Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation
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.
Data Availability
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.
Acknowledgments
We thank Drs. Charles Sims and Asli Odabasi for their help with the consumer panel; Dawn Bies for help with volatile collection; Mark Taylor for help with plant care; and Michael Thomashow for invaluable advice. This work was supported by National Science Foundation Grants IOS-0923312 (to H.J.K., J.J.G., and Z.F.); National Key Research and Development Program 2016YFD0400101; Program of International Science and Technology Cooperation Grant 2011DFB31580; the New Star Program from Zhejiang University; and the China Scholarship Council.
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Information & Authors
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Published in
Cover image: Pictured is a visualization of cortical connectivity in the primate brain. Daniel S. Margulies et al. identified a gradient of functional connectivity across cortical regions in the primate brain, with primary sensorimotor regions at one end of the gradient and the default-mode network at the other end. The gradient correlates with the spatial distance between the regions on the cortical surface and with the degree of functional abstraction. The results suggest that the default-mode network sits atop a processing hierarchy, governing abstract cognitive processes that are removed from direct environmental input but require integration across multiple systems. See the article by Margulies et al. on pages 12574–12579. Image courtesy of Joachim Böttger and Daniel S. Margulies (Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany).
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Data Availability
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.
Submission history
Published online: October 17, 2016
Published in issue: November 1, 2016
Keywords
Acknowledgments
We thank Drs. Charles Sims and Asli Odabasi for their help with the consumer panel; Dawn Bies for help with volatile collection; Mark Taylor for help with plant care; and Michael Thomashow for invaluable advice. This work was supported by National Science Foundation Grants IOS-0923312 (to H.J.K., J.J.G., and Z.F.); National Key Research and Development Program 2016YFD0400101; Program of International Science and Technology Cooperation Grant 2011DFB31580; the New Star Program from Zhejiang University; and the China Scholarship Council.
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Competing Interests
The authors declare no conflict of interest.
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