Energy Pvt Ltd. for providing the seaweed extract powder.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hemant Sood.

Ethics declarations

Conflict of interest

The authors declare that they do not have any conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharma, N., Kumar, V., Chauhan, R.S. et al. Modulation of Picroside-I Biosynthesis in Grown Elicited Shoots of Picrorhiza kurroa In Vitro. J Plant Growth Regul 35, 965–973 (2016). https://doi.org/10.1007/s00344-016-9594-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-016-9594-1

Keywords

Navigation