Benjamin J Hunt | PubMed Health

PubMed2026

Historical metabolic adaptation potentiates the rapid evolution of flonicamid resistance in Myzus persicae.

Rapid adaptation to novel environments is often shaped not only by newly acquired mutations but also by historical genetic backgrounds established through prior evolutionary events. However, the extent to which such historical contingency contributes to the rapid evolution of insecticide resistance remains poorly understood. Here, we investigated the emergence of resistance to flonicamid, a recently deployed insecticide, in the green peach aphid, Myzus persicae. We show that constitutive overexpression of the P450 enzymes CYP6CY3 and CYP6CY4, already widespread in populations of M. persicae before flonicamid deployment, confers a previously cryptic tolerance phenotype to flonicamid. However, biochemical and transgenic analyses demonstrated that these metabolic adaptations provide only weak protection against flonicamid. Following flonicamid deployment, however, a novel target-site mutation, NaamV251I, in the recently identified molecular target of 4-trifluoromethylnicotinamide (TFNA-AM), emerged in M. persicae on a genetic background of CYP6CY3 or CYP6CY4 overexpression. Structural modeling, enzymatic assays, and CRISPR-Cas9 genome editing demonstrated that this mutation reduces target sensitivity and independently confers moderate resistance. Strikingly, combining the nicotinamidase (Naam) mutation with pre-existing CYP6CY3 or CYP6CY4 overexpression produced substantially elevated resistance phenotypes that far exceeded the effects of either mechanism alone. Our results demonstrate that the pre-existing metabolic background did not itself evolve further following flonicamid deployment but fundamentally altered the phenotypic consequences of a subsequently acquired target-site mutation. These findings provide direct evidence that historical adaptive variation can potentiate rapid resistance evolution to newly introduced insecticides and reveal how interactions between past and contemporary adaptations shape evolutionary responses to novel environmental challenges.

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PubMed2024

UDP-glycosyltransferases act as key determinants of host plant range in generalist and specialist Spodoptera species.

Phytophagous insects have evolved sophisticated detoxification systems to overcome the antiherbivore chemical defenses produced by many plants. However, how these biotransformation systems differ in generalist and specialist insect species and their role in determining insect host plant range remains an open question. Here, we show that UDP-glucosyltransferases (UGTs) play a key role in determining the host range of insect species within the Spodoptera genus. Comparative genomic analyses of Spodoptera species that differ in host plant breadth identified a relatively conserved number of UGT genes in generalist species but high levels of UGT gene pseudogenization in the specialist Spodoptera picta. CRISPR-Cas9 knockouts of the three main UGT gene clusters of Spodoptera frugiperda revealed that UGT33 genes play an important role in allowing this species to utilize the poaceous plants maize, wheat, and rice, while UGT40 genes facilitate utilization of cotton. Further functional analyses in vivo and in vitro identified the UGT SfUGT33F32 as the key mechanism that allows generalist S. frugiperda to detoxify the benzoxazinoid DIMBOA (2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one), a potent insecticidal phytotoxin produced by poaceous plants. However, while this detoxification capacity is conserved in several generalist Spodoptera species, Spodoptera picta, which specializes on Crinum plants, is unable to detoxify DIMBOA due to a nonfunctionalizing mutation in SpUGT33F34. Collectively, these findings provide insight into the role of insect UGTs in host plant adaptation, the mechanistic basis of evolutionary transitions between generalism and specialism and offer molecular targets for controlling a group of notorious insect pests.

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