TaCAMTA4 negatively regulates H2O2-dependent wheat leaf rust resistance by activating catalase 1 expression

Abstract Leaf rust, caused by Puccinia triticina Erikss. (Pt), is a serious disease threatening wheat (Triticum aestivum L.) production worldwide. Hydrogen peroxide (H2O2) triggered by Pt infection in resistant wheat cultivars cause oxidative damage directly to biomolecules or is activated by calcium signaling and mediates the hypersensitive response. Calmodulin-binding transcriptional activator 4 (TaCAMTA4) has been reported to negatively regulate wheat resistance to Pt. In this study, we found that TaCAMTA4 was induced by Pt race 165 in its compatible host harboring the Pt-resistant locus Lr26, TcLr26, and silencing of TaCAMTA4 increased local H2O2 accumulation and Pt resistance. Subcellular localization and autoactivation tests revealed that TaCAMTA4 is a nucleus-localized transcriptional activator. Furthermore, 4 DNA motifs recognized by TaCAMTA4 were identified by transcription factor-centered Y1H. Through analyzing the transcriptome database, 4 gene clusters were identified, each containing a different DNA motif on each promoter. Among them, the expression of catalase 1 (TaCAT1) with motif-1 was highly induced in the compatible interaction and was decreased when TaCAMTA4 was silenced. The results of electrophoretic mobility shift assay, ChIP-qPCR, and RT-qPCR further showed that TaCAMTA4 directly bound motif-1 in the TaCAT1 promoter. Furthermore, silencing of TaCAT1 resulted in enhanced resistance to Pt and increased local H2O2 accumulation in wheat, which is consistent with that of TaCAMTA4. Since calmodulin-binding transcription activators are Ca2+ sensors and catalases catalyze the decomposition of H2O2, we hypothesize that Ca2+ regulates the plant immune networks that are controlled by H2O2 and implicate a potential mechanism for Pt to suppress resistance by inducing the expression of the TaCAMTA4-TaCAT1 module, which consequently enhances H2O2 scavenging and attenuates H2O2-dependent resistance. A calmodulin-binding transcriptional activator binds to a catalase gene promoter and activates its expression, resulting in hydrogen peroxide scavenging and impaired leaf rust resistance in wheat.