Temporal transcriptomic profiling elucidates sorghum defense mechanisms against sugarcane aphids

The sugarcane aphid (SCA; Melanaphis sacchari) has emerged as a key pest on sorghum in the United States that feeds from the phloem tissue, drains nutrients, and inflicts physical damage to plants. Previously, it has been shown that SCA reproduction was low and high on sorghum SC265 and SC1345 plants, respectively, compared to RTx430, an elite sorghum male parental line (reference line). In this study, we focused on identifying the defense-related genes that confer resistance to SCA at early and late time points in sorghum plants with varied levels of SCA resistance.

We used RNA-sequencing approach to identify the global transcriptomic responses to aphid infestation on RTx430, SC265, and SC1345 plants at early time points 6, 24, and 48 h post infestation (hpi) and after extended period of SCA feeding for 7 days. Aphid feeding on the SCA-resistant line upregulated the expression of 3827 and 2076 genes at early and late time points, respectively, which was relatively higher compared to RTx430 and SC1345 plants. Co-expression network analysis revealed that aphid infestation modulates sorghum defenses by regulating genes corresponding to phenylpropanoid metabolic pathways, secondary metabolic process, oxidoreductase activity, phytohormones, sugar metabolism and cell wall-related genes. There were 187 genes that were highly expressed during the early time of aphid infestation in the SCA-resistant line, including genes encoding leucine-rich repeat (LRR) proteins, ethylene response factors, cell wall-related, pathogenesis-related proteins, and disease resistance-responsive dirigent-like proteins. At 7 days post infestation (dpi), 173 genes had elevated expression levels in the SCA-resistant line and were involved in sucrose metabolism, callose formation, phospholipid metabolism, and proteinase inhibitors.

In summary, our results indicate that the SCA-resistant line is better adapted to activate early defense signaling mechanisms in response to SCA infestation because of the rapid activation of the defense mechanisms by regulating genes involved in monolignol biosynthesis pathway, oxidoreductase activity, biosynthesis of phytohormones, and cell wall composition. This study offers further insights to better understand sorghum defenses against aphid herbivory.