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

Guan Liu; Fengjiao Liu; Dongye Zhang; Tingting Zhao; Huanhuan Yang; Jingbin Jiang; Jingfu Li; He Zhang; Xiangyang Xu

doi:10.3389/fgene.2023.1158631

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

Front Genet. 2023 May 25:14:1158631. doi: 10.3389/fgene.2023.1158631. eCollection 2023.

Authors

Guan Liu^{1

2}, Fengjiao Liu¹, Dongye Zhang¹, Tingting Zhao³, Huanhuan Yang³, Jingbin Jiang³, Jingfu Li³, He Zhang³, Xiangyang Xu³

Affiliations

¹ College of Advanced Agriculture and Ecological Environment, Heilongjiang University, Harbin, China.
² State Key Laboratory of Tree Genetics and Breeding, College of Forestry, Northeast Forestry University, Harbin, China.
³ College of Horticulture and Landscape Architecture, Northeast Agricultural University, Harbin, China.

Abstract

Invasion of C. fulvum causes the most serious diseases affecting the reproduction of tomatoes. Cf-10-gene-carrying line showed remarkable resistance to Cladosporium fulvum. To exploit its defense response mechanism, we performed a multiple-omics profiling of Cf-10-gene-carrying line and a susceptible line without carrying any resistance genes at non-inoculation and 3 days post-inoculation (dpi) of C. fulvum. We detected 54 differentially expressed miRNAs (DE-miRNAs) between the non-inoculation and 3 dpi in the Cf-10-gene-carrying line, which potentially regulated plant-pathogen interaction pathways and hormone signaling pathways. We also revealed 3,016 differentially expressed genes (DEGs) between the non-inoculated and 3 dpi in the Cf-10-gene-carrying line whose functions enriched in pathways that were potentially regulated by the DE-miRNAs. Integrating DE-miRNAs, gene expression and plant-hormone metabolites indicated a regulation network where the downregulation of miRNAs at 3 dpi activated crucial resistance genes to trigger host hypersensitive cell death, improved hormone levels and upregulated the receptors/critical responsive transcription factors (TFs) of plant hormones, to shape immunity to the pathogen. Notably, our transcriptome, miRNA and hormone metabolites profiling and qPCR analysis suggested that that the downregulation of miR9472 potentially upregulated the expression of SAR Deficient 1 (SARD1), a key regulator for ICS1 (Isochorismate Synthase 1) induction and salicylic acid (SA) synthesis, to improve the level of SA in the Cf-10-gene-carrying line. Our results exploited potential regulatory network and new pathways underlying the resistance to C. fulvum in Cf-10-gene-carrying line, providing a more comprehensive genetic circuit and valuable gene targets for modulating resistance to the virus.

Keywords: Cf-10 gene; Cladosporium fulvum; defense response; gene expression regulation; miRNA; tomato.

Grants and funding

This work was supported by the Natural Science Outstanding Youth Foundation of Heilongjiang Province (YQ 2020C038), the Basic Scientific Research Foundation of Heilongjiang Provincial Universities (2023-KYYWF, grantee: GL), Heilongjiang Provincial Postdoctoral Science Foundation (LBH-Z21026) and Heilongjiang University graduate innovation research project funding (YJSCX 2022-263HLJU).