Multi-omics approaches for understanding spinetoram resistance in Spodoptera frugiperda (Lepidoptera: Noctuidae)

Author(s)

Rubens Hideo Kanno

• Document type: Doctoral Thesis
• Press: Piracicaba.
• Institution: Universidade de São Paulo (USP). Escola Superior de Agricultura Luiz de Queiroz (ESALA/BC)
• Defense date: 2023-08-01

Examining board members

Celso Omoto; Fernando Luis Consoli; Oscar Arnaldo Batista Neto e Silva; Herbert Álvaro Abreu de Siqueira

• Advisor: Celso Omoto

Abstract

Insecticide resistance is one of the main challenges in pest management programs. The fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), is a polyphagous pest with a high risk of resistance evolution to insecticides. Resistance of S. frugiperda to spinetoram has been reported, however, information about the molecular basis of spinetoram resistance and the possible fitness costs associated with it is not elucidated. The use of multi-omics approaches has provided insights into resistance mechanisms and adaptation processes. Thus, to support the insecticide resistance management programs and understand the spinetoram resistance in S. frugiperda, this study aimed to: i) characterize the molecular basis of spinetoram resistance in S. frugiperda employing the bulk segregant analysis combined with DNA and RNA sequencing, ii) assess the fitness costs of spinetoram resistance in S. frugiperda by comparing several biological parameters and constructing fertility life tables for resistant, susceptible, and heterozygous strains feeding on plants of corn, soybean, and cotton plants, iii) characterize and quantify the proteins of spinetoram-resistant and susceptible strains of S. frugiperda when fed on corn, soybean and cotton plants using liquid chromatography mass spectrometry (LC-MS), and iv) identify the metabolites associated with spinetoram resistance in S. frugiperda using metabolomics-based gas chromatography mass spectrometry (GC-MS). The genome mapping analysis led to the identification of the deletion of three nucleotides in the subunit α6 of the nicotinic acetylcholine receptor (nAChR α6), and the transcriptome analysis showed up-regulation of some cytochrome P450, ABC transporters and cuticle proteins genes that could be involved in spinetoram resistance. Based on life history traits, there are fitness costs associated with spinetoram resistance in S. frugiperda when the larvae feed on soybean and cottons plants, but not on corn plants. The proteomics study showed that the host plants are significant factors in shaping the protein expression of spinetoram-resistant and susceptible strains, with majority of the differentially expressed proteins between these two strains being specific to each host plant. Enrichment analysis showed that the differential expressed proteins were related to metabolic, cellular, developmental, and biological regulation processes. A total of 86 metabolites were detected using GC-MS based metabolomics, of which 20 metabolites were differentially abundant between the spinetoram-resistant and susceptible strains. The differential metabolites were mainly amino acids, carbohydrates, dicarboxylic acids and fatty acids and they were enriched in pathways related to cysteine and methionine metabolism, linoleic acid metabolism and aminoacyl-tRNA biosynthesis. The use of multi-omics approaches allowed a comprehensive and integrated understanding of the molecular mechanisms underlying insecticide and host plant adaptation in S. frugiperda, providing a holistic perspective on these two adaptive processes. (AU)

• FAPESP's process: 19/06217-8 - Impact of agricultural landscape on resistance management of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) to spinosyn insecticides
• Grantee: Rubens Hideo Kanno
• Support Opportunities: Scholarships in Brazil - Doctorate