Dataset Information

Transcriptomic Plasticity in the Arthropod Generalist Tetranychus urticae Upon Long-Term Acclimation to Different Host Plants.

ABSTRACT: The two-spotted spider mite Tetranychus urticae is an important pest with an exceptionally broad host plant range. This generalist rapidly acclimatizes and adapts to a new host, hereby overcoming nutritional challenges and a novel pallet of constitutive and induced plant defenses. Although recent studies reveal that a broad transcriptomic response upon host plant transfer is associated with a generalist life style in arthropod herbivores, it remains uncertain to what extent these transcriptional changes are general stress responses or host-specific. In the present study, we analyzed and compared the transcriptomic changes that occur in a single T. urticae population upon long-term transfer from Phaseolus vulgaris to a similar, but chemically defended, host (cyanogenic Phaseolus lunatus) and to multiple economically important crops (Glycine max, Gossypium hirsutum, Solanum lycopersicum and Zea mays). These long-term host plant transfers were associated with distinct transcriptomic responses with only a limited overlap in both specificity and directionality, suggestive of a fine-tuned transcriptional plasticity. Nonetheless, analysis at the gene family level uncovered overlapping functional processes, recruiting genes from both well-known and newly discovered detoxification families. Of note, our analyses highlighted a possible detoxification role for Tetranychus-specific short-chain dehydrogenases and single PLAT domain proteins, and manual genome annotation showed that both families are expanded in T. urticae Our results shed new light on the molecular mechanisms underlying the remarkable adaptive potential for host plant use of generalist arthropods and set the stage for functional validation of important players in T. urticae detoxification of plant secondary metabolites.

SUBMITTER: Snoeck S

PROVIDER: S-EPMC6288829 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Transcriptomic Plasticity in the Arthropod Generalist <i>Tetranychus urticae</i> Upon Long-Term Acclimation to Different Host Plants.

Snoeck Simon S Wybouw Nicky N Van Leeuwen Thomas T Dermauw Wannes W

G3 (Bethesda, Md.) 20181210 12

The two-spotted spider mite <i>Tetranychus urticae</i> is an important pest with an exceptionally broad host plant range. This generalist rapidly acclimatizes and adapts to a new host, hereby overcoming nutritional challenges and a novel pallet of constitutive and induced plant defenses. Although recent studies reveal that a broad transcriptomic response upon host plant transfer is associated with a generalist life style in arthropod herbivores, it remains uncertain to what extent these transcri ...[more]

PMID: 30333191

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Project description:The extreme adaptation potential of the generalist herbivore Tetranychus urticae (the two-spotted spider mite) to pesticides as well as diverse host plants has been associated with clade-specific gene expansions in known detoxifying enzyme families, and with extensive and rapid transcriptional responses. However, how this broad transcriptional potential is regulated remains largely unknown. Using a parental/F1 design in which four inbred strains were crossed to a common inbred strain, we assessed the genetic basis and inheritance of gene expression variation in T. urticae. Mirroring known phenotypic variation in the progenitor strains of the inbreds, we confirmed that the inbred strains we created were genetically distinct, varied markedly in pesticide resistance, and also captured variation in host plant fitness as is commonly observed in this species. By examining differences in gene expression between parents and allele-specific expression in F1s, we found that variation in RNA abundance was more often explained in trans as compared to cis, with the former associated with dominance in inheritance. Strikingly, in a gene ontology analysis, detoxification genes of the cytochrome P450 monooxygenase (CYP) family, as well as dioxygenases (DOGs) acquired from horizontal gene transfer from fungi, were specifically enriched at the extremes of trans-driven up- and downregulation. In particular, multiple CYPs and DOGs with broad substrate-specificities for pesticides or plant specialized compounds were exceptionally highly upregulated as a result of trans-regulatory variation, or in some cases synergism of cis and trans, in the most multi-pesticide resistant strains. Collectively, our findings highlight the potential importance of trans-driven expression variation in genes associated with xenobiotic metabolism and host plant use for rapid adaptation in T. urticae, and also suggests modular control of these genes, a regulatory architecture that might ameliorate negative pleiotropic effects.

Project description:Diapause is a common feature in several arthropod species that are subject to unfavorable growing seasons. The range of environmental cues that trigger the onset and termination of diapause, in addition to associated hormonal, biochemical, and molecular changes, have been studied extensively in recent years; however, such information is only available for a few insect species. Diapause and cold hardening usually occur together in overwintering arthropods, and can be characterized by recording changes to the wealth of molecules present in the tissue, hemolymph, or whole body of organisms. Recent technological advances, such as high throughput screening and quantification of metabolites via chromatographic analyses, are able to identify such molecules. In the present work, we examined the survival ability of diapausing and non-diapausing females of the two-spotted spider mite, Tetranychus urticae, in the presence (0 or 5°C) or absence of cold acclimation. Furthermore, we examined the metabolic fingerprints of these specimens via gas chromatography-mass spectrophotometry (GC-MS). Partial Least Square Discriminant Analysis (PLS-DA) of metabolites revealed that major metabolic variations were related to diapause, indicating in a clear cut-off between diapausing and non-diapausing females, regardless of acclimation state. Signs of metabolic depression were evident in diapausing females, with most amino acids and TCA cycle intermediates being significantly reduced. Out of the 40 accurately quantified metabolites, seven metabolites remained elevated or were accumulated in diapausing mites, i.e. cadaverine, gluconolactone, glucose, inositol, maltose, mannitol and sorbitol. The capacity to accumulate winter polyols during cold-acclimation was restricted to diapausing females. We conclude that the induction of increased cold hardiness in this species is associated with the diapause syndrome, rather than being a direct effect of low temperature. Our results provide novel information about biochemical events related to the cold hardening process in the two-spotted spider mite.

Dataset Information

Transcriptomic Plasticity in the Arthropod Generalist Tetranychus urticae Upon Long-Term Acclimation to Different Host Plants.

Publications

Transcriptomic Plasticity in the Arthropod Generalist <i>Tetranychus urticae</i> Upon Long-Term Acclimation to Different Host Plants.

Similar Datasets

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