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

Authors: ZHANG, BO - University Of Florida; TIEMAN, DENISE - University Of Florida; CHEN, JIAO - Boyce Thompson Institute; XU, YIMIN - Boyce Thompson Institute; CHEN, KUNSONG - Zheijiang University; FEI, ZHANGJUN - Boyce Thompson Institute; Giovannoni, James; KLEE, HARRY - University Of Florida

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/24/2016
Publication Date: 11/1/2016
Citation: Zhang, B., Tieman, D., Chen, J., Xu, Y., Chen, K., Fei, Z., Giovannoni, J.J., Klee, H. 2016. Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation. Proceedings of the National Academy of Sciences. 113:12580-12585.

Interpretive Summary: The modern commercial tomato is widely perceived as lacking flavor and is a major source of consumer dissatisfaction. Postharvest handling and retail systems are major contributors to poor flavor, particularly the commonly used practice of chilling fruit. Many consumers store purchased fruits in the refrigerator, further contributing to flavor deterioration. Tomato flavor is produced by a combination of sugars, acids, and volatiles. Production of flavor-associated volatiles is sensitive to temperatures below 12 °C and loss of volatiles has been observed during cold storage. In contrast, taste-related chemicals, sugars, and acids, are not significantly affected by cold storage. In addition to the economic impact of flavor quality loss, the tomato fruit provides an ideal system in which to examine the effects of environmental stress on a genome scale. Here, we provide a comprehensive analysis of the effect of chilling on the transcriptome and flavor metabolome. The large transcriptional reprogramming that occurred in response to chilling and following a recovery period was correlated with alterations in DNA methylation indicating a role for reversible effects on the genome in mediating fruit quality traits through altered gene expression. We demonstrate that targeted genes of chilling include regulators of ripening including key transcriptional regulators. These provide targets for optimizing chilling tolerance and fruit quality.

Technical 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.