Skip to main content
Log in

Isolation of limonoid compound (Hamisonine) from endophytic fungi Penicillium oxalicum LA-1 (KX622790) of Limonia acidissima L. for its larvicidal efficacy against LF vector, Culex quinquefasciatus (Diptera: Culicidae)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Upon screening for novel and potential biocompounds with larvicidal activities, we successfully isolated hamisonine (HMSN) a limonoid compound from endophytic fungi Penicillium oxalicum LA-1 of Limonia acidissima. The extracted compound structure was elucidated by spectral studies such as UV-vis spectroscopy, thin-layer chromatography, FTIR, LC-ESI-MS, 1H NMR, and 13C NMR upon comparing with the spectral data available in the literature. Further, the isolated HMSN was tested against III and IV instar Culex quinquefasciatus larvae. The outcome of this study clearly emphasize that the extracted compound HMSN possesses a stupendous larvicidal activity in a dose-dependent manner with the LC50 and LC90 values of 1.779 and 7.685 ppm against III instar larvae and 3.031 and 28.498 ppm against IV instar larvae of C. quinquefasciatus, respectively. Interestingly, the histological studies evidently showing the damage of peritrophic membrane and epithelial cells of testing mosquito larvae.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Abutaha N, Mashaly AMA, Al-Mekhalfi FA, Muhammed F, Al-shami1 M,WadaanMA (2015) The larvicidal activity of endophytic fungal extract of Cochliobolus specifer on Aedes caspius and Culex pipiens (Diptera: Culicidae). Appl. Entomol. Zool 50:405–414

  • Ahmad J, Wizarat K, Shamsuddin KM, Zaman A, Connolly JD (1984) Jangomolide, a novel limonoid from Flacourtia jangomas. Phytochemistry 23(6):1269–1270

    Article  CAS  Google Scholar 

  • Al-Mehmadi RM, Al-Khalaf AA (2010) Larvicidal and histological effects of Melia azedarach extract on Culex quinquefasciatus Say larvae (Diptera: Culicidae). J King Saud Univ 22:77–85

    Article  Google Scholar 

  • Andrew P, BreksaIII DK, Rosalind Y (2008) Wong isolation and identification of the first C-17 limonin epimer, epilimonin. J Agric Food Chem 56(14):5595–5598

    Article  Google Scholar 

  • Asai T, Otsuki S, Sakurai H, Yamashita K, Ozeki T, Oshima Y (2013) Benzophenones from an endophytic fungus, Graphiopsis chlorocephala, from Paeonia lactiflora cultivated in the presence of an NAD+-dependent HDAC inhibitor. Org Lett 15(8):2058–2061

    Article  CAS  Google Scholar 

  • Attri BS, Prasad GR (1980) Neem oil extractives—an effective mosquito larvicide. Indian J. Entomol 42:371–374

    Google Scholar 

  • Banerjee S, Singha S, Laskar S, Chandra G (2011) Efficacy of Limonia acidissima L.(Rutaceae) leaf extract on larval immatures of Culex quinquefasciatus Say 1823. Asian Pac. J Trop Med 4(9):711–716

    Article  CAS  Google Scholar 

  • Barbara C, Michele L, Luisa P, Raffaele P, Ines O, Giovanni B (2013) Larvicidal and repellent activity of essential oils from wild and cultivated Ruta chalepensis L. (Rutaceae) against Aedes albopictus Skuse (Diptera: Culicidae), an arbovirus vector. Parasitol Res 112(3):991–999

    Article  Google Scholar 

  • Bayazit V, Konar V (2010) Biochemical and physiological evaluations of limonoids as potential cancer destroyers. J of Animal and Veterinary Advances 9(7):1099–1107

    Article  CAS  Google Scholar 

  • Bernhard L, Bernhard P, Magnusson P (2003) Management of patients with lymphedema caused by filariasis in north eastern Tanzania: alternative approaches. Physiol 89:743–749

    Google Scholar 

  • Chavan SR (1984) Chemistry of alkanes separated from leaves of Azadirachta indica and their larvicidal/insecticidal activity against mosquitoes. In: Schmutterer, H., Ascher, K.R.S. (Eds.), Natural pesticides from the neem tree and other tropical plants. Schriftenreihe der GTZ., No. 161. Eschborn, Germany, pp. 91–94

  • Chavan SR, Deshmukh PB, Renapurkar DM (1979) Investigations of indigenous plants for larvicidal activity. Bull Haffkine Inst 7:23–33

    Google Scholar 

  • Chen G, Zhu Y, Wang HZ, Wang SJ, Zhang RQ (2007) The metabolites of a mangrove endophytic fungus, Penicillium thomi. J Asian Nat Prod Res 9(2):159–164

    Article  Google Scholar 

  • Elimat TE, Raja HA, Graf TN, Faeth SH, Cech NB, Oberlies NH (2014) Flavonolignans from Aspergillus iizukae, a fungal endophyte of milk thistle (Silybum marianum). J Nat Prod 77(2):193–199

    Article  Google Scholar 

  • Elumalai D, Hemavathi M, Hemalatha P, Deepaa CV, Kaleena PK (2016) Larvicidal activity of catechin isolated from Leucas aspera against Aedes aegypti, Anopheles stephensi and Culexquinquefasciatus (Diptera: Culicidae). Parasitol Res 115:1203–1212

    Article  Google Scholar 

  • Hamouda LS, Elayassaki WM, Hamed MS (1996) Toxicity and histopathological effect of Artmisia judaic and Anagallis arvensis extracts on Culex pipiens larvae. J Egypt Ger Soc Zool 20:43–60

    Google Scholar 

  • Hancock PA, Sinkins SP, Godfray HCJ (2011) Strategies for introducing Wolbachia to reduce transmission of mosquito-borne diseases. PLOS Neglected Tropical Disease 5:e1024

    Article  Google Scholar 

  • Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79(3):293–320

    Article  Google Scholar 

  • Hooper PJ, Bradley MH, Biswas G, Ottesen EA (2009) The global programme to eliminate lymphatic filariasis: health impact during its first 8 years (2000–2007). Annals of Tropical Medicine & Parasitology 103:17–21

    Article  Google Scholar 

  • Joseph CC, Ndoile MM, Malima RC, Nkunya MHH (2004) Larvicidal and mosquitocidal extracts, a coumarin, isoflavonoids and pterocarpans from Neorautanenia mitis. Trans Royal Soc Trop Med Hyg 98:451–455

    Article  CAS  Google Scholar 

  • Koolen HH, Soares ER, Silva FM, Almeida RA, Souza AD, Medeiros LS, Rodrigues Filho E, Souza AQ (2012) An antimicrobial alkaloid and other metabolites produced by Penicillium sp. An endophytic fungus isolated from Mauritia flexuosa L. f. Química Nova 35(4):771–774

    Article  CAS  Google Scholar 

  • Kweka EJ, Zhou G, Munga S, Lee MC, Atieli HE, Nyindo M, Githeko AK, Yan G (2012) Anopheline larval habitats seasonality and species distribution: a prerequisite for effective targeted larval habitats control programmes. PLoS One 7:e52084

    Article  Google Scholar 

  • Li XJ, Zhang Q, Zhang AL, Gao JM (2012) Metabolites from Aspergillus fumigatus, an endophytic fungus associated with Melia azedarach, and their antifungal, antifeedant, and toxic activities. J Agric Food Chem 60(13):3424–3431

    Article  CAS  Google Scholar 

  • Liu JF, Chen WJ, Xin BR, Lu J (2014) Metabolites of the endophytic fungus Penicillium sp. FJ-1 of Acanthus ilicifolius. Nat Prod Commun 9(6):799–801

    CAS  Google Scholar 

  • Li JW, Duan RG, Zou JH, Chen RD, Chen XG, Dai JG (2014) Meroterpenoids and isoberkedienolactone from endophytic fungus Penicillium sp. associated with Dysosma versipellis. Yao xue xue bao=Acta pharmaceutica Sinica 49(6):913–920

    CAS  Google Scholar 

  • Li H, Qing C, Zhang Y, Zhao Z (2005) Screening for endophytic fungi with antitumour and antifungal activities from Chinese medicinal plants. World J Microbiol Biotechnol 21:1515–1519

    Article  Google Scholar 

  • Liu C, Liu J, Rong Y, Liang N, Rong L (2012) Aqueous extraction of limonin from Citrus reticulate Blanco. Czech J Food Sci 30(4):364–368

    CAS  Google Scholar 

  • MacLeod JK, Moeller PD, Bandara BR, Leslie Gunatilaka AA, Wijeratne EK (1989) Acidissimin, a new limonoid from Limonia acidissima. J Nat Prod 52(4):882–885

    Article  CAS  Google Scholar 

  • Murray NEA, Quam MB, Smith AW (2013) Epidemiology of dengue: past, present and future prospects. Clin Epidemiol 5:299–309

    Google Scholar 

  • Muthu C, Reegan AD, Kingsley S, Ignacimuthu S (2012) Larvicidal activity of pectolinaringenin from Clerodendrum phlomidis L. against Culex quinquefasciatus Say and Aedes aegypti L. (Diptera: Culicidae). Parasitol Res 111(3):1059–1065

    Article  Google Scholar 

  • Netala VR, Kotakadi VS, Gaddam SA, Ghosh SB, Tartte V (2016) Elicitation of gymnemic acid production in cell suspension cultures of Gymnema sylvestre R.Br. through endophytic fungi. Biotech 6(2):232

    Google Scholar 

  • Parthasarathy R, Sathiyabama M (2014) Gymnemagenin-producing endophytic fungus isolated from a medicinal plant Gymnema sylvestre R.Br. Appl Biochem Biotechnol 172:3141–3152

    Article  CAS  Google Scholar 

  • Peterson SW, Vega FE, Posada F, Nagai C (2005) Penicillium coffeae, a new endophytic species isolated from a coffee plant and its phylogenetic relationship to P. fellutanum, P. thiersii and P. brocae based on parsimony analysis of multilocus DNA sequences. Mycologia 97(3):659–666

  • Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315

    Article  CAS  Google Scholar 

  • Prabukumar S, Rajkuberan C, Ravindran K, Sivaramakrishnan S (2015) Isolation and characterization of endophytic fungi from medicinal plant Crescentia cujete L. and their antibacterial, antioxidant and anticancer properties. Int J Pharm Pharm Sci 7:316–321

    Google Scholar 

  • Prabukumar S, Sathishkumar G, Rajkuberan C, Gobinath C, Murugan K, Sivaramakrishnan S (2017) Isolation and characterization of anticancer flavone chrysin (5,7-dihydroxy flavone)-producing endophytic fungi from Passiflora incarnata L. leaves. Ann Microbiol 67:321

    Article  Google Scholar 

  • Pudhom K, Teerawatananond T (2014) Rhytidenones A-F, Spirobisnaphthalenes from Rhytidhysteron sp. AS21B, an endophytic fungus. J Nat Prod 77(8):1962–1966

    Article  CAS  Google Scholar 

  • Qiu M, Xie R, Shi Y, Chen H, Wen Y, Gao YS, Hu X (2010a) Isolation and identification of endophytic fungus SX01, a red pigment producer from Ginkgo biloba L. World J Microbiol Biotechnol 26:993–998

  • Qiu M, Xie RS, Shi Y, Zhang HH, Chen HM (2010b) Isolation and identification of two flavonoid-producing endophytic fungi from Ginkgo biloba L. Ann Microbiol 60:143–150

  • Reegan AD, Gandhi MR, Paulraj MG, Balakrishna K, Ignacimuthu S (2014) Effect of nilocitin, a protolimonoid isolated from Limonia acidissima L. (Diptera: Culicidae). Acta Trop 139:67–76

  • Roy A, Saraf S (2006) Limonoids: overview of significant bioactive triterpenes distributed in plants kingdom. Biol Pharm Bull 29(2):191–201

    Article  CAS  Google Scholar 

  • Mazid S, Kalita JC, Rajkhowa RC (2011) A review on the use of biopesticides in insect pest management. International Journal of Science and Advanced Technology 1:169–178

    Google Scholar 

  • Schulz B, Boyle C, Draeger S, Rommert AK (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004

    Article  CAS  Google Scholar 

  • Senthilkumar N, Varma P, Gurusubramanian G (2009) Larvicidal and adulticidal activities of some medicinal plants against the malarial vector, Anopheles stephensi (Liston). Parasitol Res 104:237–244

    Article  CAS  Google Scholar 

  • Senthil-Nathan S (2013) Physiological and biochemical effect of neem and otherMeliaceae plants secondary metabolites against Lepidopteran insects. Front Physiol 4:1–17

    Article  Google Scholar 

  • Shweta S, Zuehlke S, Ramesha BT, Priti V, Mohana Kumar P, Ravikanth G, Spiteller M, Vasudeva R, Shaanker UR (2010) Endophytic fungal strains of Fusarium solani, from Apodytes dimidiata E. Mey. ex Arn (Icacinaceae) produce camptothecin, 10-hydroxycamptothecin and 9-methoxycamptothecin. Phytochemistry 71:117–122

    Article  CAS  Google Scholar 

  • Siriwardane AM, Kumar NS, Jayasinghe L, Fujimoto Y (2015) Chemical investigation of metabolites produced by an endophytic Aspergillus sp. isolated from Limonia acidissima. Nat Prod Res 29(14):1384–1387

    Article  CAS  Google Scholar 

  • Singh D, Rathod V, Ninganagouda S, Hiremath J, Singh AK, Mathew J (2014) Optimization and characterization of silver nanoparticle by endophytic fungi Penicillium sp. isolated from Curcuma longa (turmeric) and application studies against MDR E. coli and S. aureus. Bioinorg Chem Appl 2014:1–8

    Google Scholar 

  • Sunish IP, Rajendran R, Mani TR, Munirathinam A, Dash AP, Tyagia BK (2007) Vector control complements mass drug administration against bancroftian filariasis in Tirukoilur, India. Bull World Health Organ 85(2):138–145

    Article  CAS  Google Scholar 

  • World Health Organization. (2014) A global brief on vector-borne diseases

  • Yu H, Zhang L, Li L, Zheng C, Guo L, Li W, Sun P, Qin L (2010) Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microbiol Res 165:437–449

    Article  CAS  Google Scholar 

  • Zhang P, Lia XM, Liu H, Lia X, Wang BG (2015) Two new alkaloids from Penicillium oxalicum EN-201, an endophytic fungus derived from the marine mangrove plant Rhizophora stylosa. Phytochem Lett 13:160–164

    Article  CAS  Google Scholar 

  • Zhao J, Zhou L, Wang J, Shan T, Zhong L, Liu X, Gao X (2010) Endophytic fungi for producing bioactive compounds originally from their host plants. Curr Res Technol Educ Trop Appl Microbiol Microb Biotechnol:567–576

Download references

Acknowledgement

The authors are thankful to University grants commission-Special Assistance Programme (UGCSAP), New Delhi, Govt. of India for financial assistance Ref: 3-27/2011 (SAP-11) Dt/March, 2011.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sivaramakrishnan Sivaperumal.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seetharaman, P., Gnanasekar, S., Chandrasekaran, R. et al. Isolation of limonoid compound (Hamisonine) from endophytic fungi Penicillium oxalicum LA-1 (KX622790) of Limonia acidissima L. for its larvicidal efficacy against LF vector, Culex quinquefasciatus (Diptera: Culicidae). Environ Sci Pollut Res 24, 21272–21282 (2017). https://doi.org/10.1007/s11356-017-9770-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-9770-2

Keywords

Navigation