Disruption of the sorghum circadian clock impacts sorghum-sugarcane aphid interaction dynamics and aphid feeding behavior

Abstract

Circadian clocks play a pivotal role in orchestrating metabolic rhythms in response to environmental stress. Sorghum bicolor (sorghum), a multipurpose cereal crop, suffers severe growth and yield reduction due to feeding by sugarcane aphids (SCA; Melanaphis sacchari), which are phloem-feeding pests. Previously, it has been shown that sorghum utilizes a multitude of defense mechanisms to curb SCA colonization. However, our understanding of the impact of circadian clock on sorghum-aphid interaction dynamics is limited. To explore this, a time-series transcriptomics was conducted on sorghum plants in disrupted circadian rhythm with and without SCA infestation. Transcriptomic analysis revealed a total of 2,873 differentially expressed genes (DEGs) and weighted gene co-expression network analysis (WGCNA) identified four modules with distinct expression patterns unique to night-time. Further, a total of 946 sorghum circadian genes were identified and among those, 328 circadian genes were unique to SCA-uninfested control groups that belonged to defense responses to insects and wounding. The circadian genes upregulated during the night-time after SCA infestation were related to MYB transcription factors, primary metabolism, and transporters, suggesting that SCA feeding modulates host defenses during the night-time. Aphid feeding modulation of sorghum defense genes during the night-time is in alignment with the electrical monitoring of SCA feeding behavior analysis, which revealed that the SCA spent significantly more time in the salivation phase during the night-time feeding. Our study provides novel insights into the circadian response of sorghum-aphid interaction dynamics and identified sorghum circadian genes in response to SCA infestation.