Diurnal rhythmicity in salivary effector expression and metabolism shapes aphid performance on wheat plants

Abstract

AbstractDiurnal rhythms influence insect behavior and physiology, driving adaptive responses and synchronizing internal processes with daily light-dark cycles. Aphids are important agricultural pests that feed from phloem sieve elements for prolonged periods by delivering a diverse array of salivary effectors to modulate plant responses. Here, we show that the bird cherry-oat aphid (Rhopalosiphum padi), an important pest of cereals worldwide, expresses different putative salivary effectors at different times of the day, which may, in part, aid with wheat (Triticum aestivum) host colonization. We recorded aphid feeding with the electrical penetration graph (EPG) technique, which revealed diurnal patterns in aphid feeding, particularly extended phloem salivation occurring during early nighttime. Although no diurnal rhythms were detected for phloem sap ingestion, higher honeydew excretion was observed at night. Temporal aphid transcriptome profiles revealed 4,460 diurnally rhythmic transcripts, categorized into four distinct expression clusters linked to various metabolic pathways. Significantly, we identified distinct combinations of putative salivary effectors expressed at different times. Notably, 43% peaked in expression during early nighttime, aligning with the heightened nighttime salivation observed in the aphids using the EPG technique. Silencing key effector genes, which peak in expression at night, impaired aphid feeding and performance on wheat plants without impacting aphid performance on diets. Our study highlights aphid feeding behavior and performance as tightly linked to and influenced by the diurnal expression of salivary effectors and provides the first insights into diurnal feeding behaviors in aphids, revealing opportunities for targeted pest control strategies based on disrupting these rhythms.Significance StatementAphids are among the most destructive pests on crops, threatening food security worldwide. While diurnal rhythms in crops and their aphid pests have been briefly explored, our understanding of how these rhythms ultimately shape the plant-aphid relationship is unknown. Here, we report for the first time that aphids exhibit diurnal rhythms in feeding behaviors, salivary effector expression, and metabolism. A broadened understanding of the presence and role of diurnal rhythms in aphids offers new insights into how behavioral and molecular factors influence the plant-aphid relationship. This temporal insight into aphid biology has the potential to aid in the development of targeted pest management strategies that disrupt an aphid’s interaction with its host, thereby minimizing crop damage and yield loss.