Advertisement

Experimental and Applied Acarology

, Volume 75, Issue 3, pp 319–331 | Cite as

Molecular mechanism of synthetic pyrethroid and organophosphate resistance in field isolates of Rhipicephalus microplus tick collected from a northern state of India

  • Gaurav Nagar
  • Anil Kumar Sharma
  • Sachin Kumar
  • B. C. Saravanan
  • Rajesh Kumar
  • Suman Gupta
  • Satyanshu Kumar
  • Srikant Ghosh
Article

Abstract

The frequently used chemical control method to manage Rhipicephalus microplus is limited by the emergence of resistance populations. Understanding of resistance mechanisms is essential to develop strategy for sustainable management. The present study was focused on working out the molecular mechanisms of resistance against synthetic pyrethroids (SPs) and organophosphates (OPs) in field isolates of R. microplus collected from six districts of Uttar Pradesh, India. Adult immersion test with discriminating concentrations (AIT-DC) was used to determine resistance status of isolates to SPs (deltamethrin, cypermethrin) and OPs (diazinon, coumaphos). All the six isolates were found resistant to SPs with resistance factor (RF) of 2.9–58.6 and to one of the OP compounds, diazinon having RF of 3.5–13.7 but susceptible to coumaphos (RF < 1.4). Three R. microplus genes, viz. para-sodium channel domain II S4-5 linker, carboxylesterase (372 bp) and acetylcholinesterase 2 (1692 bp) were sequenced and compared with respective sequences of reference susceptible IVRI-I, reference OP resistant population (IVRI-III), IVRI-IV and multi-acaricide resistant population (IVRI-V) of R. microplus. A C190A mutation in the domain II S4-5 linker region of sodium channel gene leading to L64I amino acid substitution was detected in all six isolates. The G1120A mutation in the carboxylesterase gene could not be detected in any isolate. Five nucleotide substitutions viz., G138A, G889A, T1090A, C1234T and G1403A were identified in the acetylcholinesterase 2 gene leading to four amino acid substitutions. The findings of the study corroborate the role of mutation in sodium channel and acetylcholinesterase 2 genes in SP and OP resistance in this part of India.

Keywords

Rhipicephalus microplus Resistance Sodium channel S4-5 linker Acetylcholinesterase 2 

Notes

Acknowledgements

The authors are grateful to the Indian Council of Agricultural Research, New Delhi for funding through the National Agricultural Science Fund, Project Nos. NASF/ABA-6015/2016-17/357 and NFBSFARA/BSA-4004/2013-14.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 19th Livestock Census (2012) All India ReportGoogle Scholar
  2. Ahanger RR, Godara R, Katoch R, Yadav A, Bhutyal ADS, Katoch M, Singh NK, Bader MA (2015) Deltamethrin resistance in field populations of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in Jammu and Kashmir, India. Exp Appl Acarol 67:467–475CrossRefPubMedGoogle Scholar
  3. Baffi MA, de Souza GRL, Vieira CU, de Sousa CS, Gourlatt LR, Bonetti AM (2007) Identification of point mutations in a putative carboxylesterase and their association with acaricide resistance in Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Vet Parasitol 148:301–309CrossRefPubMedGoogle Scholar
  4. Baffi MA, de Souza GRL, de Sousa CS, Ceron CR, Bonetti AM (2008) Esterase enzymes involved in pyrethroid and organophosphate resistance in a Brazilian population of Riphicephallus (Boophilus) microplus (Acari: Ixodidae). Mol Biochem Parasitol 160:70–73CrossRefPubMedGoogle Scholar
  5. Bandara KMUJ, Karunaratne SHPP (2017) Mechanisms of acaricide resistance in the cattle tick Rhipicephalus (Boophilus) microplus in Sri Lanka. Pest Biochem Physiol 139:68–72CrossRefGoogle Scholar
  6. Baxter GD, Barker SC (1998) Acetylcholinesterase cDNA of the cattle tick, Boophilus microplus: characterization and role in organophosphate resistance. Insect Biochem Mol Biol 28:581–589CrossRefPubMedGoogle Scholar
  7. Baxter GD, Barker SC (2002) Analysis of the sequence and expression of a second putative acetylcholinesterase cDNA from organophosphate–susceptible and organophosphate–resistant cattle ticks. Insect Biochem Mol Biol 32:815–820CrossRefPubMedGoogle Scholar
  8. Bendele KG, Guerrero FD, Miller RJ, Li AY, Barrero RA, Moolhuijzen PM, Black M, McCooke JK, Meyer J, Hill CA, Bellgard MI (2015) Acetylcholinesterase 1 in populations of organophosphate–resistant North American strains of the cattle tick, Rhipicephalus microplus (Acari: Ixodidae). Parasitol Res 114:3027–3040CrossRefPubMedGoogle Scholar
  9. Bhat SA, Singh NK, Singh H, Rath SS (2017) Molecular prevalence of Babesia bigemina in in Rhipicephalus microplus ticks infesting cross-bred cattle of Punjab, India. Parasite Epidemiol Control 2:85–90CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brun-Barale A, Bouvier JC, Pauron D, Bergé JB, Sauphanor B (2005) Involvement of a sodium channel mutation in pyrethroid resistance in Cydia pomonella L, and development of a diagnostic test. Pest Manag Sci 61:549–554CrossRefPubMedGoogle Scholar
  11. Chen AC, He H, Temeyer KB, Jones S, Green P, Barker SC (2009) A survey of Rhipicephalus microplus populations for mutation associated with pyrethroid resistance. J Econ Entomol 102:373–380CrossRefPubMedGoogle Scholar
  12. Chigure GM, Sharma AK, Kumar S, Fular A, Sagar SV, Nagar G, Upadhaya D, Saravanan BC, Kumar R, Ghosh S (2017) Role of metabolic enzymes in conferring resistance to synthetic pyrethroids, organophosphates and phenylpyrazole compounds in Rhipicephalus microplus. Int J Acarol.  https://doi.org/10.1080/01647954.2017.1400588 Google Scholar
  13. Domingues LN, Brasil BDSAF, de Paiva Bello ACP, da Cunha AP, Medeiros de Barros AT, Leite RC, Silaghi C, Pfister K, Friche Passos LM (2012) Survey of pyrethroid and organophosphate resistance in Brazilian field populations of Rhipicephalus (Boophilus) microplus: detection of C190A mutation in domain II of the paratype sodium channel gene. Vet Parasitol 189:327–332CrossRefGoogle Scholar
  14. Ghosh S, Kumar R, Nagar G, Kumar S, Sharma AK, Srivastava A, Kumar S, Ajith Kumar KG, Saravanan BC (2015) Survey of acaricides resistance status of Rhipiciphalus (Boophilus) microplus collected from selected places of Bihar, an eastern state of India. Ticks Tick Borne Dis 6:668–675CrossRefPubMedGoogle Scholar
  15. Ghosh S, Gupta S, Ajith Kumar KG, Sharma AK, Kumar S, Nagar G, Kumar R, Paul S, Fular A, Chigure G, Nandi A, Manjunathachar HV, Mohammad A, Verma MR, Saravanan BC, Ray DD (2017) Characterization and establishment of a reference deltamethrin and cypermethrin resistant tick line (IVRI-IV) of Rhipicephalus (Boophilus) microplus. Pestic Biochem Physiol 138:66–70CrossRefPubMedGoogle Scholar
  16. Guerrero FD, Leonore L, Martins JR (2012) Acaricide resistance mechanisms in Rhipicephalus (Boophilus) microplus. Rev Bra Parasitol Vet 21:1–6CrossRefGoogle Scholar
  17. Gupta S, Ajith Kumar KG, Sharma AK, Nagar G, Kumar S, Saravanan BC, Ravikumar G, Ghosh S (2016) Esterase mediated resistance in deltamethrin resistant reference tick colony of Rhipicephalus (Boophilus) microplus. Exp Appl Acarol 69:239–248CrossRefPubMedGoogle Scholar
  18. He H, Chen AC, Davey RB, Ivie GW, George JE (1999) Identification of a point mutation in the para–type sodium channel gene from a pyrethroid-resistant cattle tick. Biochem Biophys Res Commun 261:558–561CrossRefPubMedGoogle Scholar
  19. Hernandez R, He H, Chen AC, Ivy GW, George JE, Wagner GG (1999) Cloning and sequencing of a putative acetylcholinesterase from Boophilus microplus (Acari: Ixodidae). J Med Entomol 36:764–770CrossRefPubMedGoogle Scholar
  20. Hernandez R, He H, Chen AC, Waghela SD, Ivie GW, George JE, Wagner GG (2000) Identification of a point mutation in an esterase gene in different populations of the southern cattle tick, Boophilus microplus. Insect Biochem Mol Biol 30:969–977CrossRefPubMedGoogle Scholar
  21. Hernandez R, Guerrero FD, George JE, Wagner GG (2002) Allele frequency and gene expression of a putative carboxylesterase–encoding gene in a pyrethroid resistant strain of the tick, Boophilus microplus. Insect Biochem Mol Biol 32:1009–1016CrossRefPubMedGoogle Scholar
  22. Jamroz RC, Guerrero FD, Pruett JH, Oehler DD, Miller RJ (2000) Molecular and biochemical survey of acaricide resistance mechanisms in larvae from Mexican strains of the southern cattle tick, Boophilus microplus. J Insect Physiol 46:685–695CrossRefPubMedGoogle Scholar
  23. Jonsson NN, Cutullè C, Corley SW, Seddon JM (2010) Identification of a mutation in the para–sodium channel gene of the cattle tick Rhipicephalus microplus associated with resistance to flumethrin but not to cypermethrin. Int J Parasitol 40:1659–1664CrossRefPubMedGoogle Scholar
  24. Junquera P (2017) Coumaphos for veterinary use in cattle, sheep, goats, pig, horses, and dogs against external parasites: ticks, flies, fleas, lice, mites, fly maggots. http://parasitipedia.net/index.php?option=com_content&view=article&id=2487&Itemid=2756. Accessed Feb, 2017
  25. Jyoti Singh NK, Singh H, Rath SS (2014) Malathion resistance in Rhipicephalus (Boophilus) microplus from Ludhiana district, Punjab. J Parasit Dis 38:343–346CrossRefPubMedGoogle Scholar
  26. Klafke G, Webster A, Dall Agnol B, Pradel E, Silva J, de La Canal LH, Becker M, Osório MF, Mansson M, Barreto R, Scheffer R, Souza UA, Corassini VB, Dos Santos J, Reck J, Martins JR (2017) Multiple resistance to acaricides in field populations of Rhipicephalus microplus from Rio Grande do Sul state, Southern Brazil. Ticks Tick Borne Dis 8:73–80CrossRefPubMedGoogle Scholar
  27. Kumar S, Paul S, Sharma AK, Kumar R, Tewari SS, Chaudhuri P, Ray DD, Rawat AKS, Ghosh S (2011) Diazinon resistant status in Rhipicephalus (Boophilus) microplus collected from different agro–climatic regions of India. Vet Parasitol 181:274–281CrossRefPubMedGoogle Scholar
  28. Kumar R, Nagar G, Sharma AK, Kumar S, Ray DD, Chaudhuri P, Ghosh S (2013) Survey of pyrethroids resistance in Indian isolates of Rhipicephalus (Boophilus) microplus: identification of C190A mutation in the domain II of the para–sodium channel gene. Acta Trop 125:237–245CrossRefPubMedGoogle Scholar
  29. Kumar S, Sharma A, Ghosh S (2014) Determination of discriminating dose and evaluation of amitraz resistance status in different field isolates of Rhipicephalus (Boophilus) microplus in India. Exp Appl Acarol 63:413–422CrossRefPubMedGoogle Scholar
  30. Kumar S, Sharma AK, Nagar G, Ghosh S (2015) Determination and establishment of discriminating concentrations of malathion, coumaphos, fenvalerate and fipronil for monitoring acaricide resistance in ticks infesting animals. Ticks Tick Borne Dis 6:383–387CrossRefPubMedGoogle Scholar
  31. Kumar S, Sharma AK, Nagar G, Rawat SS, Tiwari SS, Kumar R, Dhakad ML, Sharma RK, Saxana RK, Mehraniya RS, Singh RS, Jain DK, Rai A, Ray DD, Ghosh S (2016) Characterization of acaricide resistance in tick isolates collected from Rajasthan, India. Indian J Anim Sci 86:14–23Google Scholar
  32. Li A, Davey RB, Miller RJ, George JE (2003) Resistance to coumaphos and diazinon in Boophilus microplus (Acari: Ixodidae) and evidence for the involvement of an oxidative detoxification mechanism. J Med Entomol 40:482–490CrossRefPubMedGoogle Scholar
  33. Lovis L, Guerrero FD, Miller RJ, Bodine DM, Bruno Betschart B, Sager H (2012) Distribution patterns of three sodium channel mutations associated with pyrethroid resistance in Rhipicephalus (Boophilus) microplus populations from North and South America, South Africa and Australia. Int J Parasitol Drugs Drug Resist 2:216–224CrossRefPubMedPubMedCentralGoogle Scholar
  34. Martinez-Torres D, Foster SP, Field LM, Devonshire AL, Williamson MS (1999) A sodium channel point mutation is associated with resistance to DDT and pyrethroid insecticides in the peach-potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Insect Mol Biol 8:339–346CrossRefPubMedGoogle Scholar
  35. Mendes MC, Pereira JR, Prado AP (2007) Sensitivity of Boophilus microplus (Acari: Ixodidae) to pyrethroids and organophosphate in farms in the Vale do Paraíba region, São Paulo, Brazil. Arq Inst Biol 74:81–85Google Scholar
  36. Minjauw B, McLeod A (2003) Research report, DFID Animal Health Programme, Centre for tropical Veterinary medicine, University of Edinburgh, UKGoogle Scholar
  37. Morgan JAT, Corley SW, Jackson LA, Lew-Tabor AE, Moolhuijzen PM, Jonsson NN (2009) Identification of point mutation in the para–sodium channel gene of the cattle Rhipicephalus (Boophilus) microplus associated with resistance to synthetic pyrethroids acaricides. Int J Parasitol 39:775–779CrossRefPubMedGoogle Scholar
  38. Petermann J, Cauquil L, Hurlin JC, Gaia H, Hue T (2016) Survey of cattle tick, Riphicephalus (Boophilus) microplus, resistance to amitraz and deltamethrin in New Caledonia. Vet Parasitol 217:64–70CrossRefPubMedGoogle Scholar
  39. Robbertse L, Baron S, van der Merwe NA, Madder M, Stoltsz WH, Maritz-Olivier C (2016) Genetic diversity, acaricide resistance status and evolutionary potential of a Rhipicephalus microplus population from a disease-controlled cattle farming area in South Africa. Ticks Tick Borne Dis 7:595–603CrossRefPubMedGoogle Scholar
  40. Rodriguez-Vivas RI, Hodgkinson JE, Rosado-Aguilar JA, Villegas-Perez SL, Trees AJ (2012) The prevalence of pyrethroid resistance phenotype and genotype in Rhipicephalus (Boophilus) microplus in Yucatan, Mexico. Vet Parasitol 184:221–229CrossRefPubMedGoogle Scholar
  41. Rodríguez-Vivas RI, Pérez-Cogollo LC, Rosado-Aguilar JA, Ojeda-Chi MM, Trinidad-Martinez I, Miller RJ, Li AY, de León AP, Guerrero F, Klafke G (2014) Rhipicephalus (Boophilus) microplus resistant to acaricides and ivermectin in cattle farms of Mexico. Rev Bra Parasitol Vet 23:113–122CrossRefGoogle Scholar
  42. Rosario-Cruz R, Guerrero FD, Miller RJ, Rodriguez-Vivas RI, Domínguez-García DI, Cornel AJ, Hernandez-Ortiz R, George JE (2005) Roles played by esterase activity and by a sodium channel mutation involved in pyrethroid resistance in populations of Boophilus microplus (Acari: Ixodidae) collected from Yucatan, Mexico. J Med Entomol 42:1020–1025CrossRefPubMedGoogle Scholar
  43. Rosario-Cruz R, Guerrero FD, Miller RJ, Rodriguez-Vivas RI, Tijerina M, Domínguez-Garcia DI (2009) Molecular survey of pyrethroid resistance mechanisms in Mexican field populations of Rhipicephalus (Boophilus) microplus. Parasitol Res 105:1145–1153CrossRefPubMedPubMedCentralGoogle Scholar
  44. Saldivar L, Guerrero FD, Miller RJ, Bendele KG, Gondro C, Brayton KA (2008) Microarray analysis of acaricide-inducible gene expression in the southern cattle tick, Rhipicephalus (Boophilus) microplus. Insect Mol Biol 17:597–606CrossRefPubMedGoogle Scholar
  45. Sharma AK, Kumar R, Kumar S, Nagar G, Singh NK, Rawat SS, Dhakadd ML, Rawat AKS, Ray DD, Ghosh S (2012) Deltamethrin and cypermethrin resistance status of Rhipicephalus (Boophilus) microplus collected from six agro-climatic regions of India. Vet Parasitol 188:337–345CrossRefPubMedGoogle Scholar
  46. Singh NK, Jyoti Haque M, Singh H, Rath SS, Ghosh S (2014) A comparative study on cypermethrin resistance in Rhipicephalus (Boophilus) microplus and Hyalomma anatolicum from Punjab (India). Ticks Tick Borne Dis 5:90–94CrossRefPubMedGoogle Scholar
  47. Singh A, Srivastava M, Shah HK, Gupta K, Tripathi AK, Chaudhary AK (2016) Mix infestation of trypanosomiasis and theileriosis in buffaloes. Vet Pract 17:260Google Scholar
  48. Stone NE, Olafson PU, Davey RB, Buckmeier G, Bodine D, Sidak-Loftis LC, Giles JR, Duhaime R, Miller RJ, Mosqueda J, Scoles GA, Wagner DM, Busch JD (2014) Multiple mutations in the para–sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico. Parasite Vectors 7:456Google Scholar
  49. Tan J, Liu Z, Tsai TD, Valles SM, Goldin AL, Dong K (2002) Novel sodium channel gene mutations in Blattella germanica reduce the sensitivity of expressed channels to deltamethrin. Insect Biochem Mol Biol 32:445–454CrossRefPubMedPubMedCentralGoogle Scholar
  50. Temeyer KB, Davey RB, Chen AC (2004) Identification of a third Boophilus microplus (Acari: Ixodidae) cDNA presumptively encoding an acetylcholinesterase. J Med Entomol 41:259–268CrossRefPubMedGoogle Scholar
  51. Temeyer KB, Olafson PU, Brake DK, Tuckow AP, Li AY, Pérez de León AA (2013a) Acetylcholinesterase of Rhipicephalus (Boophilus) microplus and Phlebotomus papatasi: gene identification, expression, and biochemical properties of recombinant proteins. Pest Biochem Physiol 106:118–123CrossRefGoogle Scholar
  52. Temeyer KB, Tuckow AP, Brake DK, Li AY, de León AAP (2013b) Acetylcholinesterases of blood-feeding ticks and flies. Chem Biol Interact 203:319–322CrossRefPubMedGoogle Scholar
  53. Vatsya S, Yadav CL (2011) Evaluation of acaricide resistance mechanisms in field populations of Rhipicephalus (Boophilus) microplus collected from India. Int J Acarol 37:405–410CrossRefGoogle Scholar
  54. Veiga LP, Souza AP, Bellato V, Sartor AA, Nunes AP, Cardoso HM (2012) Resistance to cypermethrin and amitraz in Rhipicephalus (Boophilus) microplus on the Santa Catarina Plateau, Brazil. Rev Bra Parasitol Vet 21:133–136CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Gaurav Nagar
    • 1
  • Anil Kumar Sharma
    • 1
  • Sachin Kumar
    • 1
  • B. C. Saravanan
    • 1
  • Rajesh Kumar
    • 2
  • Suman Gupta
    • 2
  • Satyanshu Kumar
    • 3
  • Srikant Ghosh
    • 1
  1. 1.Division of ParasitologyICAR-Indian Veterinary Research InstituteIzatnagar, BareillyIndia
  2. 2.Department of Agricultural ChemicalsICAR- Indian Agriculture Research Institute, PusaNew DelhiIndia
  3. 3.ICAR-Directorate of Medicinal and Aromatic Plants ResearchBoriavi, AnandIndia

Personalised recommendations