Expressional divergence of insect GOX genes: From specialist to generalist glucose oxidase

Abstract

Insect herbivores often secrete glucose oxidase (GOX) onto plants to counteract plant defenses and potential pathogens. Whether generalist herbivores always have significantly higher GOX activities than their specialist counterparts at any comparable stage or conditions and how this is realized remain unknown. To address these two general questions, we subjected larvae of a pair of sister species differed mainly in host range, the generalist Helicoverpa armigera and its specialist counterpart Helicoverpa assulta, to the same sets of stage, protein to digestible carbohydrate (P:C) ratio, allelochemical or host plant treatments for simultaneous analyses of GOX transcripts and activities in their labial glands. GOX activity and transcripts are upregulated concurrently with food ingestion and body growth, downregulated with stopping ingestion and wandering for pupation in both species. The three tested host plants upregulated GOX transcripts, and to a lesser extent, GOX activity in both species. There were significant differences in both GOX transcripts and activity elicited by allelochemicals, but only in GOX transcripts by P:C ratios in both species. GOX activities were higher in H. armigera than H. assulta in all the comparable treatments, but GOX transcripts were significantly higher either in generalists or in specialists, depending on the developmental stages, host plants, P:C ratio and allelochemicals they encounter. These data indicate that the greater GOX activity in generalist herbivores is not achieved by greater transcription rate, but by greater transcript stability, greater translation rate, better enzyme stability and/or their combination.

Genome Size Reversely Correlates With Host Plant Range in Helicoverpa Species

“…For example, genome size expansion due to TE proliferation is subjected to developmental restriction in holometabolous insect orders (Gregory, 2002; Hanrahan and Johnston, 2011). Host plant expansion should require, as in the case of pathogenic bacteria and fungi, expansion of genes responsible for adapting to distinct host plants (e.g., allelochemical-metabolizing enzymes) (Li et al, 2007; Rane et al, 2016; Calla et al, 2017; Bansal and Michel, 2018) and/or modifying host plants (e.g., glucose oxidases and other plant defense-repressing genes) (Simon et al, 2015; Giron et al, 2016; Guiguet et al, 2016; Rivera-Vega et al, 2017; Yang et al, 2017; Basu et al, 2018) and proliferations of non-coding regulatory sequences responsible for regulation of host use related genes. Accordingly, we call insect tissues such as salivary gland and mandibular gland that express and secrete effector gene products (e.g., glucose oxidase, ATP hydrolyzing enzymes, calcium-binding proteins) into saliva or oral secretions to manipulate/modify host plant nutrients, structure and defense (Simon et al, 2015; Giron et al, 2016; Guiguet et al, 2016; Rivera-Vega et al, 2017; Yang et al, 2017; Basu et al, 2018) as host modification tissues.…”

“…Host plant expansion should require, as in the case of pathogenic bacteria and fungi, expansion of genes responsible for adapting to distinct host plants (e.g., allelochemical-metabolizing enzymes) (Li et al, 2007; Rane et al, 2016; Calla et al, 2017; Bansal and Michel, 2018) and/or modifying host plants (e.g., glucose oxidases and other plant defense-repressing genes) (Simon et al, 2015; Giron et al, 2016; Guiguet et al, 2016; Rivera-Vega et al, 2017; Yang et al, 2017; Basu et al, 2018) and proliferations of non-coding regulatory sequences responsible for regulation of host use related genes. Accordingly, we call insect tissues such as salivary gland and mandibular gland that express and secrete effector gene products (e.g., glucose oxidase, ATP hydrolyzing enzymes, calcium-binding proteins) into saliva or oral secretions to manipulate/modify host plant nutrients, structure and defense (Simon et al, 2015; Giron et al, 2016; Guiguet et al, 2016; Rivera-Vega et al, 2017; Yang et al, 2017; Basu et al, 2018) as host modification tissues. By the same criteria, we name insect tissues that produces genes product to sense/locate host plants (e.g., odorant receptors in antenna), digest plant tissues (digestion enzymes in midgut), and detoxify toxic plant defensive allelochemicals and protease inhibitors (detoxification enzymes in midgut and fat body) (Li et al, 2007; Simon et al, 2015; Rane et al, 2016; Calla et al, 2017; Bansal and Michel, 2018) as host adaptation tissues.…”

Plant Metabolites Drive Different Responses in Caterpillars of Two Closely Related Helicoverpa Species

“…The former is an extreme generalist feeding on at least 161 host plant species in 49 plant families, including cotton, tomato, and tobacco (Zalucki et al, 1986;Fitt, 1989), whereas the latter is a specialist insect species feeding on the Solanaceae and several Physalis species, tobacco, and hot pepper on the natural field (Mitter et al, 1993). The two species could be hybridized to produce viable offspring under laboratory conditions (Wang and Dong, 2001) and are good models to investigate the interaction between plants and herbivorous insects (Tang et al, 2006(Tang et al, , 2014Ahn et al, 2011;Liu et al, 2012;Yang et al, 2017;Zhu et al, 2020).…”

Overproduction of Glucose Oxidase byAspergillus tubingensisCTM 507 Randomly Obtained Mutants and Study of Its Insecticidal Activity againstEphestia kuehniella

“…Several studies reported that GOD from the labial gland of herbivorous insects suppressed infectivity of potential pathogens. It has the capacity to beat a broader range of insect pathogens [13,14]. Through its catalytic product hydrogen peroxide, the labial gland GOD importantly inhibit the direct and indirect plant defenses by attenuating the ethylene and jasmonic acid levels and eliciting the salicylic acid burst [14,15].…”

“…It has the capacity to beat a broader range of insect pathogens [13,14]. Through its catalytic product hydrogen peroxide, the labial gland GOD importantly inhibit the direct and indirect plant defenses by attenuating the ethylene and jasmonic acid levels and eliciting the salicylic acid burst [14,15]. It was demonstrated that GOD from H. zea saliva and Ostrinia nubilalis induced the defense responses in tomato [16].…”