Sugarcane yellow leaf virus impairs the transcriptomic defense responses of sugarcane to its new aphid vector Melanaphis sorghi

Abstract

Sugarcane (Saccharum spp.) is a preeminent sugar and bioenergy crop and has great economic importance in tropical countries. A major disease affecting this crop is yellow leaf disease, which is caused by sugarcane yellow leaf virus (SCYLV, Polerovirus SCYLV, Solemoviridae). The sugarcane aphid Melanaphis sacchari is considered the main vector of SCYLV, and the closely related sorghum aphid Melanaphis sorghi, which has recently emerged as a pest of great relevance in sorghum, has also been suspected as a vector. Genetic resistance is an important resource for preventing yield losses caused by SCYLV and its vectors, but knowledge on the underlying molecular mechanisms is lacking. Therefore, the present work was aimed at investigating the transcriptomic responses of sugarcane to SCYLV and M. sorghi, which was reported to transmit this virus for the first time herein. Two sugarcane cultivars, one susceptible and one tolerant to SCYLV, were fed upon by aviruliferous and viruliferous aphids. The transcriptome of the plants was assessed by RNA-Seq using differential gene expression analyses and a gene coexpression network. The susceptible cultivar showed an incipient reaction to both M. sorghi and SCYLV, with very few differentially expressed genes (DEGs) identified in comparison with aphid-free plants. The response of the tolerant cultivar to aviruliferous M. sorghi involved pathways typically associated with defense against herbivory, which were also enriched in coexpression network modules in which DEGs were overrepresented. Some of these genes were hubs in their respective modules, indicating they are potential key regulators of the defense responses. However, these responses were diminished when viruliferous aphids were used, and other processes linked to infection with SCYLV were altered. These results indicated that SCYLV could affect sugarcane defense responses to its vector, similar to other viruses of the same genus. Some possible implications for the epidemiology and impact of SCYLV and M. sorghi are discussed.