Identification of candidate host-manipulating effector genes in Aphis gossypii (Hemiptera: Aphididae) using a combination of transcriptome, genome, and differential gene expression data

Authors: Zhao, Chaoyang; MUELLER, NICHOLAS - Auburn University; OWENS, ISABELLA - Auburn University; Bansal, Raman; JACOBSON, ALANA - Auburn University

Submitted to: Journal of Insect Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/16/2025
Publication Date: 5/29/2025
Citation: Zhao, C., Mueller, N., Owens, I., Bansal, R., Jacobson, A.L. 2025. Identification of candidate host-manipulating effector genes in Aphis gossypii (Hemiptera: Aphididae) using a combination of transcriptome, genome, and differential gene expression data. Journal of Insect Science. 25(3):11. https://doi.org/10.1093/jisesa/ieaf053.
DOI: https://doi.org/10.1093/jisesa/ieaf053

Interpretive Summary: The cotton aphid is a widespread agricultural pest that transmits numerous plant diseases and feeds on a variety of plants. During feeding, the aphid's salivary glands produce secretory proteins, which are key components of aphid saliva that facilitate the transmission of plant viruses and the colonization of host plants. Using a bioinformatics approach that combines different types of genetic data, researchers identified 351 genes that might be involved in these processes. Further analyses revealed that some of these genes matched aphid saliva proteins found in previous studies, and certain genes showed higher activity in specific body parts and life stages of the aphids. This suggests that these genes play crucial roles in helping aphids adapt to new host plants. Overall, this research highlights key genes that may facilitate the colonization of cotton aphids on their host plants, providing valuable insights into their complex interactions.

Technical Abstract: The cotton aphid, Aphis gossypii, is an important plant disease vector and a highly polyphagous agricultural pest that feeds on a broad range of host plants. During feeding, its salivary glands serve as a route for the transmission of circulative plant viruses and produce a range of secretory proteins, called effectors, to modulate host cellular processes. To understand the molecular mechanisms underlying aphid-plant interactions, we developed a bioinformatics pipeline that incorporated the salivary gland transcriptome, genome, and head vs. abdomen differential gene expression data to predict secretory protein-encoding genes enriched in the salivary glands of A. gossypii. Annotation of the 351 predicted genes showed that the most abundant functional categories were associated with cellular signaling and metabolism processes, and revealed that 98 genes were hemipteran-specific. Notably, 51 genes encode secretory proteins matching the putative saliva proteins identified in prior proteomics studies. Quantitative PCR analysis validated differential expression of four selected genes between heads and abdomens and indicated that alate adults exhibited the highest gene expression, suggesting these genes may play key roles in host colonization. Additionally, 25 genes showed sequence similarities to functionally characterized hemipteran effectors, with some appearing to form effector groups with distinct evolutionary patterns. Collectively, this study identified numerous putative plant-manipulating genes in A. gossypii and provided valuable insights into the mechanisms of aphid-plant interactions.