Multi-omics analyses reveal <i>MdMYB10</i> hypermethylation being responsible for a bud sport of apple fruit color

Abstract Apple bud sports enable a rich resource for clonal selection of numerous elite cultivars. The accumulation of somatic mutations as plants develop may potentially impact the emergence of bud sport. Previous studies focused on the somatic mutation in the essential genes associated with the bud sport. However, the rate and function of genome-wide somatic mutations that accumulate when bud sport arises remain unclear. In this study, we identified a bud sport as a branch from a ten-year-old tree of the apple cultivar ‘Oregon Spur II’. The mutant branch showed reduced red coloration on fruit skin. Using these plant materials, we assembled a high-quality haplotype reference genome consisting of 649.61 Mb sequences with a contig N50 value of 2.04 Mb. We then estimated the somatic mutation rate of the apple tree being 4.56×10-8 per base per year, and further identified 253 somatic SNPs, including five nonsynonymous SNPs, between original type and mutant samples. Transcriptome analyses identified 69 differentially expressed genes (DEGs) between original type and mutant fruit skin were highly correlated with anthocyanin content. DNA methylation in the promoter of five anthocyanin associated genes was increased in the mutant compared to the original type as determined using DNA methylation profiling. Among genetic and epigenetic factors that directly and indirectly influence anthocyanin content in the mutant apple fruit skin, the hypermethylated promoter of MdMYB10 is an important factor. This study indicated that numerous somatic mutations accumulated at the emergence of bud sport from a genome-wide perspective, some of which contribute to the low coloration bud sport.