Temporal transcriptomic profiling elucidates sorghum defense mechanisms against sugarcane aphids

Authors: PURI, HEENA - University Of Nebraska; GROVER, SAJJAN - University Of Nebraska; PINGAULT, LISE - University Of Nebraska; Sattler, Scott; LOUIS, JOE - University Of Nebraska

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/22/2023
Publication Date: 8/5/2023
Citation: Puri, H., Grover, S., Pingault, L., Sattler, S.E., Louis, J. 2023. Temporal transcriptomic profiling elucidates sorghum defense mechanisms against sugarcane aphids. BMC Genomics. 24:441. https://doi.org/10.1186/s12864-023-09529-5.
DOI: https://doi.org/10.1186/s12864-023-09529-5

Interpretive Summary: The sugarcane aphid (SCA) has emerged as a key pest on sorghum in the United States, which drains nutrients and inflicts physical damage to sorghum plants. Previously, it has been shown that SCA reproduction was low on SC265 (resistant) and high on SC1345 (susceptible) sorghums compared to RTx430 sorghum (intermediate), a common reference line. In this study, sorghum defense responses to SCA were examined using a technique called RNA-seq to analyze gene expression to discover the responses involved in aphid resistance. The responses to the aphids were examined RTx430, SC265, and SC1345 after 6, 24, 48 hours and 7 days exposure to aphid feeding. Aphid feeding altered the expression of genes in a wide range of sorghum biochemical pathways, which include defense compounds and plant hormones. The earliest responses included genes encodings a class of protein known to detect attacks by other organism such as insects. The late responses included genes whose products function in sugar metabolism and a cell wall-based defense that impedes aphid feeding. In summary, these results indicated that the resistant sorghum SC265 is better adapted to activate early defense signals upon exposure to SCA than the other two sorghums RTx430 and SC1345. This study offers further insights into potential ways to protect sorghum from aphids through improving its own defenses.

Technical Abstract: Background 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. Results 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. Conclusions 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.