WRKY transcription factors are involved in defense responses caused by biotic stresses. Phylloxera (Daktulosphaira vitifoliae Fitch), a pest widespread in viticulture, elicits transcriptional reprogramming of plant defense-associated components, such as regulons related to WRKYs and salicylic acid (SA) signaling. In this study, we characterized WRKY46, a WRKY transcription factor responsible for phylloxera attack, and revealed the molecular mechanism for WRKY-mediated defense responses to phylloxera. qRT-PCR and GUS staining analyses revealed that WRKY46 is induced in response to phylloxera damage and mechanical wounding. VvWRKY46 is a nuclear-localized transcription factor that activates its downstream target VvCHIB by direct protein–DNA interaction. Regulons involved in the SA-mediated defense response were regulated during incompatible interactions between “1103 Paulsen” rootstock and phylloxera. In addition, WRKY46 exhibited a higher transcript abundance in “1103 Paulsen” than in “Crimson Seedless”, regardless of whether the plants were infected with phylloxera. Furthermore, the enhanced expression of VvWRKY46 significantly attenuated phylloxera attack and delayed nymph development of composite grape plants. In summary, we demonstrated that WRKY46 plays a role in the SA-mediated defense-regulatory network by directly binding to the downstream structural gene VvCHIB. The phylloxera-responsive gene WRKY46 was identified, which could improve the understanding of the basic mechanism of grapevine in response to phylloxera.

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