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Title: Comprehensive transcriptome analysis and functional characterization of PR-5 for its involvement in tomato Sw-7 resistance to tomato spotted wilt tospovirus

Author
item Padmanabhan, Chellappan
item MA, Q. - Boyce Thompson Institute
item SHEKASTEBAND, R - University Of Florida
item Stewart, Kevin
item HUTTON, S - University Of Florida
item SCOTT, J.W. - University Of Florida
item FEI, Z - Boyce Thompson Institute
item Ling, Kai-Shu

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/8/2019
Publication Date: 5/21/2019
Citation: Padmanabhan, C., Ma, Q., Shekasteband, R., Stewart, K.S., Hutton, S.F., Scott, J., Fei, Z., Ling, K. 2019. Comprehensive transcriptome analysis and functional characterization of PR-5 for its involvement in tomato Sw-7 resistance to tomato spotted wilt tospovirus. Scientific Reports. 9:7673. https://doi.org/10.1038/s41598-019-44100-x.
DOI: https://doi.org/10.1038/s41598-019-44100-x

Interpretive Summary: Tomato spotted wilt virus (TSWV), the type member of genus Tospovirus in the Bunyaviridae family, is one of the most prevalent tomato viruses in the world. This virus has a broad host range, infecting over 1,090 plant species. Under field conditions, TSWV is spread from plant to plant by multiple species of thrips, primarily the western flower thrips, in a persistent manner. TSWV cause plant stunting, chlorotic or necrotic rings on leaves and fruits of tomato plants, resulting in yield loss over a billion dollars annually in the U.S. Plant disease resistance is the most effective and economical means of viral disease management. Over the years, seven genes in tomato confer disease resistance to TSWV have been identified. Sw-7, recently introgressed from S. chilense LA 1938 into tomato exhibited excellent field resistance to various isolates of TSWV, including those isolates that overcome Sw-5. To gain a fundamental knowledge on the potential genes of interest on tomato carrying Sw-7 as well as possible gene expression pathways influenced by TSWV infection, we performed, for the first time, a comprehensive comparative analysis of global gene expression between a susceptible and a near-isogenic resistant line in response to TSWV infection. In total, 1,791 unique differentially expressed genes were identified in five different time points, from inoculation to symptom expression. Based on functional category analysis, three networks of genes responsible in plant defense, photosynthesis, and ribonucleicacid (RNA) silencing pathway were most significantly affected. In addition, protein kinases (PKs), transcription factors (TFs) pathway genes and microRNA were altered, that are important regulators for gene expression. This global transcriptome analysis will provide us a first step to characterize the potential disease resistance gene(s) and to elucidate the underlying mechanism of resistance against TSWV in tomato Sw-7 lines.

Technical Abstract: Tomato spotted wilt orthotospovirus (TSWV), one of the most important plant viruses, causes serious yield losses on tomato (Solanum lycopersicum) worldwide. In consideration of the potential resistance breaking of common Sw-5 gene against TSWV, it is essential to understand the resistance mechanism associated with Sw-7, an alternative loci conferring resistance to TSWV. In an effort to uncover gene networks that are associated with Sw-7 resistance, we performed comparative transcriptome profiling and gene expression analysis between an isogenic Sw-7 line and its susceptible recurrent parent (Fla. 8059). A total of 1,244 differentially expressed genes (DEGs) were identified at five time points throughout a disease progression process, involving networks of host resistance genes, RNA silencing/antiviral defense genes, and crucial transcriptional and translational regulators. Notable induced expression genes in Sw-7 include callose accumulation, lignin deposition, proteolysis process, transcriptional activation/repression, and phosphorylation. Finally, we investigated the potential involvement of PR-5 in the Sw-7 resistance, by overexpressing in TSWV-susceptible tomato genotype. Interestingly, PR-5 overexpression conferred an enhanced resistance to TSWV infection resulting in a delay in virus accumulation and symptom expression. These findings would pave the way to facilitate breeding and genetic engineering efforts to incorporate this new source of resistance in tomato against TSWV.