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

Bo Zhang; Denise M. Tieman; Chen Jiao; Yimin Xu; Kunsong Chen; Zhangjun Fei; James J. Giovannoni; Harry J. Klee

doi:10.1073/pnas.1613910113

Contributed by Harry J. Klee, August 24, 2016 (sent for review July 31, 2016; reviewed by Richard M. Amasino and Graham B. Seymour)

Significance

Cold storage is widely used to extend shelf-life of agriculture products. For tomato, this handling results in reduced flavor quality. Our work provides major insights into the effects of chilling on consumer liking, the flavor metabolome and transcriptome, as well as DNA methylation status. Transcripts for some key volatile synthesis enzymes and the most important ripening-associated transcription factors are greatly reduced in response to chilling. These reductions are accompanied by major changes in the methylation status of promoter regions. Transient increases in DNA methylation occur during chilling. Our analysis provides insight into the molecular mechanisms of tomato fruit flavor loss caused by chilling.

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.

Footnotes

↵¹To whom correspondence should be addressed. Email: hjklee{at}ufl.edu.

Author contributions: B.Z., J.J.G., and H.J.K. designed research; B.Z., D.M.T., C.J., and Y.X. performed research; B.Z., D.M.T., C.J., Z.F., J.J.G., and H.J.K. analyzed data; B.Z., K.C., Z.F., J.J.G., and H.J.K. wrote the paper; and K.C. provided support and partial supervision of B.Z.
Reviewers: R.M.A., University of Wisconsin–Madison; and G.B.S., University of Nottingham.
The authors declare no conflict of interest.
Data deposition: All of the chilling-related methylome data generated for this paper are archived at single-base resolution in the tomato epigenome database at ted.bti.cornell.edu/epigenome/. Raw sequence reads of methylome and transcriptome have also been deposited in NCBI Sequence Read Archive (SRA) under accession numbers SRP082267 and SRP082266, respectively.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1613910113/-/DCSupplemental.

View Full Text