Investigating a role for piRNA-associated <i>piwi</i> genes in overcoming host-plant resistance in the soybean aphid, <i>Aphis glycines</i>

Natural host-plant resistance provides a sustainable solution to control insect outbreaks but can be limited due to insect counter-adaptation. The exact mechanisms of insect adaptation to host-plant resistance remain unclear in most systems. Some insect adaptations are controlled by epigenetic mechanisms, such as through noncoding RNA. PIWI-interacting RNAs are specific noncoding RNAs that bind with PIWI proteins to control a diverse range of gene regulatory functions, particularly in insects. Previous investigation into aphid PIWI gene copies showed expansion in their abundance compared to other insects, which may suggest PIWI genes have additional functions among aphids. We first characterized PIWI gene evolution through a phylogenetic analysis, then investigated the role of PIWIs by examining gene expression in the soybean aphid (Aphis glycines), a significant insect pest of soybean which has adapted to overcome aphid-resistance in host plants. Our data indicated the presence of three PIWI ortholog groups, as well as taxon-specific gene expansions, with gene copy numbers ranging from 3 to 17 across species. To evaluate a potential role of PIWIs in overcoming host-plant resistance, we measured their gene expression in Ap. glycines with (virulent) and without (avirulent) the ability to survive on aphid-resistant soybean. We found that virulent Ap. glycines have significantly higher expression of 2 PIWI genes (Agl1.1 and Agl1.3) compared to the avirulent biotype. These data suggest that gene regulatory mechanisms related to the PIWI pathway, potentially including piRNAs, are important in aphid systems and may enable adaptation to host-plant resistance.