Genome scan detection of selective sweeps among biotypes of the soybean aphid, Aphis glycines, with differing virulence to resistance to A. glycines (Rag) traits in soybean, Glycine max

Authors: Coates, Brad; HOHENSTEIN, JESSICA - Iowa State University; GIORDANO, ROSANNA - University Of Illinois; DONTHU, RAVI - Puerto Rico Science, Technology And Research Trust; MICHEL, ANDREW - Iowa State University; HODGSON, ERIN - Iowa State University; ONEAL, MATTHEW - Iowa State University

Submitted to: Insect Biochemistry and Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/18/2020
Publication Date: 4/30/2020
Citation: Coates, B.S., Hohenstein, J.D., Giordano, R., Donthu, R.K., Michel, A.P., Hodgson, E.W., O'Neal, M.E. 2020. Genome scan detection of selective sweeps among biotypes of the soybean aphid, Aphis glycines, with differing virulence to resistance to A. glycines (Rag) traits in soybean, Glycine max. Insect Biochemistry and Molecular Biology. 124. Article 103364. https://doi.org/10.1016/j.ibmb.2020.103364.
DOI: https://doi.org/10.1016/j.ibmb.2020.103364

Interpretive Summary: Soybeans are a major agricultural commodity grown in the United States, but damage caused by the soybean aphid result in reduced plant vigor and grain yield. Moreover, soybean aphids are capable of transmitting plant viruses that further reduce crop yields and producer profits. Biotypes of the soybean aphid have also adapted to survive on soybean varieties with host plant resistance traits that repel aphid feeding. These adaptations represent a threat to sustainable soybean production practices in the United States. Although the genetic basis of aphid adaptations remains unknown, it is known that during feeding these insects secrete a class of proteins, called effectors, into susceptible soybean plants which suppress the plant defensive responses. An ARS researcher led a team of university cooperators to compare nucleotide sequence variation across the entire soybean aphid genome, and in doing so, identified a relatively small number of genome regions that differ greatly between biotypes. Mutations that were different between adapted and non-adapted aphid biotypes were positioned in proximity to protein coding genes, some of which are predicted to be involved in intracellular vesicle transport and protein secretion outside of the cell. The role of these secretory pathway genes in aphid adaptation remains unknown, but their identification provides valuable new insights into the possible mechanism(s) involved in aphid adaptations to soybean plant resistant traits. These results will be of interest to University, Industry and Government scientists involved in investigating the genetic mechanisms insects use to overcome host plant resistance traits, and developing methods to enhance the control of agricultural pest species of aphids.

Technical Abstract: In North America, biotypes of the soybean aphid, Aphis glycines, have adapted for optimal survival (virulence) on cultivars of soybean, Glycine max, with one or more different resistance to A. glycines (Rag) traits. The genomic basis for variation among biotypes remains unknown. Between 167,249 and 217,750 single nucleotide polymorphisms (SNPs) were predicted from whole genome re-sequencing A. glycines avirulent biotype 1 (B1) and virulent B2, B3 and B4-derived iso-female lines when compared to the draft A. glycines B1 genome assembly, Ag_bt1_v6.0. Differences in nucleotide diversity (p) indices estimated within 1,000 bp sliding windows demonstrated that the 237 of 353 (67.4%) regions most differentiated between B1 and = 2 virulent biotypes are located on 15 unordered scaffolds. Overall genome-wide p estimates were low between B2 and B3 compared to either with B4. Annotation of 179 protein coding genes within or in proximity to divergent regions did not show any significant enrichment for functional categories. Regardless, a previously identified secreted endocuticle structural glycoprotein effector coding regions is located in proximity to a genome two adjacent genome intervals with low p estimates in avirulent B1. Additionally, SNPs are clustered in or in proximity to genes putatively involved in intracellular molecular motor activity and regulation of secretion; dynein light chain roadblock 1 (DYNLRB1), and non-muscle myosins, a myosin II regulatory light chain and an unconventional myosin Va. These results indicate that a small number of scaffolds of the A. glycines genome may vary due to directional selection in response to feeding on Rag cultivars