Field-evolved resistance of Helicoverpa zea (Boddie) to transgenic maize expressing pyramided Cry1A.105/Cry2Ab2 proteins in northeast Louisiana, the United States

Kaur, Gagandeep; Guo, Jianguo; Brown, Sebe; Head, Graham P.; Price, Paula A.; Paula‐Moraes, Silvana V.; Ni, Xinzhi; Dimase, Marcelo; Huang, Fangneng

doi:10.1016/j.jip.2019.02.007

Cited by 88 publications

(108 citation statements)

References 49 publications

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“…Prior to 2015, larvae of H. zea were susceptible to MON 89034 expressing Cry1A.105/Cry2Ab2 in the U.S. 13,22,33 However, in recent years, multiple authors [16][17][18][19]34 have reported that susceptibility to Cry1A and Cry2A proteins in H. zea collected from corn and cotton fields in the southern region of the U.S. has been significantly reduced. Dively et al 15 also showed significant reductions in field performance of Cry1Ab sweet corn and MON 89034 pyramided Bt sweet corn for control of H. zea in Maryland, particularly in 2016.…”

Section: Discussionmentioning

confidence: 99%

“…Field control problems in both pyramided Bt corn and Bt cotton expressing Cry1A/Cry2A against H. zea have been reported in the United States. [15][16][17][18][19] The appearance of resistance to the pyramided Bt crops emphasizes the importance of using appropriate IRM strategies to preserve their efficacy. Currently, the RIB strategy has not been implemented in the southern U.S. where Bt cotton is also a field crop.…”

Section: Introductionmentioning

confidence: 99%

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Extended evaluation of Bt protein cross‐pollination in seed blend plantings on survival, growth, and development of Helicoverpa zea feeding on refuge ears

Yang

Kerns

Head

et al. 2019

Pest Management Science

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BACKGROUND A seed blend, also called refuge in a bag (RIB), is used as a strategy to provide refuge for planting pyramided Bt corn in the U.S. Corn Belt. A major concern for the RIB strategy is cross‐pollination between Bt and refuge plants, which may reduce susceptible populations of ear‐feeding insects like Helicoverpa zea and affect the evolution of resistance. Previous studies showed a 5:95% (Non‐Bt: Bt) RIB would be unlikely to provide sufficient refuge populations of H. zea for resistance management. In this study, we extended our research and conducted multiple trials to determine if three RIB plantings with greater refuge sizes (10, 20, and 30% refuge) could provide sufficient H. zea susceptible populations to delay resistance development. RESULTS Experimental results showed that cross‐pollination in 10:90%, 20:80%, and 30:70% RIB plantings still significantly reduced larval survival, delayed larval development and decreased the pupal size of H. zea on refuge plants. Regression analysis showed that the percent reduction of neonate‐to‐adult survivorship, relative to the survivorship on pure non‐Bt ears, was significantly negatively correlated with the refuge percentage. CONCLUSION These findings suggest that, approximately a 15% non‐Bt refuge plants in RIB plantings could produce a similar number of susceptible adult moths as a 5% structured refuge planting, while an approximately 30% non‐Bt refuge plant in RIB plantings could provide a similar number of susceptible moths as a 20% structured refuge planting. Information generated from this study should be useful in refining resistance management strategies for Bt crop technologies. © 2019 Society of Chemical Industry

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Extended evaluation of Bt protein cross‐pollination in seed blend plantings on survival, growth, and development of Helicoverpa zea feeding on refuge ears

Yang

Kerns

Head

et al. 2019

Pest Management Science

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“…The assay was done in a 128 well bioassay plate (C-D International Inc., Pitman, NJ). A single CEW neonate from a laboratory CEW colony obtained from Benzon Research Inc. (Carlisle, PA) was added to each well with 1 g diet using a camel hair brush (Kaur et al 2019). At least 20 larvae were tested per treatment and the assay was repeated four times.…”

Section: Methodsmentioning

confidence: 99%

“…Corn earworm [ CEW ; Helicoverpa zea (Boddie); formerly in the genus Heliothis ] has become the most economically important pest in the southern United States where non-freezing winters are conducive for CEW to multiply by 4-7 generations in a year. Resistance of this pest to a wide range of insecticides and to Bt maize has also been documented (Capinera 2004; Dively et al 2016; Kaur et al 2019). Although CEW has multiple crop and weed hosts, maize is its preferred host (Johnson et al 1975).…”

Section: Introductionmentioning

confidence: 99%

Low aflatoxin levels and flowering delay inAspergillus flavus-resistant maize lines are correlated with increased corn earworm damage and enhanced seed fumonisin content

Subbaiah

Huang

Busman

et al. 2020

Preprint

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Preharvest mycotoxin contamination of field-grown crops is influenced not only by the host genotype, but also inoculum load, insect pressure and their confounding interactions with seasonal weather. In two field trials, we observed a preferred natural infestation of specific maize (Zea mays L.) genotypes by corn earworm (Helicoverpa zea Boddie) and investigated this unexpected interaction. These studies involved four maize lines with contrasting levels of resistance to Aspergillus flavus. The resistant lines had 7 to 14-fold greater infested ears than the susceptible lines. However, seed aflatoxin B1 levels, in mock- or A. flavus-inoculated ears were consistent with maize genotype resistance to A. flavus. Further, the corn earworm-infested ears had greater levels of fumonisin content in seeds than uninfested ears, indicating that the insect may have vectored native Fusarium verticillioides inoculum. The two maize lines with heavy infestation showed delayed flowering. The availability of young silk for egg-laying could have been a factor in the pervasive corn earworm damage of these lines. At the same time, H. zea larvae reared on AF-infused diet showed decreasing mass with increasing AF and >30% lethality at 250 ppb. In contrast, corn earworm was tolerant to fumonisin with no significant loss in mass even at 100 ppm, implicating the low seed aflatoxin content as a predominant factor for the prevalence of corn earworm infestation and the associated fumonisin contamination in A. flavus resistant lines. These results highlight the need for integrated strategies targeting mycotoxigenic fungi and their insect vectors to enhance the safety of crop commodities.IMPORTANCEAspergillus and Fusarium spp. not only cause ear rots in maize leading to crop loss, they can also contaminate the grain with carcinogenic mycotoxins. Incorporation of genetic resistance into breeding lines is an ideal solution for mycotoxin mitigation. However, the goal is fraught by a major problem. Resistance for AF or FUM accumulation is quantitative and contributed by several loci with small effects. Our work reveals that host phenology (flowering time) and insect vector-mycotoxin interactions can further confound breeding efforts. A host genotype even with demonstrable resistance can become vulnerable due to seasonal variation in flowering time or an outbreak of chewing insects. Incorporation of resistance to a single mycotoxin accumulation and not pairing it with insect resistance may not adequately ensure food safety. Diverse strategies including host-induced silencing of genes essential for fungal and insect pest colonization and broad-spectrum biocontrol systems need to be considered for robust mycotoxin mitigation.

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“…Helicoverpa zea is one lepidopteran species targeted by Bt crops with low susceptibility to Cry proteins (Stone and Sims, 1993; Ali et al, 2006; Sivasupramaniam et al, 2008). A major pest of both corn and cotton in the U.S., H. zea has evolved resistance to several Cry proteins (Welch et al, 2015; Dively et al, 2016; Reisig et al, 2018; Kaur et al, 2019; Yang et al, 2019). While some efforts have been made to understand the molecular mechanisms underlying Cry resistance in H. zea (Caccia et al, 2012; Zhang et al, 2019), we still know little about how selection by Cry proteins has shaped genotype frequencies in this important pest.…”

Section: Introductionmentioning

confidence: 99%

Mutations in a novel cadherin gene associated with Bt resistance inHelicoverpa zea

Fritz

Nunziata

Guo

et al. 2019

Preprint

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20Transgenic corn and cotton produce crystalline (Cry) proteins derived from the soil 21 bacterium Bacillus thuringiensis (Bt) that are toxic to lepidopteran larvae. Helicoverpa zea, a 22 key pest of corn and cotton in the U.S., has evolved widespread resistance to these proteins 23 produced in Bt corn and cotton. While the genomic targets of Cry selection and the mutations 24 that produce resistant phenotypes are known in other lepidopteran species, little is known about 25 how Cry proteins shape the genome of H. zea. We scanned the genomes of Cry1Ac-selected and 26 unselected H. zea lines, and identified eleven genes on six scaffolds that showed evidence of 27 selection by Cry1Ac, including cadherin-86C (cad-86C), a gene from a family that is involved in 28 Cry1A resistance in other lepidopterans. Although this gene was expressed in the H. zea larval 29 midgut, the protein it encodes has only 17 to 22% identity with cadherin proteins from other 30 species previously reported to be involved in Bt resistance. An analysis of midgut-expressed 31 cDNAs showed significant between-line differences in the frequencies of putative 32 nonsynonymous substitutions (both SNPs and indels). Our results indicate that cad-86C is a 33 target of Cry1Ac selection in H. zea. Future work should investigate phenotypic effects of these 34 nonsynonymous substitutions and their impact on phenotypic resistance in field populations.

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Field-evolved resistance of Helicoverpa zea (Boddie) to transgenic maize expressing pyramided Cry1A.105/Cry2Ab2 proteins in northeast Louisiana, the United States

Cited by 88 publications

References 49 publications

Extended evaluation of Bt protein cross‐pollination in seed blend plantings on survival, growth, and development of Helicoverpa zea feeding on refuge ears

Extended evaluation of Bt protein cross‐pollination in seed blend plantings on survival, growth, and development of Helicoverpa zea feeding on refuge ears

Low aflatoxin levels and flowering delay inAspergillus flavus-resistant maize lines are correlated with increased corn earworm damage and enhanced seed fumonisin content

Mutations in a novel cadherin gene associated with Bt resistance inHelicoverpa zea

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