Comparative metabolomics and transcriptomics of plant response to Tomato yellow leaf curl virus infection in resistant and susceptible tomato cultivars

In order to understand resistance to Tomato yellow leaf curl virus (TYLCV) we have performed a combined analysis of the metabolome and transcriptome of resistant (R) and susceptible (S) tomato plants both prior to and following TYLCV infection. Metabolites detected by gas chromatography–mass spectrometry (GC–MS) and liquid chromatography–mass spectrometry analysis, in leaves of R and S plants, at 1, 3, 7 and 14 days post infection and control plants, were used for the reconstruction of four independent metabolic networks. Measuring the network parameters revealed distinctive systemic metabolic responses to TYLCV infection between the R and S plants. Notably, the GC–MS metabolic network indicated that, following infection, the R plant exhibited tight coordination of the metabolome than the S plant. Clear differences in the level of specialized metabolites between the S and R plants were revealed; among them, substantial alteration in the abundance of amino acids and polyamines, phenolic and indolic metabolites, all leading to the synthesis of defense compounds. Integrating metabolome and transcriptome data highlighted differently regulated pathways in the R and S plants in response to TYLCV, including the phenylpropanoid, tryptophan/nicotinate and urea/polyamine pathways. Salicylic acid biosynthesis was additionally distinctively activated in R plants upon infection. Comparing the expression of genes of the urea and phenylpropanoid pathways in S, R and Solanum habrochaites, the resistance genitor wild species tomato, indicated a time-shift in the expression patterns, before and following infection, which on one hand reflected the genetic similarity between these plants, and on the other hand demonstrated that the resistant phenotype is intermediate between that of S and S. habrochaites.