Abstract

BackgroundRecently, DNA methylation was proposed to regulate fleshy fruit ripening. Fleshy fruits can be distinguished by their ripening process as climacteric fruits, such as tomatoes, or non-climacteric fruits, such as strawberries. Tomatoes undergo a global decrease in DNA methylation during ripening, due to increased expression of a DNA demethylase gene. The dynamics and biological relevance of DNA methylation during the ripening of non-climacteric fruits are unknown.ResultsHere, we generate single-base resolution maps of the DNA methylome in immature and ripe strawberry. We observe an overall loss of DNA methylation during strawberry fruit ripening. Thus, ripening-induced DNA hypomethylation occurs not only in climacteric fruit, but also in non-climacteric fruit. Application of a DNA methylation inhibitor causes an early ripening phenotype, suggesting that DNA hypomethylation is important for strawberry fruit ripening. The mechanisms underlying DNA hypomethylation during the ripening of tomato and strawberry are distinct. Unlike in tomatoes, DNA demethylase genes are not upregulated during the ripening of strawberries. Instead, genes involved in RNA-directed DNA methylation are downregulated during strawberry ripening. Further, ripening-induced DNA hypomethylation is associated with decreased siRNA levels, consistent with reduced RdDM activity. Therefore, we propose that a downregulation of RdDM contributes to DNA hypomethylation during strawberry ripening.ConclusionsOur findings provide new insight into the DNA methylation dynamics during the ripening of non-climacteric fruit and suggest a novel function of RdDM in regulating an important process in plant development.

Highlights

  • DNA methylation was proposed to regulate fleshy fruit ripening

  • We discovered that DNA hypomethylation during strawberry ripening is associated with decreased expression of genes encoding components in the RNA-directed DNA methylation (RdDM) pathway and with decreased Small interfering RNA (siRNA) levels

  • We found that 24-nt siRNAs in strawberry have a preference for 5′ terminal adenosine (Additional file 2: Figure S5a), suggesting that 24-nt siRNA biogenesis is conserved in strawberry and Arabidopsis

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Summary

Introduction

DNA methylation was proposed to regulate fleshy fruit ripening. Tomatoes undergo a global decrease in DNA methylation during ripening, due to increased expression of a DNA demethylase gene. The dynamics and biological relevance of DNA methylation during the ripening of non-climacteric fruits are unknown. DNA methylation status can be dynamically regulated by both DNA methyltransferases and demethylases. The DNA demethylases, REPRESSOR OF SILENCING 1 (ROS1) family proteins, have DNA glycosylase/lyase activities and can actively initiate DNA demethylation process by removal of the mC base and cleavage of the DNA backbone at the abasic site, leaving a single-nucleotide gap that is later filled with a non-methylated cytosine [1, 6]

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