Soybean aphid biotype 1 genome: Insights into the invasive biology and adaptive evolution of a major agricultural pest

Authors: GIORDANO, ROSANNA - Puerto Rico Science, Technology And Research Trust; Hartman, Glen; Avalos, Arian; Coates, Brad; Lagos-Kutz, Doris

Submitted to: Insect Biochemistry and Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/10/2020
Publication Date: 2/25/2020
Citation: Giordano, R., Donthu, R.K., Zimin, A.V., Julca Chavez, I.C., Gabalon, T., van Munster, M., Hon, L., Hall, R., Badger, J.H., Nguyen, M., Flores, A., Potter, B., Giray, T., Sato-Adames, F.N., Weber, E., Marcelino, J. A.P., Fields, C.J., Voegtlin, D.J., Hill, C.B., Hartman, G.L., Akraiko, Ta., Aschwanden, A., Avalos, A., Band, M., Bonning, B., Bretaudeau, A., Chiesa, O., Chirumamilla, A., Coates, B.S., Cocuzza, G., Cullen, E., Desborough, P., Diers, B., DiFonzo, C., Heimpel, G.E., Herman, T., Huanga, Y., Knodel, J., Ko, C., Labrie, G., Lagos-Kutz, D., Lee, J., Lee, S., Legeai, F., Mandriolo, M.,, Manicadi, G.C., Mazzoni, E., Melchiori, G., Micijevic, A., Miller, N., Nasuddin, A., Nault, B.A., O’Neal, M.E, Panini, M., Pessino, M., Prischmann-Voldseth, D., Robertson, H.M., Liu, S., Song, H., Tilmon, K., Tooker, J., Wu, K., Zhan, S. 2020. Soybean aphid biotype 1 genome: Insights into the invasive biology and adaptive evolution of a major agricultural pest. Insect Biochemistry and Molecular Biology. 120:103334. https://doi.org/10.1016/j.ibmb.2020.103334.
DOI: https://doi.org/10.1016/j.ibmb.2020.103334

Interpretive Summary: The Asian soybean aphid is a serious pest of the soybean crop. We assembled a de novo genome sequence of the soybean aphid Biotype 1, from a culture established shortly after this species invaded North America in 2000. Approximately one-third of the genes show parallel duplication to other aphids. Populations of a world-wide collection of soybean aphids were analyzed for their relationships to North American soybean aphids. Soybean aphids from China and South Korean are the closest to those found in North America. China is the likely origin of other Asian soybean aphid populations. The most distantly related soybean aphids to those in North America are from Australia. The soybean aphid Biotype 1 genome sequence will provide needed information for future analyses of mechanisms of aphid virulence and pesticide resistance as well as facilitate comparative analyses between aphids with differing natural history and host plant range. This information is useful to molecular biologists, ecologists, and taxonomists.

Technical Abstract: The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) is a serious pest of the soybean plant, Glycine max, a major world-wide agricultural crop. We assembled a de novo genome sequence of Ap. glycines Biotype 1, from a culture established shortly after this species invaded North America. 20.4% of the Ap. glycines proteome is duplicated. These in-paralogs are enriched with Gene Ontology (GO) categories mostly related to apoptosis, a possible adaptation to plant chemistry and other environmental stressors. Approximately one-third of these genes show parallel duplication in other aphids. But Ap. gossypii, its closest related species, has the lowest number of these duplicated genes. An Illumina GoldenGate assay of 2,380 SNPs was used to determine the world-wide population structure of Ap. Glycines. China and South Korean aphids are the closest to those in North America. China is the likely origin of other Asian aphid populations. The most distantly related aphids to those in North America are from Australia. The diversity of Ap. glycines in North America has decreased over time since its arrival. The genetic diversity of Ap. glycines North American population sampled shortly after its first detection in 2001 up to 2012 does not appear to correlate with geography. However, aphids collected on soybean Rag experimental varieties in MN, IA, and WI, closer to high density Rhamnus cathartica stands, appear to have higher capacity to colonize resistant soybean plants than aphids sampled in OH, ND, and SD. Samples from the former states have SNP alleles with high FST values and frequencies, that overlap with genes involved in iron metabolism, a crucial metabolic pathway that may be affected by the Rag-associated soybean plant response. The Ap. glycines Biotype 1 genome will provide needed information for future analyses of mechanisms of aphid virulence and pesticide resistance as well as facilitate comparative analyses between aphids with differing natural history and host plant range.