Evlution of Folir Dmge y Spodopter frugiperd (Lepidopter: Notuide) to Genetilly Modified Corn (Poles: Poee) in Mexio Author(s): Luis A. Aguirre, Agustín Hernández-Juàrez, Mrino Flores, Ernesto Cern, Jerónimo Lnderos, Gustvo A. Frís nd Mrvin K. Hrris Soure: Florid Entomologist, 99(2):276-280. Pulished By: Florid Entomologil Soiety https://doi.org/10.1653/024.099.0218 URL: http://www.ioone.org/doi/full/10.1653/024.099.0218 BioOne (www.ioone.org) is nonprofit, online ggregtion of ore reserh in the iologil, eologil, nd environmentl sienes. BioOne provides sustinle online pltform for over 170 journls nd ooks pulished y nonprofit soieties, ssoitions, museums, institutions, nd presses. Your use of this PDF, the BioOne We site, nd ll posted nd ssoited ontent indites your eptne of BioOne s Terms of Use, ville t www.ioone.org/pge/terms_of_use. Usge of BioOne ontent is stritly limited to personl, edutionl, nd non-ommeril use. Commeril inquiries or rights nd permissions requests should e direted to the individul pulisher s opyright holder. BioOne sees sustinle sholrly pulishing s n inherently ollortive enterprise onneting uthors, nonprofit pulishers, demi institutions, reserh lirries, nd reserh funders in the ommon gol of mximizing ess to ritil reserh.
Evlution of folir dmge y Spodopter frugiperd (Lepidopter: Notuide) to genetilly modified orn (Poles: Poee) in Mexio Luis A. Aguirre 1, *, Agustín Hernández-Juàrez 1, Mrino Flores 1, Ernesto Cern 1, Jerónimo Lnderos 1, Gustvo A. Frís 1, nd Mrvin K. Hrris 2 Astrt The fll rmyworm, Spodopter frugiperd Smith & Aot (Lepidopter: Notuide), is key pest of orn, Ze mys L. (Poles: Poee), in Mexio. The development of genetilly modified (GM) orn hyrids for resistne to this inset, with the inlusion of severl genes oding for proteins Cry1A, Vip3A20, nd mcry3a of Billus thuringiensis Berliner (Billles: Billee) (Bt), offer n lterntive to onventionl insetiides to ontrol this pest. Resistne to fll rmyworms of the GM orn hyrids Agrisure3000 GT, Agrisure Vipter3110, nd Agrisure Vipter3111 ws evluted in 4 lotions t Sinlo for 3 yr period. Dmge evlution showed tht the mize hyrids with the Bt gene insertion were not ffeted y the fll rmyworm s ompred with their respetive isolines, whih were seriously dmged. The results reffirm the inset ontrol enefits provided y this tehnology nd provide seline for resistne mngement. Key Words: Billus thuringiensis; δ-endotoxin; fll rmyworm; lef dmge Resumen El gusno ogollero Spodopter frugiperd Smith & Aot (Lepidopter: Notuide), es l plg de myor importni eonómi del míz Ze mys L. (Poles: Poee) en Méxio. El desrrollo de híridos de míz genétimente modifidos pr resisteni este inseto, on l inserión de diversos genes que odifin pr ls proteíns Cry1A, Vip3A20 y mcry3a de Billus thuringiensis Berliner (Billles: Billee) (Bt), ofreen un lterntiv los insetiids onvenionles de ontrol de est plg. Se evluó durnte tres ños, el dño folir del gusno ogollero en míz GM on los híridos Agrisure 3000 GT, Agrisure Vipter 3110 y Agrisure Vipter 3111 en utro loliddes del estdo de Sinlo. L evluión del dño demostró que el míz on l inserión de genes de Bt son efies pr ontrrrestr o no ser fetdo por el dño provodo por l plg, en omprión on sus respetivs línes onvenionles que fueron serimente dñds. Los resultdos refirmn los enefiios del ontrol de insetos que ofree est tenologí y proporion un líne se pr el mnejo de l resisteni. Plrs Clve: Billus thuringiensis; δ-endotoxin; gusno ogollero; dño folir The fll rmyworm, Spodopter frugiperd Smith & Aot (Lepidopter: Notuide), is indigenous to the Amerin ontinent (Sen et l. 2003) nd hs een reported to infest 186 host plnt speies in North nd Centrl Ameri (Csmuz et l. 2010). Corn, Ze mys L. (Poles: Poee), is the primry host of eonomi importne wherever it is grown in Mexio (Sen et l. 2003). Tropil nd sutropil res re most seriously ffeted (Orteg 1987; Rodríguez & Mrín 2008) with losses inurred from post-emergene to mturity (Orteg 1987). Yield losses over 30% re ommon (Herrer 1979; Grí-Gutiérrez et l. 2012), nd in some ses totl rop loss ours (Silv-Aguyo et l. 2010). A reline on hemil ontrol to mnge pest popultions hs eome inresingly ineffetive s S. frugiperd now expresses resistne to severl toxiologil groups of insetiides (Georghiou & Mellon 1983; Yu 1991; Pheo-Covrruis 1993; Morillo & Notz 2001; Yu et l. 2003). The development of new ontrol tehniques led to the elortion of genetilly modified orn hyrids expressing Billus thuringiensis Berliner (Billles: Billee) (Bt) rystl protein tht, when onsumed y lepidopterous lrve, proved ftl to the Europen orn orer, Ostrini nuillis Hüner (Lepidopter: Crmide), the southwestern orn orer, Ditre grndiosell Dyr (Lepidopter: Crmide), the sugrne orer, Ditre shrlis (F.) (Lepidopter: Crmide), the orn erworm, Helioverp ze Boddie (Lepidopter: Notuide), nd S. frugiperd (Ael et l. 2000; Cstro et l. 2004). A pyrmided strtegy tht omines 2 or more Bt genes deployed in the sme orn plnt is now used to onserve insetiidl effiy (Burkness et l. 2010; Niu et l. 2013; Yng et l. 2013). Genetilly modified orn (GM) hyrids with Bt genes hve lso een developed to resist wider rnge of pests within Lepidopter nd Coleopter (Buntin et l. 2004,; Buntin 2008; Dun et l. 2008; Hrdke et l. 2011). These hyrids support 1 Universidd Autónom Agrri Antonio Nrro, Deprtmento de Prsitologí, Clzd Antonio Nrro 1923, Buenvist, Sltillo, Cohuil, 25315, Méxio 2 Texs A&M University, Deprtment of Entomology, College Sttion, Texs 77843, USA *Corresponding uthor; E-mil: luisguirreu@yhoo.om.mx 276 2016 Florid Entomologist Volume 99, No. 2
Aguirre et l.: Lef dmge y Spodopter frugiperd in Bt orn 277 pest mngement strtegy in modern griulture (Fernndes et l. 2007), lthough onerns from n eonomi, sientifi, nd soil stndpoint remin in Mexio. Mexio is the enter of origin of over 61 ntive res of orn (Reyes 1990; Mtsuok 2005; CONABIO 2006; Kto et l. 2009), nd there is onern tht GM orn ould jeoprdize those res (Kto-Ymkke 2004; Serrtos-Hernández et l. 2004; Turrent et l. 2010); however, Bltzr et l. (2015) suggest tht mesures suh s sptil isoltion ould minimize ontmintion risks. More informtion is needed in Mexio to vlidte if the Bt Cry proteins of GM orn re effetive in ontrolling the rop pests under vrious environmentl onditions eyond those reported y Aguirre et l. (2015) to ontrol orn erworm in the stte of Sinlo nd y Aguirre et l. (2015) to ontrol S. frugiperd in the stte of Tmulips. Thus, the ojetive of this study ws to evlute folir dmge in orn hyrids with Cry1A, Vip3A20, nd mcry3a toxins from B. thuringiensis to ontrol S. frugiperd lrve in Sinlo, Mexio, during 3 growing sesons. Mterils nd Methods Reserh ws onduted t Oso Viejo, El Dordo, nd Cmlote in the ity of Culin nd the ity of Nvolto, oth in the stte of Sinlo, during the 2011 2013 fll winter growing sesons. Plots were plnted under iosfety onditions, isolted t lest 500 m from ommeril orn plots nd plnted t lest 21 d lter thn reommended to void ross-pollintion with non-gm hyrids in ordne with government regultions for field tests with GM orn (Hlsey et l. 2005; LBOGM 2005). Three Bt orn hyrids (Agrisure TM 3000 GT with Cry1A nd mcry3a proteins; Agrisure Vipter TM 3111 with Cry1A, Vip3A20, nd mcry3a; nd Agrisure Vipter TM 3110 with Cry1A nd Vip3A20) were used in this reserh nd ompred with their respetive non-gm isolines provided y Syngent Agro S.A de C.V. de Méxio (Sn Lorenzo 1009, Primer Piso, Coloni Del Vlle, 03100, Méxio, D.F.). The first two hyrids re resistnt to Lepidopter nd Coleopter nd the lst one is resistnt to Lepidopter. A rndomized omplete lok design ws used in eh lolity nd dte. In 2011, Agrisure 3000 GT nd Agrisure Vipter 3110, plus their isolines, were plnted t Oso Viejo. In ddition, eh vriety hd orresponding tretment tht inluded folir insetiide ontrol (see Tle 1). There were 4 replite loks per tretment, nd they were plnted on 28 Jn. In 2012, Agrisure Vipter 3111 nd Agrisure 3000 GT hyrids, with nd without insetiide tretments, were plnted on 15 Fe t Nvolto. Agrisure Vipter 3111 ws plnted t El Dordo on 19 Fe, lso with nd without insetiide pplitions (see Tle 1). Only 3 replites were plnted in these res. In 2013, Agrisure Vipter 3111 ws plnted t Cmlote nd Oso Viejo on 14 nd 15 Mrh, respetively, with 3 tretments (GM hyrid, isoline, isoline plus insetiide) nd 4 replites (see Tle 1). In ddition, experimentl plots during the 3 yr period reeived n insetiide tretment for S. frugiperd if plnts less thn 20 m tll rehed 10% infesttion level, or plnts 20 Tle 1. Insetiide tretments used to evlute lef dmge y fll rmyworms in genetilly modified (GM) orn during 2011 2013 fll winter growing sesons in lolities of Culin nd Nvolto, Sinlo, Mexio. Yer Hyrid Lolity Insetiide, 2011 Agrisure 3000 GT Oso Viejo without insetiide pplition Agrisure 3000 GT + i Oso Viejo permethrin lmd yhlothrin emmetin enzote Isoline + i Oso Viejo permethrin lmd yhlothrin emmetin enzote Isoline Oso Viejo hek Agrisure Vipter 3110 Oso Viejo without insetiide pplition Agrisure Vipter 3110 + i Oso Viejo permethrin lmd yhlothrin emmetin enzote Isoline + i Oso Viejo permethrin lmd yhlothrin emmetin enzote Isoline Oso Viejo hek 2012 Agrisure Vipter 3111 El Dordo without insetiide pplition Agrisure Vipter 3111+ i El Dordo permethrin lmd yhlothrin emmetin enzote Isoline + i El Dordo permethrin lmd yhlothrin emmetin enzote Isoline El Dordo hek Agrisure Vipter 3111 Nvolto without insetiide pplition Agrisure Vipter 3111 + i Nvolto permethrin lmd yhlothrin emmetin enzote Isoline + i Nvolto permethrin lmd yhlothrin emmetin enzote Isoline Nvolto hek Agrisure3000 GT Nvolto without insetiide pplition Agrisure 3000 GT + i Nvolto permethrin lmd yhlothrin emmetin enzote Isoline + i Nvolto permethrin lmd yhlothrin emmetin enzote Isoline Nvolto hek 2013 Agrisure Vipter 3111 Cmlote without insetiide pplition Isoline + i Cmlote emmetin enzote Isoline Cmlote hek Agrisure Vipter 3111 Oso Viejo without insetiide pplition Isoline + i Oso Viejo emmetin enzote Isoline Oso Viejo hek i = insetiide ontrol hek = isoline without insetiide pplition Insetiides were pplied t the following rtes: permethrin, 400 ml/h; lmd yhlothrin, 500 ml/h; emmetin enzote, 200 ml/h.
278 2016 Florid Entomologist Volume 99, No. 2 m or tller rehed 20% infesttion level, t the rte of 2 pplitions per yer (Tle 1). Eh experimentl plot onsisted of 10 rows, eh 5 m long, with 0.8 m etween rows with 40 to 50 seed plnting density. The seedlings were lter thinned to 34 plnts per row. The experimentl plot ws surrounded with uffer re of 6 rows of onventionl orn, nd other uffer res were plnted etween replites, whih were plnted the sme time s the experimentl mteril s required y offiil regultions. Agriulturl mngement of the plot followed the tehnil guide for orn growers developed y the Instituto Nionl de Investigiones Forestles, Agríols y Peuris (INIFAP 2010). Folir dmge under nturl infesttion y fll rmyworms ws evluted y smpling 10 plnts rndomly in the 4 entrl rows t V6 V8 (2011), nd V2 V4, V6 V8, nd V10 V12 (2012 nd 2013) phenologil stges of the plnt. A numeril sle (1 9), lso known s the Dvis sle, ws used to evlute folir feeding dmge (Dvis et l. 1989, 1992; Mihm 1983) rnging from 1 = no folir dmge (highly resistnt) to 9 = severe folir dmge (totlly suseptile). PROC ANOVA nd Tukey s multiple rnk test (P < 0.05) were used to ompre mong tretments. SAS/STAT (SAS version 9.0; SAS Institute, Cry, North Crolin) softwre ws used to nlyze the perentge of injury to plnts injured nd the dmge rtings (Dvis sle). Results Genetilly modified hyrids t Oso Viejo in 2011 did not show signifint (P > 0.05) dmge y fll rmyworms. The isolines with insetiide tretment lso hd low dmge sores, 1.85 nd 1.22 (Dvis sle) for Agrisure 3000 GT nd Agrisure Vipter 3110, respetively, with only some pinhole feeding mrks on leves nd no signifint differenes etween tretments (P > 0.05). In ontrst, isolines without hemil tretment hd n verge of dmge sore of 4.20 in oth hyrids, whih possessed lrge holes nd long lesions on leves. Spodopter frugiperd did not dmge Agrisure Vipter 3110 nd Agrisure 3000 GT with insetiide tretment, nd 5.0% of plnts were dmged in the ltter without tretment. The non-gm hyrids displyed dmged plnts from 15.0 to 90.0%, inluding those in whih hemil ontrol ws used (Tle 2). At El Dordo nd Nvolto in 2012, results were similr to those in 2011. Agrisure Vipter 3111 nd Agrisure 3000 GT, inluding those with Tle 2. Folir dmge nd perentge of plnts injured y fll rmyworms on the genetilly modified hyrids Agrisure 3000 GT nd Agrisure Vipter 3110 nd their respetive isolines t Oso Viejo, Culin, Sinlo, in 2011. Hyrid Lef dmge, Plnts injured (%) Agrisure 3000 GT 1.10 5.0 Agrisure 3000 GT + i 1.00 0.0 Isoline + i 1.85 30.0 Isoline 4.20 82.5 F = 17.33*** F = 38.58*** Agrisure Vipter 3110 1.00 0.0 Agrisure Vipter 3110 + i 1.00 0.0 Isoline + i 1.22 15.0 Isoline 4.20 90.0 F = 13.22*** F = 297.00*** i = insetiide ontrol Men numeril sle Genetilly modified hyrids nd their respetive isolines followed y the sme letter do not differ signifintly (ANOVA nd Tukey s test; P > 0.05). *** Indites signifint F vlue t P < 0.001, df = 3,15. insetiide tretment, showed little folir dmge (<1.4 on the Dvis sle) nd few injured plnts, with some plnts with pinholes nd only 13.3% of plnts injured in the Agrisure 3000 GT tretment. The isolines of the GM hyrids were signifintly different, with 52.2 to 81.1% of plnts injured nd plnt dmge tht vried from 2.89 to 4.97 on the Dvis sle, inluding lrge holes nd long lef lesions (Tle 3). In 2013, Agrisure Vipter 3111 did not show feeding signs y S. frugiperd t ny of the test sites, wheres the isolines were hevily infested inluding those in whih hemil ontrol ws pplied. Folir injury ws 1.72 to 3.22 on the Dvis sle nd 35.8 to 74.2% of plnts injured, inluding lrge lesions (Tle 4). Disussion Agrisure3000 GT, Agrisure Vipter 3110, nd Agrisure Vipter 3111 hyrids were resistnt to S. frugiperd s ompred with their severely injured respetive isolines during the 3 yr reserh study in the Sinlo orn-growing res. These results re similr to those found y Aguirre et l. (2015), testing the sme Bt hyrids in the stte of Tmulips. Also, Piñ & Solleiro (2013) indited tht experimentl tests of GM orn in vrious res of Mexio re onsistently effiious in ontrolling key pests. This reserh showed tht use of GM Bt orn hyrids provides seson-long protetion from S. frugiperd. In ontrst, hemil ontrol only protets the plnt when the insetiide residue is present, nd filure in timing of pplition(s) represents risk in ontrol effiy. Piñ & Solleiro (2013) reported tht proteting non-bt orn in severl res of Mexio from infesttions of orn erworms nd fll rmyworms required from 3 to 5 insetiide pplitions per seson, nd from 720 g to 3.6 kg of tive ingredient per h. In ddition, reserhers in other ountries reported similr results of Bt orn with the Cry1A toxin for ontrolling the fll rmyworm with respet to onventionl hyrids with nd without insetiide ontrol (Buntin et l. 2001, 2004,; Buntin 2008; Hrdke et l. 2011; Hung et l. 2011; Ríos-Díez et l. 2012). Hyrids with the Bt toxin used in this reserh onsistently demonstrted redution in folir dmge. However, in ll res tested, Agrisure 3000 GT displyed more injured plnts nd lrger lesion size thn Agrisure Vipter 3110 nd Agrisure Vipter 3111. The higher level of dmge is thought to e due to Agrisure 3000 GT hving only 1 Bt toxin (Cry1A) for Lepidopter ontrol, wheres the other tested hyrids hve 2 pyrmided Bt genes. Multiple genes for resistne re thought to provide etter resistne to the pest. Agrisure Vipter 3110 nd Agrisure Vipter 3111 hve 2 toxins (pyrmid events) for Lepidopter ontrol, the δ-endotoxin Cry1A nd the vegettive insetiide protein Vip3A20, whih provide exellent protetion to the rop, not only from S. frugiperd ut lso from other Lepidopter (Burkness et l. 2010; Niu et l. 2013; Yng et l. 2013). Plnting dtes of experimentl plots were t lest 21 d lter thn the reommended dte in Sinlo. This requirement ws imposed y regultory uthorities in order to void ross pollintion with onventionl orn in the re. This ondition put the experimentl plots in this reserh under high pest pressure, whih me from surrounding orn fields nd sorghum fields. Despite this high level of pest pressure, the Bt toxin in the rop redued the infesttion level nd dmge. If these GM hyrids were plnted on the reommended plnting dte under optiml onditions to the rop, these Bt hyrids ould e expeted to perform well. Suh orn pest mngement progrm would redue the use of hemil insetiides, llow the rop to etter express its geneti potentil, nd onserve yield nd grin qulity y deresing folir dmge.
Aguirre et l.: Lef dmge y Spodopter frugiperd in Bt orn 279 Tle 3. Folir dmge nd perentge of plnts injured y fll rmyworms on the genetilly modified orn hyrids Agrisure Vipter 3111 nd Agrisure 3000 GT nd their respetive isolines t El Dordo nd Nvolto, Sinlo, in 2012. Hyrid Lolity Lef dmge, Plnts injured (%) Agrisure Vipter 3111 El Dordo 1.00 0.0 Agrisure Vipter 3111 + i El Dordo 1.00 0.0 Isoline + i El Dordo 3.53 64.4 Isoline El Dordo 2.89 56.7 F = 10.35*** F = 16.54*** Agrisure Vipter 3111 Nvolto 1.07 1.1 Agrisure Vipter 3111 + i Nvolto 1.07 1.1 Isoline + i Nvolto 3.20 52.2 Isoline Nvolto 4.90 81.1 F = 11.52*** F = 14.99*** Agrisure 3000 GT Nvolto 1.34 13.3 Agrisure 3000 GT + i Nvolto 1.13 7.8 Isoline + i Nvolto 3.87 66.7 Isoline Nvolto 4.97 77.8 F = 9.65*** F = 10.39*** i = insetiide ontrol Men numeril sle Genetilly modified hyrids nd their respetive isolines followed y the sme letter do not differ signifintly (ANOVA nd Tukey s test; P > 0.05). *** Indites signifint F vlue t P < 0.001, df = 11,35. Tle 4. Folir dmge nd perentge of plnts injured y fll rmyworms on the genetilly modified orn hyrid Agrisure Vipter 3111 nd its respetive isoline t Cmlote nd Oso Viejo, Culin, Sinlo, in 2013. Hyrid Lolity Lef dmge, Plnts injured (%) Agrisure Vipter 3111 Cmlote 1.00 0.0 Isoline + i Cmlote 1.72 35.8 Isoline Cmlote 3.22 74.2 F = 48.92*** F = 58.44*** Agrisure Vipter 3111 Oso Viejo 1.00 0.0 Isoline + i Oso Viejo 1.80 39.2 Isoline Oso Viejo 2.63 62.5 F = 35.46*** F = 27.38*** i = insetiide ontrol Men numeril sle Genetilly modified hyrid nd the respetive isoline tretments followed y the sme letter do not differ signifintly (ANOVA nd Tukey s test; P > 0.05). *** Indites signifint F vlue t P < 0.001, df = 8,35. Aknowledgments The uthors would like to thnk Syngent Agro S.A de C.V. de Méxio for providing the geneti mteril tht mde this reserh possile. Referenes Cited Ael CA, Wilson RL, Wisemn BR, White WH, Dvis FM. 2000. Conventionl resistne of experimentl mize lines to orn erworm (Lepidopter: Notuide), fll rmyworm (Lepidopter: Notuide), southwestern orn orer (Lepidopter: Crmide), nd sugrne orer (Lepidopter: Crmide). Journl of Eonomi Entomology 93: 982 988. Aguirre LA, Hernández A, Flores M, Frís GA, Cern E, Lnderos J, Hrris MK. 2015. Genetilly modified mize resistnt to orn erworm (Lepidopter: Notuide) in Sinlo, Mexio. Florid Entomologist 98: 821 826. Aguirre LA, Hernández A, Flores M, Pérez-Zuiri R, Cern E, Lnderos J, Frís GA. 2015. Comprión del nivel de dño de Spodopter frugiperd (Lepidopter: Notuide) en plnts de míz genétimente modifido y onvenionl en el Norte de Méxio. Southwestern Entomologist 40: 171 178. Bltzr BM, Cstro EL, Espinoz BA, de l Fuente MJM, Grzón TJA, González GJ, Gutiérrez MA, Guzmán RJL, Heredi DO, Hork MJ, Mdueño MJI, Shpugh WA, Stojšin D, Urie MHR, Zvl GF. 2015. Pollen-medited gene flow in mize: implitions for isoltion requirements nd oexistene in Mexio, the enter of origin of mize. PLoS One 10: e0131549. Buntin GD. 2008. Corn expressing Cry1A or Cry1F endotoxin for fll rmyworm nd orn erworm (Lepidopter: Notuide) mngement in field orn for grin prodution. Florid Entomologist 91: 523 530. Buntin GD, Dewey LR, Wilson DM, MPherson RM. 2001. Evlution of Yieldgrd trnsgeni resistne for ontrol of fll rmyworm nd orn erworm (Lepidopter: Notuide) on orn. Florid Entomologist 84: 37 42. Buntin GD, All JN, Lee RD, Wilson DM. 2004. Plnt-inorported Billus thuringiensis resistne for ontrol of fll rmyworm nd orn erworm (Lepidopter: Notuide) in orn. Journl of Eonomi Entomology 97: 1603 1611. Buntin GD, Flnders KL, Lynh RE. 2004. Assessment of experimentl Bt events ginst fll rmyworm nd orn erworm in field orn. Journl of Eonomi Entomology 97: 259 264. Burkness EC, Dively G, Ptton T, Morey AC, Huthison WD. 2010. Novel Vip3A Billus thuringiensis (Bt) mize pprohes high-dose effiy ginst Helioverp ze (Lepidopter: Notuide) under field onditions. GM Crops 1: 337 343. Csmuz A, Juárez ML, Soís MG, Murú MG, Prieto S, Medin S, Willink E, Gstminz G. 2010. Revisión de los hospederos del gusno ogollero del míz, Spodopter frugiperd (Lepidopter: Notuide). Revist de l Soiedd Entomológi Argentin 69: 209 231. Cstro BA, Leonrd BR, Riley TJ. 2004. Mngement of feeding dmge nd survivl of southwestern orn orer nd sugrne orer (Lepidopter: Crm-
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