Transcriptome profiling reveals differential gene expression of detoxification enzymes in a hemimetabolous tobacco pest after feeding on jasmonate-silenced Nicotiana attenuata plants

Abstract

BackgroundThe evolutionary arms race between plants and insects has driven the co-evolution of sophisticated defense mechanisms used by plants to deter herbivores and equally sophisticated strategies that enable phytophagous insects to rapidly detoxify the plant’s defense metabolites. In this study, we identify the genetic determinants that enable the mirid, Tupiocoris notatus, to feed on its well-defended host plant, Nicotiana attenuata, an outstanding model for plant-insect interaction studies.ResultsWe used an RNAseq approach to evaluate the global gene expression of T. notatus after feeding on a transgenic N. attenuata line which does not accumulate jasmonic acid (JA) after herbivory, and consequently accumulates very low levels of defense metabolites. Using Illumina sequencing, we generated a de novo assembled transcriptome which resulted in 63,062 contigs (putative transcript isoforms) contained in 42,610 isotigs (putative identified genes). Differential expression analysis based on RSEM-estimated transcript abundances identified 82 differentially expressed (DE) transcripts between T. notatus fed on wild-type and the defenseless plants. The same analysis conducted with Corset-estimated transcript abundances identified 59 DE clusters containing 85 transcripts. In both analyses, a larger number of DE transcripts were found down-regulated in mirids feeding on JA-silenced plants (around 70%). Among these down-regulated transcripts we identified seven transcripts possibly involved in the detoxification of N. attenuata defense metabolite, specifically, one glutathione-S-transferase (GST), one UDP-glucosyltransferase (UGT), five cytochrome P450 (P450s), and six serine proteases. Real-time quantitative PCR confirmed the down-regulation for six transcripts (encoding GST, UGT and four P450s) and revealed that their expression was only slightly decreased in mirids feeding on another N. attenuata transgenic line specifically silenced in the accumulation of diterpene glycosides, one of the many classes of JA-mediated defenses in N. attenuata.ConclusionsThe results provide a transcriptional overview of the changes in a specialist hemimetabolous insect associated with feeding on host plants depleted in chemical defenses. Overall, the analysis reveals that T. notatus responses to host plant defenses are narrow and engages P450 detoxification pathways. It further identifies candidate genes which can be tested in future experiments to understand their role in shaping the T. notatus-N. attenuata interaction.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3348-0) contains supplementary material, which is available to authorized users.

iTRAQ‐based quantitative proteome revealed metabolic changes of Sitophilus zeamais in response to terpinen‐4‐ol fumigation

“…Upregulated P450s and GSTs were mainly from the CYP6 and GST epsilon families, which are tightly associated with xenobiotic metabolism and insecticide resistance . P450s and GSTs participate in xenobiotic metabolism at two different phases and usually function cooperatively: P450s catalyze phase I reactions by increasing the molecule's hydrophilicity, and GSTs participate in phase II reactions, acting on the products of phase I reactions . P450s and GSTs in DEPs likely provide important detoxification mechanisms for terpinen‐4‐ol in stored‐grain insects.…”

Effects of terpinen‐4‐ol fumigation on protein levels of detoxification enzymes in Tribolium confusum

“…Moreover, GSTs and UGTs were upregulated in T. confusum exposed to terpinen‐4‐ol. GSTs attend Phase II reactions in xenobiotic metabolism and usually function cooperatively with P450s (Crava, Brutting, & Baldwin, ). UGTs catalyze the transfer of glucuronic acid to lipophilic molecules to further increase the compound's water solubility for later excretion or sequestration in Phase II reactions (Crava et al, ; Okazaki & Katayama, ).…”

“…GSTs attend Phase II reactions in xenobiotic metabolism and usually function cooperatively with P450s (Crava, Brutting, & Baldwin, ). UGTs catalyze the transfer of glucuronic acid to lipophilic molecules to further increase the compound's water solubility for later excretion or sequestration in Phase II reactions (Crava et al, ; Okazaki & Katayama, ). UGTs were considered to detoxify xenobiotics including insecticides and participate in insecticide resistance (Lv et al, ; Reid, Zhang, Liu, & Liu, ).…”

“…Moreover, GSTs and UGTs were upregulated in T. confusum exposed to terpinen-4-ol. GSTs attend Phase II reactions in xenobiotic metabolism and usually function cooperatively with P450s (Crava, Brutting, & Baldwin, 2016 (Lv et al, 2016;Reid, Zhang, Liu, & Liu, 2012). The upregulation of GSTs and UGTs indicated their potential participation in the water solubilization and excretion of terpinen-4-ol in pests.…”

Transcriptomics of monarch butterflies (Danaus plexippus) reveals strong differential gene expression in response to host plant toxicity, but weak response to parasite infection

“…For instance, Drosophila mettleri, a 417 fruit fly species specialized on cacti with toxic alkaloids, differentially expresses several 418 detoxification genes, including P450s, UGTs, GST, and carboxylesterases, when feeding on 419 different food sources(Hoang, Matzkin, & Bono, 2015). Tupiocoris notatus, a mirid species, down-420 regulates several GST, UGT, and P450s when feeding on defenseless (JA-silenced) Nicotiana 421 attenuata(Crava, Brütting, & Baldwin, 2016). Similarly, our results demonstrate differences in 422 transcriptional profiles of monarch larvae feeding on different milkweed species.…”