Dichotomous Role of Jasmonic Acid in Modulating Sorghum Defense Against Aphids

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

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/7/2022
Publication Date: 9/22/2022
Citation: Grover, S., Puri, H., Xin, Z., Sattler, S.E., Louis, J. 2022. Genetic analysis of seed traits in Sorghum bicolor that affect the human gut microbiome. Molecular Plant-Microbe Interactions. 35(9):755-767. https://doi.org/10.1094/MPMI-01-22-0005-R.
DOI: https://doi.org/10.1094/MPMI-01-22-0005-R

Interpretive Summary: The sugarcane aphid is a major threat to U.S. sorghum production. There are several sorghum lines resistance to this pest, but the mechanisms that protect these plants are unknown. The plant defense hormone, jasmonic acid (JA) was investigated as a potential factor involved in sorghum resistance to the sugarcane aphid. JA was increased at early stages of aphid feeding and deterred aphid settling in the resistant sorghum line SC265. Monitoring of aphid feeding behavior showed that SC265 plants restricted aphid feeding from the phloem sap. However, application of additional JA to plants decreased their resistant and promoted aphid feeding and colonization on SC265 plants. JA-deficient sorghum confirmed these findings, in which lack of JA promoted aphid settling, however, it also reduced aphid feeding from the phloem sap and reduced the aphid population. The applications of JA to JA-deficient plants caused enhanced feeding and aphid proliferation. These findings underscore a previously unknown dichotomous role of JA, which may have opposing effects by deterring aphid settling upon leaves and stalks during early stages of aphid colonization and enhance aphid reproduction during later-stages on sorghum plants. Sorghum plants able to pivot JA production from high initial level at early stage of aphid infestation to lower ones at later stages may be critical for sugarcane aphid resistance.

Technical Abstract: 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 Zehntner), which is considered a major threat to sorghum production, remains elusive. Here, we provide several lines of evidence that JA has an unexpected dichotomous role in modulating sorghum defense against SCA. 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. Furthermore, our results suggest that JA depletion-mediated SCA resistance is disengaged with JA’s antagonistic effect on salicylic acid pathway. Thus, our findings underscore a previously unknown dichotomous role of JA, which may have opposing effects by deterring aphid settling during early stage and enhancing aphid’s proliferative capacity during later-stages of aphid colonization on sorghum plants.