A nuclear receptor HR96-related gene underlies large trans-driven differences in detoxification gene expression in a generalist herbivore

Abstract

The role, magnitude, and molecular nature of trans-driven expression variation underlying the upregulation of detoxification genes in pesticide resistant arthropod populations has remained enigmatic. In this study, we performed expression quantitative trait locus (eQTL) mapping (n = 458) between a pesticide resistant and a susceptible strain of the generalist herbivore and crop pest Tetranychus urticae. We found that a single trans eQTL hotspot controlled large differences in the expression of a subset of genes in different detoxification gene families, as well as other genes associated with host plant use. As established by additional genetic approaches including RNAi gene knockdown, a duplicated gene with a nuclear hormone receptor HR96-related ligand-binding domain was identified as causal for the expression differences between strains. The presence of a large family of HR96-related genes in T. urticae may enable modular control of detoxification and host plant use genes, facilitating this species’ known and rapid evolution to diverse pesticides and host plants.

Independent genetic mapping experiments identify diverse molecular determinants of host adaptation in a generalist herbivore

“…In the F2 backcross approach, we found evidence for the dominant inheritance of performance on tomato (Figure 5B). Natural variation in the expression of genes involved in allelochemical detoxification is often trans-regulated and inherited as a dominant trait in this species, and thus is open for selection when it is exposed in heterozygous diploid females (Ji et al, 2023;Kurlovs et al, 2022).…”

“…In contrast, generalists exploit a wide range of hosts, requiring flexibility in their mechanisms of host use (Grbić et al, 2011). Plasticity in the molecular mechanisms that regulate genes involved in host use can enable generalists to cope with multiple classes of phytochemicals (Ji et al, 2023;Pym et al, 2019;Snoeck et al, 2018;Vandenhole et al, 2021). While generalists and specialists largely employ similar, but not identical mechanisms to exploit their hosts (Ali & Agrawal, 2012;Bruinsma et al, 2023;Bui et al, 2018), it is not well understood how selection shapes the diversity of mechanisms involved in host use in generalists, or whether genetic changes due to selection impact the host range of locally adapted populations.…”

“…With a short generation time of 12-14 days under laboratory conditions, populations experimentally isolated on challenging hosts show clear adaptation patterns within 5 to 25 generations (Belliure et al, 2010;Cazaux et al, 2014). Genetically distinct populations often show no signs of reproductive isolation, allowing to create hybrid lines in which parental alleles can be traced and recombination is even (Ji et al, 2023;Xue et al, 2023). In addition, a wellannotated, chromosome-level assembled genome facilitates the integration of bioassays with genomic tools to identify causal genes within quantitative trait loci (QTLs) (Grbić et al, 2011;Kurlovs et al, 2019;Wybouw et al, 2019).…”

Structural and functional studies reveal the molecular basis of substrate promiscuity of a glycosyltransferase originating from a major agricultural pest

“…( 10 ) were the first ones to show, in vitro , the ability of these enzymes to glycosylate a broad range of plant secondary metabolites and acaricides, indicating that these UGTs play a role in mite host and pesticide adaptations. A recent eQTL study revealed that the over-expression of at least some UGTs is coregulated with other detoxifying enzymes such as cytochrome P450s, by a master regulator from the HR96 hormone receptor family, reinforcing their role in adaptation and resistance ( 23 ).…”

“…It is assumed that specific properties of flavonoids arise from their molecular structure, such as the presence or absence of functional groups, as well as conjugated groups, like sugar moieties ( 29 , 30 , 31 ). For example, different flavonoids and their glycoside derivatives possess different anti-herbivore and anti-cancer attributes ( 23 , 32 ). Consistently, it has been shown that bacteria and herbivores rely on UGTs to detoxify these compounds ( 10 , 33 , 34 ).…”