Antagonism of tomato spotted wilt virus against tomato yellow leaf curl virus in Nicotiana benthamiana detected by transcriptome analysis

Background Tomato spot wilt virus (TSWV) and tomato yellow leaf curl virus (TYLCV) are highly harmful viruses in agricultural production, which can cause serious economic losses to crops and even devastating consequences for vegetable yield in some countries and regions. Although the two viruses belong to different families and have different transmission vectors, they share most hosts. Objective This study aimed to examine the transcriptomic expression of single and mixed inoculations of TSWV and TYLCV, leading to antagonism using high-throughput RNA sequencing. Methods We confirmed the single and mixed infections of these viruses in Nicotiana benthamiana (N. benthamiana) by artificial inoculation. And the expression changes of related genes and their biological functions and pathways during the mixed infection of TSWV and TYLCV were analyzed by comparative transcriptome. Results Basically, similar symptoms were observed in the plants singly infected with TSWV and co-infected with TYLCV; the symptoms of TYLCV in the co-infected plants were not obvious compared with single TYLCV infections. When inoculated with TYLCV, the accumulation of the virus significantly reduced in single and mixed infections with TSWV; the TSWV accumulated slightly less in co-infection with TYLCV, whereas this reduction was much smaller than that of TYLCV. The results suggested that TSWV had an antagonistic effect on the accumulation of TYLCV in N. benthamiana. It mainly focused on the changes in unique differentially expressed genes (DEGs) caused by the co-infection of TSWV and TYLCV. The eight pathways enriched by upregulated DEGs mainly included amino acid biosynthesis, citrate cycle (or tricarboxylic acid cycle, TCA cycle), and so on. However, only pentose phosphate pathway (PPP) and peptidoglycan biosynthesis could be downregulated in the Kyoto Encyclopedia of Genes and Genomes pathway in which peptidoglycan biosynthesis was involved in upregulated and downregulated pathways. Conclusions The antagonistic effect of TSWV on TYLCV in N.benthamiana and the change trends and specific pathways of DEGs in this process were found. Our study provided new insights into the host regulation and competition between viruses in response to TSWV and TYLCV mixed infection.