A sorghum genome-wide association study (GWAS) identifies a WRKY transcription factor as a candidate gene underlying sugarcane aphid (Melanaphis sacchari) resistance

Authors: POOSAPATI, SOWMYA - University Of California, San Diego; PORETSKY, ELLY - University Of California, San Diego; DRESSANO, KEINI - University Of California, San Diego; RUIZ, MIGUEL - University Of California, San Diego; VAZQUEZ, ARMANDO - University Of California, San Diego; SANDOVAL, EVAN - University Of California, San Diego; ESTRADA-CARDENAS, ADELAIDA - University Of California, San Diego; DUGGAL, SARTHAK - University Of California, San Diego; LIM, JIA-HUI - University Of California, San Diego; MORRIS, GEOFFREY - Colorado State University; SZCZEPANIEC, ADRIANNA - Colorado State University; Walse, Spencer; Ni, Xinzhi; SCHMELZ, ERIC - University Of California, San Diego; HUFFAKER, ALISA - University Of California, San Diego

Submitted to: Planta
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/19/2021
Publication Date: 1/12/2022
Citation: Poosapati, S., Poretsky, E., Dressano, K., Ruiz, M., Vazquez, A., Sandoval, E., Estrada-Cardenas, A., Duggal, S., Lim, J., Morris, G., Szczepaniec, A., Walse, S.S., Ni, X., Schmelz, E.A., Huffaker, A. 2022. A sorghum genome-wide association study (GWAS) identifies a WRKY transcription factor as a candidate gene underlying sugarcane aphid (Melanaphis sacchari) resistance. Planta. 255. Article 37. https://doi.org/10.1007/s00425-021-03814-x.
DOI: https://doi.org/10.1007/s00425-021-03814-x

Interpretive Summary: The sugarcane aphid has been long appreciated to not infest on sorghum plants; however, since 2013 a specific predominant sugarcane aphid clone became an aggressive pest on grain sorghum in the United States. As a threat to sorghum production, the invasive sugarcane aphid infestation has caused great yield and economic losses in recent years. Developing new resistant crop varieties is one of the most effective strategies for managing an invasive pest outbreak. To identify new genetic sources and accelerate developing new sorghum germplasm lines with sugarcane aphid resistance, we undertook a large experiment to link sugarcane aphid damage levels with gene candidates. A total of 796 sorghum germplasm lines with extensive genotype data were evaluated for sugarcane aphid resistance under the field conditions, and then four representative germplasm lines were further evaluated under the greenhouse conditions. In the current study we identified a transcription factor as a gene candidate on chromosome 9 that is significantly associated with sugarcane aphid resistance in sorghum. The finding from the current study is different from previous reports of a cluster of genes on chromosome 6 that confers aphid resistance in sorghum.

Technical Abstract: Crop plant resistance to insect pests is based on genetically encoded traits which often display variability across diverse germplasm. In a comparatively recent event, a predominant sugarcane aphid (SCA: Melanaphis sacchari) clone has become a significant agronomic pest for grain sorghum (Sorghum bicolor) production. In an effort to uncover candidate genes underlying SCA resistance, we used a forward genetics approach combining the genetic diversity present in the Sorghum Association Panel (SAP) and the Bioenergy Association Panel (BAP) for a Genome Wide Association Study, employing an established SCA damage rating. Statistically significant single nucleotide polymorphisms were found on Chromosome 9 within the WRKY transcription factor 86 (SbWRKY86). Transcripts encoding SbWRKY86 were previously identified as upregulated in SCA-resistant germplasm and the syntenic ortholog in maize accumulates following Rhopalosiphum maidis infestation. Analyses of SbWRKY86 transcript levels displayed elevated levels in additional SCA resistant sorghum lines. Heterologous expression of SbWRKY86 in both tobacco (Nicotiana benthamiana) and Arabidopsis resulted in reduced population growth of green peach aphid (Myzus persicae). Comparative RNA-Seq analyses of Arabidopsis lines expressing 35S:SbWRKY86-YFP identified changes in expression for a small network of genes associated with carbon-nitrogen metabolism and callose deposition, both contributing factors to defense against aphids. As a test of altered plant responses, 35S:SbWRKY86 Arabidopsis lines were activated using the flagellin epitope elicitor, flg22, and displayed significantly increased in callose deposition. Our findings indicate that both heterologous and increased native expression of the transcription factor SbWRKY86 is associated with reduced aphid levels in diverse plant models.