Unveiling diurnal rhythmicity: Gene expression patterns and impact on aphid fitness and plant interactions

The alternating day-night cycles as a result of the Earth's rotation have profound effects on all living organisms, leading to the development of internal circadian clocks that govern ~24-hour patterns in physiology, metabolism, and behavior. Synchronizing the internal circadian clock with environmental cues provides organisms with a significant fitness advantage, ensuring that vital biological activities occur at optimal times. In insects, the diurnal rhythm greatly influences behaviors and physiological aspects such as movement, growth, feeding, and reproduction. To explore the diurnal rhythmicity of genes in the bird cherry-oat aphid (Rhopalosiphum padi), a notable pest and vector of the barley yellow dwarf virus, we conducted a diurnal time-course experiment to monitor the global gene expressions in R. padi at 4-hour intervals over a diel cycle. Our study revealed a total of 4,460 rhythmic transcripts in the whole-body aphids, which were further classified into four major gene clusters based on their temporal expression patterns. Additionally, we identified putative salivary effectors (264) in the whole-body R. padi by comparing them to a previously curated dataset of R. padi salivary effector sequences. Among these putative effectors, 42 exhibited rhythmic expression, with some notably showing heightened expression during the nighttime. Perturbing the diurnally rhythmic osmoregulatory and salivary effector genes by RNA interference had a significant impact on aphid mortality, fecundity, and feeding behavior. This study contributes to an improved understanding of diurnal cycle-driven dynamics in the interactions between phloem-feeding insects and their host plants.