- -

Functional characterization and fitness cost of spinosad-resistant alleles in Ceratitis capitata

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

Functional characterization and fitness cost of spinosad-resistant alleles in Ceratitis capitata

Mostrar el registro sencillo del ítem

Ficheros en el ítem

dc.contributor.author Guillem-Amat, Ana es_ES
dc.contributor.author Ureña, Enric es_ES
dc.contributor.author López-Errasquín, Elena es_ES
dc.contributor.author Navarro-Llopis, Vicente es_ES
dc.contributor.author Batterham, Philip es_ES
dc.contributor.author Sánchez, Lucas es_ES
dc.contributor.author Perry, Trent es_ES
dc.contributor.author Hernández-Crespo, Pedro es_ES
dc.contributor.author Ortego, Félix es_ES
dc.date.accessioned 2021-04-01T03:31:26Z
dc.date.available 2021-04-01T03:31:26Z
dc.date.issued 2020-06 es_ES
dc.identifier.issn 1612-4758 es_ES
dc.identifier.uri http://hdl.handle.net/10251/164816
dc.description.abstract [EN] The sustainability of control programs for the Mediterranean fruit fly, Ceratitis capitata, for citrus crops in Spain has been threatened by the development of resistance to malathion and lambda-cyhalothrin in recent years. Spinosad is widely used without apparent loss of efficacy. However, a highly resistant strain, JW-100s, has been obtained after laboratory selection. Spinosad resistance in JW-100s has been associated with different mutant alleles of the alpha 6 subunit of the nicotinic acetylcholine receptor (Cc alpha 6) including an isoform-specific truncation allele, Cc alpha 6(3aQ68*). Using the GAL4 > UAS system in Drosophila melanogaster to demonstrate expression of this truncated alpha 6 subunit, in a d alpha 6 loss-of-function genetic background, does not rescue susceptibility to spinosad, while the expression of Cc alpha 6 wild-type isoforms does. We have also generated C. capitata isolines from JW-100s homozygous for: (1) the Cc alpha 6(3aQ68*Delta 3b-4) allele, which contains the mutation 3aQ68*, and (2) the Cc alpha 6(3aQ68*-K352*) allele, which contains the mutations 3aQ68* and K352*. Neither of these produce complete Cc alpha 6 transcripts. The frequency of resistant alleles declined when in competition with individuals carrying the wild-type allele. Through extensive testing of both biological and behavioral fitness traits, we identified a reduced ability of Cc alpha 6(3aQ68*Delta 3b-4) males to detect the parapheromone and to mate with females carrying the Cc alpha 6(3aQ68*-K352*) allele in competition experiments. Thus, not only the potential for spontaneous resistant mutations to arise in Cc alpha 6 but also their fitness costs must be considered when planning resistance management strategies for C. capitata. es_ES
dc.description.sponsorship This work received financial support from CICYT (AGL2016-76516-R). The Spanish MINECO granted A. Guillem-Amat a predoc (BES-C-2014-068937) and a mobility (EEBB-I-16-11336) fellowships. We gratefully acknowledge Maria Torne (Dow Agro-Science Iberica) for providing technical grade spinosad, Charles Robin (University of Melbourne) for assisting with bureaucratic issues with the Australian Government, Tinna Yang (University of Melbourne) for the keeping and shipping of the flies and Sandra Vacas (Universitat Politecnica de Valencia) for the scientific advice on electroantennography. es_ES
dc.language Inglés es_ES
dc.publisher Springer-Verlag es_ES
dc.relation.ispartof Journal of Pest Science es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject Medfly es_ES
dc.subject NAChR es_ES
dc.subject GAL4 > UAS es_ES
dc.subject Fitness traits es_ES
dc.subject Behavior es_ES
dc.title Functional characterization and fitness cost of spinosad-resistant alleles in Ceratitis capitata es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1007/s10340-020-01205-x es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//AGL2016-76516-R/ES/HERRAMIENTAS PARA LA DETECCION Y EL MANEJO PROACTIVO DE LA RESISTENCIA MULTIPLE EN CERATITIS CAPITATA/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BES-2014-068937/ES/BES-2014-068937/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//EEBB-I-16-11336/ES/EEBB-I-16-11336/ es_ES
dc.rights.accessRights Abierto es_ES
dc.description.bibliographicCitation Guillem-Amat, A.; Ureña, E.; López-Errasquín, E.; Navarro-Llopis, V.; Batterham, P.; Sánchez, L.; Perry, T.... (2020). Functional characterization and fitness cost of spinosad-resistant alleles in Ceratitis capitata. Journal of Pest Science. 93(3):1043-1058. https://doi.org/10.1007/s10340-020-01205-x es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1007/s10340-020-01205-x es_ES
dc.description.upvformatpinicio 1043 es_ES
dc.description.upvformatpfin 1058 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 93 es_ES
dc.description.issue 3 es_ES
dc.relation.pasarela S\424322 es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.description.references Abbas N, Mansoor MM, Shad SA et al (2014) Fitness cost and realized heritability of resistance to spinosad in Chrysoperla carnea (Neuroptera: Chrysopidae). Bull Entomol Res 104:707–715. https://doi.org/10.1017/S0007485314000522 es_ES
dc.description.references Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267. https://doi.org/10.1093/jee/18.2.265a es_ES
dc.description.references Anstead CA, Korhonen PK, Young ND et al (2015) Lucilia cuprina genome unlocks parasitic fly biology to underpin future interventions. Nat Commun 6:1–11. https://doi.org/10.1038/ncomms8344 es_ES
dc.description.references Arouri R, Le Goff G, Hemden H et al (2015) Resistance to lambda-cyhalothrin in Spanish field populations of Ceratitis capitata and metabolic resistance mediated by P450 in a resistant strain. Pest Manag Sci 71:1281–1291. https://doi.org/10.1002/ps.3924 es_ES
dc.description.references Bao WX, Narai Y, Nakano A et al (2014) Spinosad resistance of melon thrips, Thrips palmi, is conferred by G275E mutation in α6 subunit of nicotinic acetylcholine receptor and cytochrome P450 detoxification. Pestic Biochem Physiol 112:51–55. https://doi.org/10.1016/j.pestbp.2014.04.013 es_ES
dc.description.references Baxter SW, Chen M, Dawson A et al (2010) Mis-spliced transcripts of nicotinic acetylcholine receptor α6 are associated with field evolved spinosad resistance in Plutella xylostella (L.). PLoS Genet. https://doi.org/10.1371/journal.pgen.1000802 es_ES
dc.description.references Berger M, Puinean AM, Randall E et al (2016) Insecticide resistance mediated by an exon skipping event. Mol Ecol 25:5692–5704. https://doi.org/10.1111/mec.13882 es_ES
dc.description.references Bielza P, Quinto V, Fernandez E et al (2007) Genetics of spinosad resistance in Frankliniella occidentalis (Thysanoptera: Thripidae). J Econ Entomol 100:916–920. https://doi.org/10.1603/0022-0493(2007)100%5b916:gosrif%5d2.0.co;2 es_ES
dc.description.references Bielza P, Quinto V, Gravalos C et al (2008a) Lack of fitness costs of insecticide resistance in the western flower thrips (Thysanoptera: Thripidae). J Econ Entomol. https://doi.org/10.1603/0022-0493(2008)101%5b499:lofcoi%5d2.0.co;2 es_ES
dc.description.references Bielza P, Quinto V, Grávalos C et al (2008b) Stability of spinosad resistance in Frankliniella occidentalis (Pergande) under laboratory conditions. Bull Entomol Res 98:355–359. https://doi.org/10.1017/S0007485308005658 es_ES
dc.description.references Bischof J, Maeda RK, Hediger M et al (2007) An optimized transgenesis system for Drosophila using germ-line-specific C31 integrases. Proc Natl Acad Sci 104:3312–3317. https://doi.org/10.1073/pnas.0611511104 es_ES
dc.description.references Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:289–295. https://doi.org/10.1101/lm.1331809 es_ES
dc.description.references Campos MR, Rodrigues ARS, Silva WM et al (2014) Spinosad and the tomato borer Tuta absoluta: a bioinsecticide, an invasive pest threat, and high insecticide resistance. PLoS ONE. https://doi.org/10.1371/journal.pone.0103235 es_ES
dc.description.references Cossé AA, Todd JL, Millar JG et al (1995) Electroantennographic and coupled gas chromatographic-electroantennographic responses of the mediterranean fruit fly, Ceratitis capitata, to male-produced volatiles and mango odor. J Chem Ecol 21:1823–1836 es_ES
dc.description.references Engebrecht J, Brent R, Kaderbhai MA (1991) Minipreps of plasmid DNA. Curr Protoc Mol Biol. https://doi.org/10.1002/0471142727.mb0106s15 es_ES
dc.description.references Fayyazuddin A, Zaheer MA, Hiesinger PR, Bellen HJ (2006) The nicotinic acetylcholine receptor Da7 is required for an escape behavior in Drosophila. PLoS Biol 4:0420–0431. https://doi.org/10.1371/journal.pbio.0040063 es_ES
dc.description.references Ferguson JS (2004) Development and stability of insecticide resistance in the leafminer Liriomyza trifolii (Diptera: Agromyzidae) to cyromazine, abamectin, and spinosad. J Econ Entomol 97:112–119. https://doi.org/10.1603/0022-0493-97.1.112 es_ES
dc.description.references Ffrench-Constant RH, Bass C (2017) Does resistance really carry a fitness cost? Curr Opin Insect Sci 21:39–46. https://doi.org/10.1016/j.cois.2017.04.011 es_ES
dc.description.references Geng C, Watson GB, Sparks TC (2013) Nicotinic acetylcholine receptors as spinosyn targets for insect pest management, 1st edn. Elsevier, Amsterdam es_ES
dc.description.references Hsu JC, Feng HT, Wu WJ et al (2012) Truncated transcripts of nicotinic acetylcholine subunit gene Bdα6 are associated with spinosad resistance in Bactrocera dorsalis. Insect Biochem Mol Biol 42:806–815. https://doi.org/10.1016/j.ibmb.2012.07.010 es_ES
dc.description.references IRAC (2019) Arthropod pesticide resistance database. https://www.pesticideresistance.org/index.php. Accessed 16 May 2019 es_ES
dc.description.references Jang EB, Light DM, Binder RG et al (1994) Attraction of female mediterranean fruit flies to the five major components of male-produced pheromone in a laboratory flight tunnel. J Chem Ecol 20:9–20. https://doi.org/10.1007/BF02065987 es_ES
dc.description.references Jin Y, Tian N, Cao J et al (2007) RNA editing and alternative splicing of the insect nAChR subunit alpha6 transcript: evolutionary conservation, divergence and regulation. BMC Evol Biol 7:1–12. https://doi.org/10.1186/1471-2148-7-98 es_ES
dc.description.references Jones AK, Raymond-Delpech V, Thany SH et al (2006) The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. Genome Res 16:1422–1430. https://doi.org/10.1101/gr.4549206 es_ES
dc.description.references Khan HAA, Akram W, Shad SA (2014) Genetics, cross-resistance and mechanism of resistance to spinosad in a field strain of Musca domestica L. (Diptera: Muscidae). Acta Trop 130:148–154. https://doi.org/10.1016/j.actatropica.2013.11.006 es_ES
dc.description.references Li ZM, Liu SS, Liu YQ, Ye GY (2007) Temperature-related fitness costs of resistance to spinosad in the diamondback moth, Plutella xylostella (Lepidoptera: Plutelidae). Bull Entomol Res 97:627–635. https://doi.org/10.1017/S0007485307005366 es_ES
dc.description.references Li X, Wan Y, Yuan G et al (2017) Fitness trade-off associated with spinosad resistance in Frankliniella occidentalis (Thysanoptera: Thripidae). J Econ Entomol 110:1755–1763. https://doi.org/10.1093/jee/tox122 es_ES
dc.description.references Magaña C, Hernandez-Crespo P, Ortego F, Castañera P (2007) Resistance to malathion in field populations of Ceratitis capitata. J Econ Entomol 100:1836–1843. https://doi.org/10.1603/0022-0493(2007)100%5b1836:rtmifp%5d2.0.co;2 es_ES
dc.description.references Magaña C, Hernández-Crespo P, Brun-Barale A et al (2008) Mechanisms of resistance to malathion in the medfly Ceratitis capitata. Insect Biochem Mol Biol 38:756–762. https://doi.org/10.1016/j.ibmb.2008.05.001 es_ES
dc.description.references MAPA (2019) Ministerio de Agricultura, Pesca y Alimentación. https://www.mapa.gob.es/es/. Accessed 12 Jun 2019 es_ES
dc.description.references Navarro-Llopis V, Primo J, Vacas S (2015) Bait station devices can improve mass trapping performance for the control of the Mediterranean fruit fly. Pest Manag Sci 71:923–927. https://doi.org/10.1002/ps.3864 es_ES
dc.description.references Okuma DM, Bernardi D, Horikoshi RJ et al (2018) Inheritance and fitness costs of Spodoptera frugiperda (Lepidoptera: Noctuidae) resistance to spinosad in Brazil. Pest Manag Sci 74:1441–1448. https://doi.org/10.1002/ps.4829 es_ES
dc.description.references Perry T, Batterham P (2018) Harnessing model organisms to study insecticide resistance. Curr Opin Insect Sci 27:61–67. https://doi.org/10.1016/j.cois.2018.03.005 es_ES
dc.description.references Perry T, McKenzie JA, Batterham P (2007) A D α6 knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad. Insect Biochem Mol Biol 37:184–188. https://doi.org/10.1016/j.ibmb.2006.11.009 es_ES
dc.description.references Perry T, Batterham P, Daborn PJ (2011) The biology of insecticidal activity and resistance. Insect Biochem Mol Biol 41:411–422. https://doi.org/10.1016/j.ibmb.2011.03.003 es_ES
dc.description.references Perry T, Somers J, Yang YT, Batterham P (2015) Expression of insect α6-like nicotinic acetylcholine receptors in Drosophila melanogaster highlights a high level of conservation of the receptor: spinosyn interaction. Insect Biochem Mol Biol 64:106–115. https://doi.org/10.1016/j.ibmb.2015.01.017 es_ES
dc.description.references Puinean AM, Lansdell SJ, Collins T et al (2013) A nicotinic acetylcholine receptor transmembrane point mutation (G275E) associated with resistance to spinosad in Frankliniella occidentalis. J Neurochem 124:590–601. https://doi.org/10.1111/jnc.12029 es_ES
dc.description.references Raymond M, Berticat C, Weill M et al (2001) Insecticide resistance in the mosquito Culex pipiens: what have we learned about adaptation? Genetica 112–113:287–296. https://doi.org/10.1023/A:1013300108134 es_ES
dc.description.references Reddy PVR, Rashmi MA (2016) Sterile insect technique (SIT) as a component of area-wide integrated management of fruit flies: status and scope. Pest Manag Hortic Ecosyst 22:1–11. https://doi.org/10.1097/01.ede.0000100289.82156.8b es_ES
dc.description.references Rehan A, Freed S (2014) Selection, mechanism, cross resistance and stability of spinosad resistance in Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Crop Prot 56:10–15. https://doi.org/10.1016/j.cropro.2013.10.013 es_ES
dc.description.references Rehan A, Freed S (2015) Fitness cost of methoxyfenozide and the effects of its sublethal doses on development, reproduction, and survival of spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Neotrop Entomol 44:513–520. https://doi.org/10.1007/s13744-015-0306-5 es_ES
dc.description.references Rinkevich FD, Scott JG (2009) Transcriptional diversity and allelic variation in nicotinic acetylcholine receptor subunits of the red flour beetle, Tribolium castaneum. Insect Mol Biol 18:233–242. https://doi.org/10.1111/j.1365-2583.2009.00873.x es_ES
dc.description.references Rinkevich FD, Chen M, Shelton AM, Scott JG (2010) Transcripts of the nicotinic acetylcholine receptor subunit gene Pxyla6 with premature stop codons are associated with spinosad resistance in diamondback moth, Plutella xylostella. Invertebr Neurosci 10:25–33. https://doi.org/10.1007/s10158-010-0102-1 es_ES
dc.description.references Robertson JL, Preisler HK (1992) Pesticide bioassays with arthropods. CRC Press, Boca Raton es_ES
dc.description.references Salgado VL, Sparks TC (2005) 6.5—the spinosyns: chemistry, biochemistry, mode of action, and resistance. In: Comprehensive molecular insect science. pp 137–173 es_ES
dc.description.references Sattelle DB, Jones AK, Sattelle BM et al (2005) Edit, cut and paste in the nicotinic acetylcholine receptor gene family of Drosophila melanogaster. BioEssays 27:366–376. https://doi.org/10.1002/bies.20207 es_ES
dc.description.references Sayyed AH, Saeed S, Noor-Ul-Ane M, Crickmore N (2008) Genetic, biochemical, and physiological characterization of spinosad resistance in Plutella xylostella (Lepidoptera: Plutellidae). J Econ Entomol 101:1658–1666. https://doi.org/10.1603/0022-0493 es_ES
dc.description.references Shao YM, Dong K, Zhang CX (2007) The nicotinic acetylcholine receptor gene family of the silkworm, Bombyx mori. BMC Genom 8:1–10. https://doi.org/10.1186/1471-2164-8-324 es_ES
dc.description.references Shi M, Yue Z, Kuryatov A et al (2014) Identification of redeye, a new sleep-regulating protein whose expression is modulated by sleep amount. Elife 2014:1–17. https://doi.org/10.7554/eLife.01473 es_ES
dc.description.references Silva WM, Berger M, Bass C et al (2016) Mutation (G275E) of the nicotinic acetylcholine receptor α6 subunit is associated with high levels of resistance to spinosyns in Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Pestic Biochem Physiol 131:1–8. https://doi.org/10.1016/j.pestbp.2016.02.006 es_ES
dc.description.references Somers J, Nguyen J, Lumb C et al (2015) In vivo functional analysis of the Drosophila melanogaster nicotinic acetylcholine receptor Dα6 using the insecticide spinosad. Insect Biochem Mol Biol 64:116–127. https://doi.org/10.1016/j.ibmb.2015.01.018 es_ES
dc.description.references Somers J, Luong HNB, Batterham P, Perry T (2017) Deletion of the nicotinic acetylcholine receptor subunit gene Dα1 confers insecticide resistance, but at what cost? Fly (Austin) 12:46–54. https://doi.org/10.1080/19336934.2017.1396399 es_ES
dc.description.references Ureña E, Guillem-Amat A, Couso-Ferrer F et al (2019) Multiple mutations in the nicotinic acetylcholine receptor Ccα6 gene associated with resistance to spinosad in medfly. Sci Rep 9:2961. https://doi.org/10.1038/s41598-019-38681-w es_ES
dc.description.references Vontas J, Hernández-Crespo P, Margaritopoulos JT et al (2011) Insecticide resistance in Tephritid flies. Pestic Biochem Physiol 100:199–205. https://doi.org/10.1016/j.pestbp.2011.04.004 es_ES
dc.description.references Wang D, Qiu X, Wang H et al (2010) Reduced fitness associated with spinosad resistance in Helicoverpa armigera. Phytoparasitica 38:103–110. https://doi.org/10.1007/s12600-009-0077-9 es_ES
dc.description.references Wang J, Wang X, Lansdell SJ et al (2016) A three amino acid deletion in the transmembrane domain of the nicotinic acetylcholine receptor α6 subunit confers high-level resistance to spinosad in Plutella xylostella. Insect Biochem Mol Biol 71:29–36. https://doi.org/10.1016/j.ibmb.2016.02.001 es_ES
dc.description.references Watson GB, Chouinard SW, Cook KR et al (2010) A spinosyn-sensitive Drosophila melanogaster nicotinic acetylcholine receptor identified through chemically induced target site resistance, resistance gene identification, and heterologous expression. Insect Biochem Mol Biol 40:376–384. https://doi.org/10.1016/j.ibmb.2009.11.004 es_ES
dc.description.references Wu M, Robinson JE, Joiner WJ (2014) SLEEPLESS is a bifunctional regulator of excitability and cholinergic synaptic transmission. Curr Biol 24:621–629. https://doi.org/10.1016/j.cub.2014.02.026 es_ES
dc.description.references Wyss CF, Young HP, Shukla J, Roe RM (2003) Biology and genetics of a laboratory strain of the tobacco budworm, Heliothis virescens (Lepidoptera: Noctuidae), highly resistant to spinosad. Crop Prot 22:307–314. https://doi.org/10.1016/S0261-2194(02)00153-9 es_ES
dc.subject.ods 08.- Fomentar el crecimiento económico sostenido, inclusivo y sostenible, el empleo pleno y productivo, y el trabajo decente para todos es_ES
dc.subject.ods 15.- Proteger, restaurar y promover la utilización sostenible de los ecosistemas terrestres, gestionar de manera sostenible los bosques, combatir la desertificación y detener y revertir la degradación de la tierra, y frenar la pérdida de diversidad biológica es_ES


Este ítem aparece en la(s) siguiente(s) colección(ones)

Mostrar el registro sencillo del ítem