Overcoming short-day-dependent tuberization to adapt to long-day conditions is critical for the widespread geographical success of potato. The genetic pathways of photoperiodic tuberization are similar to those of photoperiodic flowering. DNA methylation plays an important role in photoperiodic flowering. However, little is known about how DNA methylation affects photoperiodic tuberization in potato. Here, we verified the effect of a DNA methylation inhibitor on photoperiodic tuberization and compared the DNA methylation levels and differentially methylated genes (DMGs) in the photoperiodic tuberization process between photoperiod-sensitive and photoperiod-insensitive genotypes, aiming to dissect the role of DNA methylation in the photoperiodic tuberization of potato. We found that a DNA methylation inhibitor could promote tuber initiation in strict short-day genotypes. Whole-genome DNA methylation sequencing showed that the photoperiod-sensitive and photoperiod-insensitive genotypes had distinct DNA methylation modes in which few differentially methylated genes were shared. Transcriptome analysis confirmed that the DNA methylation inhibitor regulated the expression of the key genes involved in the photoperiod and GA pathways to promote tuber initiation in the photoperiod-sensitive genotype. Comparison of the DNA methylation levels and transcriptome levels identified 52 candidate genes regulated by DNA methylation that were predicted to be involved in photoperiodic tuberization. Our findings provide a new perspective for understanding the relationship between photoperiod-dependent and GA-regulated tuberization. Uncovering the epigenomic signatures of these pathways will greatly enhance potato breeding for adaptation to a wide range of environments.

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