Molecular basis governing diapause and pigmentation in the hawthorn spider mite, Amphitetranychus viennensis.

Background: Diapause is a physiological adaptation that evolves in arthropods to cope with unfavorable environmental conditions. By synchronizing their development and reproduction to seasonal variations, these animals can maximize their odds to survive adverse conditions. Among the environmental cues that trigger diapause, photoperiod is the most extensively studied. The hawthorn spider mite, Amphitetranychus viennensis, is one of the most devastating arthropod pests in fruit trees and woody ornamental plants. Overwintering females undergo a reproductive facultative diapause when A. viennensis immatures are exposed to long nights, which is consistent with the two-spotted spider mite, Tetranychus urticae. However, the molecular mechanisms underlying diapause in A. viennensis remain unexplored.

Results: Here, we first developed a photoperiodic diapause bioassay for A. viennensis and identified protochrysalis, a non-feeding resting stage between the larva and protonymph, as a crucial developmental stage for diapause induction. We then identified six genes related to the carotenoid pathway, including three involved in synthesis, AvPD, AvLC/PS1, and AvLC/PS2, and the other three associated with metabolism, AvBCO1, AvBCO2, and AvCYP384A1. Phylogenetic analysis suggested that AvPD, AvLC/PS1, and AvLC/PS2 were acquired through horizontal transfer from fungi. Finally, functional characterization using RNA interference (RNAi) demonstrated that AvPD, AvLC/PS1, AvBCO2, and AvCYP384A1 contribute to pigmentation, while AvPD, AvLC/PS1, and AvBCO1 are involved in the regulation of diapause in A. viennensis.

Conclusions: This study not only advances our current knowledge on the molecular basis governing pigmentation and diapause, but also sheds light on the development of long-term sustainable management strategies for these polyphagous herbivores in spider mites in general and A. viennensis in particular.