Transcriptomic Profiling Unravels the Disruption of Photosynthesis Apparatuses and Induction of Immune Responses by a Bipartite Begomovirus in Tomato Plants

Diseases caused by begomoviruses such as tomato yellow leaf curl disease (TYLCD) are major constraints in agriculture. While the interactions between plants and monopartite begomoviruses during TYLCD pathogenesis have been explored extensively, how bipartite begomoviruses interact with tomato plants are understudied. Here we first found that a bipartite begomovirus tomato yellow leaf curl Thailand virus (TYLCTHV) induced stunted growth, leaf curl and yellowing in tomato plants. We then profiled the tomato transcriptomic changes in response to TYLCTHV infection. In total, we identified 2322 upregulated and 1377 downregulated genes. KEGG enrichment analysis of the differentially expressed genes (DEGs) revealed that many KEGG pathways regulating plant photosynthesis processes and defenses were enriched. Specifically, TYLCTHV infection disrupted the expression of DEGs that function in the light-harvesting chlorophyll protein complex, photosystem I and II, cytochrome b6/f complex, photosynthetic electron transport and F-type ATPase. Additionally, the expression of many DEGs regulating plant defenses including pathogen-associated molecular pattern (PAMP)-triggered immunity, effector-triggered immunity and hypersensitive response was upregulated upon TYLCTHV infection. Taken together, we found that during the pathogenesis of TYLCD induced by TYLCTHV, the virus actively disrupts plant photosynthesis processes and induces defense responses. Our findings add to our knowledge of TYLCD pathogenesis and plant–virus interactions in general.