Sugarcane aphid (SCA; Melanaphis sacchari Zehntner) is a key piercing-sucking pest of sorghum (Sorghum bicolor) that cause significant yield losses. While feeding on host plants, complex signaling networks are invoked from recognition of insect attack to induction of plant defenses. Consequently, these signaling networks lead to the production of insecticidal compounds or limited access of nutrients to insects. Previously, several studies were published on the transcriptomics analysis of sorghum in response to SCA infestation, but no information is available on the physiological changes of sorghum at the proteome level. We used the SCA resistant sorghum genotype SC265 for the global proteomics analysis after 1 and 7 days of SCA infestation using the TMT-plex technique. Peptides matching a total of 4211 proteins were identified and 158 proteins were differentially expressed at day 1 and 7. Overall, proteome profiling of SC265 after SCA infestation at days 1 and 7 revealed the suppression of plant defense-related proteins and upregulation of plant defense and signaling-related proteins, respectively. The plant defense responses based on proteome data were validated using electrical penetration graph (EPG) technique to observe changes in aphid feeding. Feeding behavior analyses revealed that SCA spent significantly longer time in phloem phase on SCA infested plants for day 1 and lesser time in day 7 SCA infested sorghum plants, compared to their respective control plants. Overall, our study provides insights into underlying mechanisms that contribute to sorghum resistance to SCA.

The precursors and derivatives of jasmonic acid (JA) contribute to plant protective immunity to insect attack. However, the role of JA in sorghum (Sorghum bicolor) defense against sugarcane aphid (SCA) (Melanaphis sacchari), which is considered a major threat to sorghum production, remains elusive. Sorghum SC265, previously identified as a SCA-resistant genotype among the sorghum nested association mapping founder lines, transiently increased JA at early stages of aphid feeding and deterred aphid settling. Monitoring of aphid feeding behavior using electropenetrography, a technique to unveil feeding process of piercing-sucking insects, revealed that SC265 plants restricted SCA feeding from the phloem sap. However, exogenous application of JA attenuated the resistant phenotype and promoted improved aphid feeding and colonization on SC265 plants. This was further confirmed with sorghum JA-deficient plants, in which JA deficiency promoted aphid settling, however, it also reduced aphid feeding from the phloem sap and curtailed SCA population. Exogenous application of JA caused enhanced feeding and aphid proliferation on JA-deficient plants, suggesting that JA promotes aphid growth and development. SCA feeding on JA-deficient plants altered the sugar metabolism and enhanced the levels of fructose and trehalose compared with wild-type plants. Furthermore, aphid artificial diet containing fructose and trehalose curtailed aphid growth and reproduction. Our findings underscore a previously unknown dichotomous role of JA, which may have opposing effects by deterring aphid settling during the early stage and enhancing aphid proliferative capacity during later stages of aphid colonization on sorghum plants. [Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.