Ethylene Response Factor 3 represses SA pathway defense but promotes hormone responses upon pathogen infection

ERF/AP2 family transcription factors play crucial roles in plant growth, development, and stress responses. However, the functions of most family members remain unclear. Here, the role of ERF3 in Arabidopsis thaliana​​ was investigated through the analysis of ​​CRISPR/Cas9-generated erf3mutants and ERF3-overexpressing plants​​. We found that ​​the erf3 mutants exhibited enhanced resistance, whereas ERF3-overexpressing (ERF3-OE) plants showed slightly reduced resistance to the bacterial pathogen Pst DC3000 compared with wild-type plants​​. Transcriptomic sequencing identified 674 differentially expressed genes (DEGs) between ​​the erf3 mutants and wild-type plants​​, including 134 upregulated genes (​​erf3up DEGs​​) and 540 downregulated genes (erf3down DEGs​​). The ​​erf3up DEGs were significantly enriched in defense-related processes, including SA pathway marker genes (PR2 and PR5)​​, whereas ​​the erf3down DEGs were enriched in hormone-responsive pathways, such as responses to JA, ethylene, SA, auxin, GA, and ABA​​. Interestingly, ​​most of these hormone-responsive genes are not involved in disease resistance but play important roles in growth, development, and abiotic stress responses​​. ​​ERF3 is induced by Pst DC3000, SA, and JA, and ERF3 proteins are enriched on the promoters of target genes harboring cis-acting elements (GCC or DRE boxes), such as PR5, IAA29, RAV2, BG1, LECRK-1.1, and AZI1, as demonstrated by ChIP analysis​​. ​​Overall, ERF3 functions as a negative regulator of the SA pathway in disease resistance and plays a critical role in balancing disease resistance with hormone-mediated growth and abiotic stress responses. Our work provides novel insights into the potential of exploiting ERF3 function to enhance plant disease resistance​​.