Huidong Wang, Jing Song, Benjamin J. Hunt, Kairan Zuo, Huiru Zhou, Angela Hayward, Bingbing Li, Yajuan Xiao, Xing Geng, Chris Bass, and Shutang Zhou.

PNAS; April 29, 2024; 121 (19) e2402045121

Significance

The genetic factors that influence diet breadth in herbivorous insects remain poorly understood. Here, we demonstrate that uridine diphosphate (UDP)-glycosyltransferase (UGT) genes play a key role in the capacity of species within the Spodoptera genus of insects to utilize certain host plants and thus act as important determinants of host range. We uncover a conserved UGT-mediated mechanism of plant defense chemical detoxification in generalist Spodoptera species that allows them to utilize maize, wheat, and rice. However, this mechanism has been lost in the specialist Spodoptera picta through mutation, rendering it unable to feed on these plants. Our findings provide insights into the molecular innovations required for ecological adaptation and the role of gene gain and loss in determining insect host range.

Abstract

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.

See https://www.pnas.org/doi/10.1073/pnas.2402045121

Figure 4:

Performance of S. frugiperda UGT cluster knockout strains on different host plants and sensitivity to phytotoxins. (A and B) Schematic of the UGT genes knocked out in the XZ-d33c1, XZ-d33c2, and XZ-d40c strains. (C) Performance (relative weight index, RWI) of the XZ-d33c1, XZ-d33c2, and XZ-d40c strains on seven different host plants. RWI = (the weight of knockout strain on plant/average weight of knockout strain on artificial diet)/(average weight of XZ strain on plant/average weight of XZ strain on artificial diet). The red rectangle indicates the decreased performance of knockout strains on a specific plant compared to the XZ strain, and the blue rectangle indicates increased performance. Forty-eight or sixty individuals were tested on each plant or artificial diet for all strains. (D–K) Sensitivity of the XZ-d33c1, XZ-d33c2, and XZ-d40c strains to seven phytotoxins. Values are means of corrected mortality ± SEM, n = 3 to 6 biologically independent samples, twenty-four larvae were used as a biologically independent sample. Unpaired t tests were used for statistical comparisons, **P < 0.01, ***P < 0.001.