Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation

Abstract

Commercial tomatoes are widely perceived by consumers as lacking flavor. A major part of that problem is a postharvest handling system that chills fruit. Low-temperature storage is widely used to slow ripening and reduce decay. However, chilling results in loss of flavor. Flavor-associated volatiles are sensitive to temperatures below 12 °C, and their loss greatly reduces flavor quality. Here, we provide a comprehensive view of the effects of chilling on flavor and volatiles associated with consumer liking. Reduced levels of specific volatiles are associated with significant reductions in transcripts encoding key volatile synthesis enzymes. Although expression of some genes critical to volatile synthesis recovers after a return to 20 °C, some genes do not. RNAs encoding transcription factors essential for ripening, including RIPENING INHIBITOR (RIN), NONRIPENING, and COLORLESS NONRIPENING are reduced in response to chilling and may be responsible for reduced transcript levels in many downstream genes during chilling. Those reductions are accompanied by major changes in the methylation status of promoters, including RIN. Methylation changes are transient and may contribute to the fidelity of gene expression required to provide maximal beneficial environmental response with minimal tangential influence on broader fruit developmental biology.

Single‐base methylome analysis reveals dynamic epigenomic differences associated with water deficit in apple

“…Indeed, many changes in gene expression were not correlated with the corresponding methylation changes in this study (Figure b and c). Similar results were also observed in tomato fruit under chilling stress, revealing that only 37%–67% of different GO term genes presented a negative correlation between methylation level and transcript abundance (Zhang et al ., ). This phenomenon was partly caused by methylation alterations that did not affect gene expression in some regions.…”

“…Paper bagging (environmental factor changes) altered the DNA methylation and histone modifications on MdMYB1 and activated the MdMYB1 gene and downstream genes, leading to differential anthocyanin pigmentation (Bai et al ., ). Cold storage of tomato increased methylation of RIN (RIPENING INHIBITOR) and decreased the transcripts of RIN and some of its direct targets (Zhang et al ., ). Compared with regulating structural genes, it is understandable that plants prefer a more energy‐saving and high‐efficient way of controlling TFs to further regulate biological pathways in response to environmental influences.…”

Genome-Wide Identification, Expression Patterns, and Functional Analysis of UDP Glycosyltransferase Family in Peach (Prunus persica L. Batsch)

“…Libraries for high-throughput Illumina strand-specific RNA-seq were prepared as described previously (Zhang et al, 2016). Three biological replicates for various organs, fruit development and ripening stages and treatment were prepared.…”

Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit

“…Evidence has recently emerged that, in addition to ethylene and the TFs, DNA methylation is another key regulator of fruit ripening (27). Furthermore, a recent study revealed that DNA methylation is associated with chilling-induced flavor loss in tomato fruits (28). Tomato fruits undergo a dramatic loss in DNA methylation during ripening (27).…”