Integrating omics reveals that miRNA-guided genetic regulation at the plant hormone level and defense response pathways shape resistance to Cladosporium fulvum in the tomato Cf-10-carrying line

Background: Invasion of Cladosporium fulvum causes the most serious diseases affecting the reproduction of tomatoes. The Cf-10 gene has been proven to confer resistance to C. fulvum . However, how the Cf-10 gene mediates host defense gene expression and physiological changes to activate immunity in C. fulvum remains unknown. Multiple-omics studies could reveal potential regulation among different data types, providing an opportunity for dissecting the genetic regulatory mechanism underlying the Cf-10 -mediated defense response. Results: To exploit the genetic mechanism underlying the Cf-10 gene, we performed a multiple-omics study of a resistant line carrying the Cf-10 gene and a susceptible line not carrying any resistance genes for the control and for 3 days postinoculation (dpi) of C. fulvum . By miRNA profiling, we detected 54 differentially expressed miRNAs (DE-miRNAs) between the control and 3 dpi in the resistant line, 79.63% of which were downregulated at 3 dpi. The miRNAs potentially regulate 894 genes whose functions are involved in the plant–pathogen interaction pathway and the auxin, JA, ethylene, ABA and SA signaling pathways. Transcriptome profiling revealed 1,100 differentially expressed genes (DEGs) between the control and 3 dpi in the resistant line whose functions were enriched in pathways that were potentially regulated by the DE-miRNAs. Integrating DE-miRNAs, gene expression patterns and plant-hormone metabolism profiling demonstrated that the downregulation of miRNAs at 3 dpi activated crucial resistance genes, such as Prf / PTO and RESISTANCE TO P. SYRINGAE PV MACULICOLA 1 ( RPM1 ), to trigger host hypersensitive cell death and upregulated the receptors/critical responsive transcription factors (TFs) of plant hormones to shape immunity to the pathogen. Notably, we identified and expressionally validated that the downregulation of miR9472 would upregulate the expression of IAA-LEUCINE RESISTANT (ILR)-LIKE GENE 6 (ILL6), a gene that transforms JA to its major active component (+)-7-iso-jasmonoyl-l-isoleucine (JA-Ile), to improve the level of JA-Ile and activate JA-response genes in the Cf-10 -carrying line. Conclusion: The Cf-10 gene carrying line employs a miRNA-guided “trade-off” strategy to coordinate plant growth and defense response: it expresses miRNAs to suppress invasion recognition and signal transduction pathways and reduce the level of JA and ethylene to maintain plant growth under normal conditions, but the infection of C. fulvum downregulates these miRNAs to activate the defense response pathways for acquiring disease resistance.