A translocation between chromosome 6 and 8 influences lncRNA_MYB114 and PpRPP13 expression and underpins red leaf trait and powdery mildew resistance in peach

Red leaf peach has important ornamental value owing to its characteristic leaf coloration. However, this species is highly susceptible to powdery mildew, and the mechanisms of red leaf formation, resistance to powdery mildew, and their relationship remain unclear. We performed population genetic analyses of red leaf peach, revealing that the translocation of chromosomes 6 and 8 is genetically linked to both the red leaf trait and powdery mildew resistance. Bulk segregant analysis-sequencing, genome resequencing, and expression analysis indicated that the PpMYB114 and the resistance gene PpRPP13 are responsible for the red leaf phenotype and powdery mildew resistance, respectively. The chromosomal translocation causes a promoter fragment of PpRPP13 on chromosome 8 to integrate into the antisense chain of PpMYB114 on chromosome 6, thereby enhancing the expression of PpMYB114 and inhibiting the expression of PpRPP13. Further, lncRNA-seq identified a new antisense lncRNA, lncRNA_MYB114, which is generated by the translocation and can activate PpMYB114 expression to synthesize anthocyanin. Moreover, the overexpression of PpRPP13 resulted in enhanced resistance to powdery mildew. In summary, these results revealed the molecular mechanism of a chromosomal translocation altering the expression of PpMYB114 and PpRPP13 to form the red leaf phenotype that is linked to powdery mildew susceptibility.