Rapid specialization of counter defenses enables two-spotted spider mite to adapt to novel plant hosts

Abstract

Genetic adaptation, occurring over a long evolutionary time, enables host-specialized herbivores to develop novel resistance traits and to efficiently counteract the defenses of a narrow range of host plants. In contrast, physiological acclimation, leading to the suppression and/or detoxification of host defenses, is hypothesized to enable broad-generalists to shift between plant hosts. However, the host adaptation mechanisms used by generalists composed of host-adapted populations are not known. Two-spotted spider mite (Tetranychus urticae) is an extreme generalist herbivore whose individual populations perform well only on a subset of potential hosts. We combined experimental evolution, Arabidopsis thaliana genetics, mite reverse genetics, and pharmacological approaches to examine mite host adaptation upon the shift of a bean (Phaseolus vulgaris)-adapted population to Arabidopsis. We showed that cytochrome P450 monooxygenases are required for mite adaptation to Arabidopsis. We identified activities of two tiers of P450s: general xenobiotic-responsive P450s that have a limited contribution to mite adaptation to Arabidopsis and adaptation-associated P450s that efficiently counteract Arabidopsis defenses. In ∼25 generations of mite selection on Arabidopsis plants, mites evolved highly efficient detoxification-based adaptation, characteristic of specialist herbivores. This demonstrates that specialization to plant resistance traits can occur within the ecological timescale, enabling the two-spotted spider mite to shift to novel plant hosts.

β-Cyanoalanine synthase protects mites against Arabidopsis defenses

“…Tetranychus urticae is an example of a composite generalist herbivore whose individual populations perform well only on a subset of potential hosts ( Fellous et al, 2014 ; Rioja et al, 2017 ). However, mites have an ability to adapt to originally unfavorable hosts in just 5–25 generations and overcome initially effective plant host defenses ( Gould, 1979 ; Fry, 1989 ; Magalhaes et al, 2007 ; Wybouw et al, 2015 ; Salehipourshirazi et al, 2021) . The expansion of gene families implicated in digestion, detoxification, and transport of xenobiotics and their dynamic expressional changes when mites shift to new plant hosts indicate that mites, like other generalist herbivores, can quickly reprogram their xenobiotic responses ( Grbic et al, 2011 ; Herde and Howe, 2014 ; Schweizer et al, 2017 ; Salehipourshirazi et al, 2021) .…”

“…However, mites have an ability to adapt to originally unfavorable hosts in just 5–25 generations and overcome initially effective plant host defenses ( Gould, 1979 ; Fry, 1989 ; Magalhaes et al, 2007 ; Wybouw et al, 2015 ; Salehipourshirazi et al, 2021) . The expansion of gene families implicated in digestion, detoxification, and transport of xenobiotics and their dynamic expressional changes when mites shift to new plant hosts indicate that mites, like other generalist herbivores, can quickly reprogram their xenobiotic responses ( Grbic et al, 2011 ; Herde and Howe, 2014 ; Schweizer et al, 2017 ; Salehipourshirazi et al, 2021) . The detoxification potential of mites is enriched with genes that have been acquired through horizontal gene transfer ( Wybouw et al, 2018 ).…”

“…Arabidopsis is a nonhost plant to the reference London mite population ( Grbic et al, 2011 ; Zhurov et al, 2014 ; Santamaría et al, 2017 , 2019 ; Salehipourshirazi et al, 2021 ; Widemann et al, 2021) . At least two classes of jasmonic acid (JA)-regulated defenses protect Arabidopsis plants against mite herbivory ( Figure 1A ; Salehipourshirazi et al, 2021 ; Widemann et al, 2021 ). Trp-derived indole glucosinolates are one class of defensive compounds ( Widemann et al, 2021) .…”

“…Their identity is currently not known. We recently demonstrated that a reference London bean-reared ( Phaseolus vulgaris ) mite population can adapt to Arabidopsis ( Salehipourshirazi et al, 2021) . In these experiments, London mites were selected on Columbia-0 (Col-0) fully defended wild-type (WT) plants, and cyp79b2 cyp79b3 ( CYTOCHROME P450 , FAMILY 79 , SUBFAMILY B , POLYPEPTIDE 2 and 3 , AT4G39950 , and AT2G22330 ) plants that are deficient in conversion of Trp to indole-3-acetaldoxime (IAOx), lack Trp-derived compounds but display the remaining JA-regulated defenses, resulting in Col-a and cyp -a mite populations, respectively ( Figure 1A ).…”

Effect of Neo-Boost Pesticide on Mortality and Development of Different Life Stages of Two-Spotted Spider Mite, Tetranychus urticae

“…It was also implicated in priming jasmonic acid-plant induced defense responses (Sakr, 2017). As jasmonic acid is a general inducer of plant defenses against herbivores (Pieterse et al, 2012) including spider mites (Li et al, 2002;Zhurov et al, 2014;Salehipourshirazi et al, 2021;Widemann et al, 2021), Si in the Neo-Boost formulation may contribute to plant resistance against a wide range of herbivores.…”