Glomerella leaf spot (GLS), caused by the fungal pathogen Colletotrichum fructicola, significantly threatens apple production. Some resistances to plant disease are mediated by the accumulation of nucleotide‐binding site and leucine‐rich repeat (NBS‐LRR) proteins that are encoded by a major class of plant disease resistance genes (R genes). However, the R genes that confer resistance to GLS in apple remain largely unclear. Malus hupehensis YT521‐B homology domain‐containing protein 2 (MhYTP2) was identified as an N6‐methyladenosine RNA methylation (m6A) modified RNA reader in our previous study. However, whether MhYTP2 binds to mRNAs without m6A RNA modifications remains unknown. In this study, we discovered that MhYTP2 exerts both m6A‐dependent and ‐independent functions by analysing previously obtained RNA immunoprecipitation sequencing results. The overexpression of MhYTP2 significantly reduced the resistance of apple to GLS and down‐regulated the transcript levels of some R genes whose transcripts do not contain m6A modifications. Further analysis indicated that MhYTP2 binds to and reduces the stability of MdRGA2L mRNA. MdRGA2L positively regulates resistance to GLS by activating salicylic acid signalling. Our findings revealed that MhYTP2 plays an essential role in the regulation of resistance to GLS and identified a promising R gene, MdRGA2L, for use in developing apple cultivars with GLS resistance.

Studies have shown that the m6A reader primarily affects genes expression by participating in the regulation of mRNA localization, splicing, degradation, translation, and other metabolic processes. Previously, we discovered that the apple (Malus domestica) m6A reader MhYTP2 bound with and destabilized m6A-modified MdMLO19 mRNA. In addition, it enhanced the translation efficiency of m6A-modified mRNA of MdGDH1L, encoding a glutamate dehydrogenase, which confers resistance to powdery mildew. In this study, we report the function of MhYTP2 in the regulation of resistance to low nitrogen (N). The overexpression of MhYTP2 enhances the resistance of apple to low N. We show that MhYTP2 binds with and stabilizes the mRNAs of MdALN, which participates in the allantoin catabolic process and cellular response to N starvation in apple; MdPIDL, which participates in root hair elongation; MdTTG1, which is involved in the differentiation process of trichomes; and MdATG8A, which is a core participant in the regulation of autophagy. In addition, MhYTP2 accelerates the degradation of MdRHD3 mRNA, which regulates root development. RNA immunoprecipitation-seq and electrophoretic mobility shift assays show that the mRNAs of MdALN, MdATG8A, MdPIDL, MdTTG1, and MdRHD3 are the direct targets of MhYTP2. Overexpressing or knocking down the above genes in MhYTP2 overexpressing plants dismisses the function of MhYTP2 under low N, suggesting the role of MhYTP2 is dependent on those genes. Together, these results demonstrate that MhYTP2 enhances the resistance of apple to N deficiency by affecting the stability of the bound mRNAs.