Extended Sentinel Monitoring of Helicoverpa zea Resistance to Cry and Vip3Aa Toxins in Bt Sweet Corn: Assessing Changes in Phenotypic and Allele Frequencies of Resistance

Galen P Dively; Tom P Kuhar; Sally V Taylor; Helene Doughty; Kristian Holmstrom; Daniel O Gilrein; Brian A Nault; Joseph Ingerson-Mahar; Anders Huseth; Dominic Reisig; Shelby Fleischer; David Owens; Kelley Tilmon; Francis Reay-Jones; Pat Porter; Jocelyn Smith; Julien Saguez; Jason Wells; Caitlin Congdon; Holly Byker; Bryan Jensen; Chris DiFonzo; William D Hutchison; Eric Burkness; Robert Wright; Michael Crossley; Heather Darby; Tom Bilbo; Nicholas Seiter; Christian Krupke; Craig Abel; Brad S Coates; Bradley McManus; Billy Fuller; Jeffrey Bradshaw; Julie A Peterson; David Buntin; Silvana Paula-Moraes; Katelyn Kesheimer; Whitney Crow; Jeffrey Gore; Fangneng Huang; Dalton C Ludwick; Amy Raudenbush; Sebastian Jimenez; Yves Carrière; Timothy Elkner; Kelly Hamby

doi:10.3390/insects14070577

Extended Sentinel Monitoring of Helicoverpa zea Resistance to Cry and Vip3Aa Toxins in Bt Sweet Corn: Assessing Changes in Phenotypic and Allele Frequencies of Resistance

Insects. 2023 Jun 25;14(7):577. doi: 10.3390/insects14070577.

Authors

Galen P Dively¹, Tom P Kuhar², Sally V Taylor³, Helene Doughty⁴, Kristian Holmstrom⁵, Daniel O Gilrein⁶, Brian A Nault⁷, Joseph Ingerson-Mahar⁸, Anders Huseth⁹, Dominic Reisig¹⁰, Shelby Fleischer¹¹, David Owens¹², Kelley Tilmon¹³, Francis Reay-Jones¹⁴, Pat Porter¹⁵, Jocelyn Smith¹⁶, Julien Saguez¹⁷, Jason Wells¹⁸, Caitlin Congdon¹⁹, Holly Byker²⁰, Bryan Jensen²¹, Chris DiFonzo²², William D Hutchison²³, Eric Burkness²³, Robert Wright²⁴, Michael Crossley²⁵, Heather Darby²⁶, Tom Bilbo²⁷, Nicholas Seiter²⁸, Christian Krupke²⁹, Craig Abel³⁰, Brad S Coates³⁰, Bradley McManus³¹, Billy Fuller³¹, Jeffrey Bradshaw³², Julie A Peterson³³, David Buntin³⁴, Silvana Paula-Moraes³⁵, Katelyn Kesheimer³⁶, Whitney Crow³⁷, Jeffrey Gore³⁷, Fangneng Huang³⁸, Dalton C Ludwick³⁹, Amy Raudenbush¹³, Sebastian Jimenez⁴⁰, Yves Carrière⁴¹, Timothy Elkner⁴², Kelly Hamby¹

Affiliations

¹ Department of Entomology, University of Maryland, College Park, MD 20742, USA.
² Department of Entomology, Virginia Tech, Blacksburg, VA 24060, USA.
³ Department of Entomology, Virginia Tech, Suffolk, VA 23434, USA.
⁴ Virginia Tech ESAREC/Entomology, Painter, VA 23420, USA.
⁵ Pest Management Office, Rutgers University, New Brunswick, NJ 08901, USA.
⁶ LIHREC, Cornell University, Riverhead, NY 11901, USA.
⁷ Department of Entomology, Cornell AgriTech, Geneva, NY 14456, USA.
⁸ Rutgers Agricultural Research and Extension Center, Rutgers University, Bridgeton, NJ 08302, USA.
⁹ Department of Entomology and Plant Pathology, NC State University, Raleigh, NC 27601, USA.
¹⁰ Department of Entomology and Plant Pathology, NC State University, Plymouth, NC 27962, USA.
¹¹ Department of Entomology, Penn State University, University Park, PA 16802, USA.
¹² Cooperative Extension, Carvel REC, University of Delaware, Georgetown, DE 19947, USA.
¹³ Ohio Agricultural Research and Development Center, Wooster, OH 44691, USA.
¹⁴ Department of Plant and Environmental Sciences, Clemson University, Florence, SC 29501, USA.
¹⁵ Department of Entomology, AgriLife Research and Extension Center, Texas A&M University, Lubbock, TX 79401, USA.
¹⁶ Department of Plant Agriculture, University of Guelph, Ridgetown Campus, ON N1G 2W1, Canada.
¹⁷ CEROM, 740 Chemin Trudeau, Saint-Mathieu-de-Beloeil, QC J3G 0E2, Canada.
¹⁸ New Brunswick Department of Agriculture, Sussex, NB E4E 5L8, Canada.
¹⁹ Perennia Food and Agriculture, Kentville, NS B4N 1J5, Canada.
²⁰ Department of Plant Agriculture, University of Guelph, Winchester, ON N1G 2W1, Canada.
²¹ Arlington Agricultural Research Station, University of Wisconsin, WI 53706, USA.
²² Department of Entomology, Michigan State University, East Lansing, MI 48824, USA.
²³ Department of Entomology, University of Minnesota, St. Paul, MN 55455, USA.
²⁴ Department of Entomology, University of Nebraska-Lincoln, NE 68588, USA.
²⁵ Department of Entomology and Wildlife Ecology, University of Delaware, Newark, DE 19711, USA.
²⁶ Department of Plant and Soil Sciences, University of Vermont, Burlington, VT 05405, USA.
²⁷ Department of Plant and Environmental Sciences, Clemson University, Charleston, SC 29414, USA.
²⁸ Illinois Extension, University of Illinois, Urbana, IL 61820, USA.
²⁹ Department of Entomology, Purdue University, West Lafayette, IN 47906, USA.
³⁰ USDA-ARS Corn Insects and Crop Genetics Research, Iowa State University, Ames, IA 50011, USA.
³¹ South Dakota State, Brookings, SD 57006, USA.
³² Panhandle Research and Extension Center, Scottsbluff, NE 69361, USA.
³³ West Central Research and Extension Center, University of Nebraska, North Platte, NE 69101, USA.
³⁴ Griffin Campus, University of Georgia, Griffin, GA 30223, USA.
³⁵ UF/IFAS West Florida Research and Education Center, Jay, FL 32565, USA.
³⁶ Department of Entomology & Plant Pathology, Auburn University, Auburn, AL 36849, USA.
³⁷ Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Delta Research and Extension Center, Mississippi State University, Stoneville, MS 39762, USA.
³⁸ Department of Entomology, Louisiana State University, Baton Rouge, LA 70803, USA.
³⁹ Department of Entomology, Texas A&M AgriLife Extension Service, Corpus Christi, TX 78404, USA.
⁴⁰ PEI Department of Agriculture and Land, Charlotte, PE C1A 7N8, Canada.
⁴¹ Department of Entomology, University of Arizona, Tucson, AZ 85721, USA.
⁴² Southeast Research and Extension Center, Landisville, PA 17538, USA.

Abstract

Transgenic corn and cotton that produce Cry and Vip3Aa toxins derived from Bacillus thuringiensis (Bt) are widely planted in the United States to control lepidopteran pests. The sustainability of these Bt crops is threatened because the corn earworm/bollworm, Helicoverpa zea (Boddie), is evolving a resistance to these toxins. Using Bt sweet corn as a sentinel plant to monitor the evolution of resistance, collaborators established 146 trials in twenty-five states and five Canadian provinces during 2020-2022. The study evaluated overall changes in the phenotypic frequency of resistance (the ratio of larval densities in Bt ears relative to densities in non-Bt ears) in H. zea populations and the range of resistance allele frequencies for Cry1Ab and Vip3Aa. The results revealed a widespread resistance to Cry1Ab, Cry2Ab2, and Cry1A.105 Cry toxins, with higher numbers of larvae surviving in Bt ears than in non-Bt ears at many trial locations. Depending on assumptions about the inheritance of resistance, allele frequencies for Cry1Ab ranged from 0.465 (dominant resistance) to 0.995 (recessive resistance). Although Vip3Aa provided high control efficacy against H. zea, the results show a notable increase in ear damage and a number of surviving older larvae, particularly at southern locations. Assuming recessive resistance, the estimated resistance allele frequencies for Vip3Aa ranged from 0.115 in the Gulf states to 0.032 at more northern locations. These findings indicate that better resistance management practices are urgently needed to sustain efficacy the of corn and cotton that produce Vip3Aa.

Keywords: Bacillus thuringiensis toxins; bollworm; corn earworm; phenotypic and allele resistance frequency; resistance monitoring.

Grants and funding

Most authors volunteered their time without external funding; however, we specifically acknowledge partial funding from the following: Friends of Long Island Horticulture, the Hatch Multistate Research Fund (NC, no. 1006646; MD, no. 0095671), the National Institute of Food and Agriculture, the Crop Protection and Pest Management Program, the Extension Implementation Program (DE, no. 2017-70006-27286; MN, no. 2017-70006-27278), the Atlantic Grains Council, and the Canadian Agricultural Partnership Program. This research was supported (in part) by the U.S. Department of Agriculture, Agricultural Research Service. Any mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. The USDA is an equal opportunity provider and employer.