Transcriptome differential co‐expression reveals distinct molecular response of fall‐armyworm strains to DIMBOA

Abstract

BACKGROUND: 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), the main benzoxazinoid found in corn, elicits variable larval responses from different pest moths. For the widespread and highly polyphagous Spodoptera frugiperda (Lepidoptera: Noctuidae), the fall-armyworm (FAW), DIMBOA acts as a feeding stimulant and improves larval growth at low concentrations. The FAW present two host plant-related strains, corn and rice strains, related to host preference on corn and other Graminae or rice. Based on both host preference and strain divergence of the FAW on corn, a cereal containing DIMBOA, and rice, lacking this compound, we question if corn and rice strains larvae respond equally toward DIMBOA. We evaluated differential expression in the transcriptome of both midgut and fat body larval tissues of the two strains reared on either DIMBOAenriched artificial diet or control diet and inferred Bayesian networks. RESULTS: We found differences in performance between corn and rice strain larvae reared on DIMBOA, as well as several differentially regulated contigs annotated as esterases, peptidases, transferases and reductases, all of them known for being related to responses of lepidopterans and other insects to DIMBOA. We also found a UDP-glucuronosyltransferase very similar to others found in many lepidopterans occupying a central hub within a transferase Bayesian network, suggesting that it is essential to an effective response to DIMBOA in FAW. CONCLUSION: Our results suggest that there is an intrinsic cost for FAW rice strain larvae to metabolize corn-originated hydroxamic acids, which could have resulted in the partial host-associated genetic isolation found at FAW field populations.

Population genomics of fall armyworm in Brazil and Argentina revealed by Genotyping-by- Sequencing and implications for pest management

“…Odorant receptors function in insects olfaction process, which is indispensable for host selection for feeding and oviposition 45 . UDP-glucuronosyltransferase, in turn, appears to be associated with C-strain ability to detoxify DIMBOA 47 , a toxic compound produced by corn plants but not rice. In conclusion, our work strongly suggest that positive selection is affecting allele frequencies at the level of populations and host strains.…”

Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (Sitobion avenae)

“…The resistance of benzoxazinoid towards herbivores can be implemented by toxic and antifeedant activities. Benzoxazinoids have been shown to be toxic to many chewing herbivores, such as Ostrinia nubilalis, O. furnacalis, Spodoptera exigua, and S. frugiperda [38][39][40][41]. Compared to chewing herbivores, aphids feed upon phloem sap with their stylet-like mouthparts from plant sieve elements and cause little damage to host plants [42].…”

Fitness costs associated with spinetoram resistance inSpodoptera frugiperdais driven by host plants

“…Researchers showed the involvement of UDP-glycosyltransferases in detoxification of DIMBOA by S. frugiperda (Israni et al 2020;Silva-Brandão et al 2021) and allied it to the coevolutionary relationship between them (Mello and Silva-Filho 2002).…”

“…This controversy between a toxic secondary component of corn and the absence of fitness cost in S. frugiperda has been recently studied. Researchers showed the involvement of UDP-glycosyltransferases in detoxification of DIMBOA by S. frugiperda (Israni et al 2020; Silva-Brandão et al 2021) and allied it to the coevolutionary relationship between them (Mello and Silva-Filho 2002).…”