Integrative analysis of the methylome and transcriptome of tomato fruit (Solanum lycopersicum L.) induced by postharvest handling

Abstract

Tomato fruit ripening is triggered by the demethylation of key genes, which alters their transcriptional levels thereby initiating and propagating a cascade of physiological events. What is unknown is how these processes are altered when fruit are ripened using postharvest practices to extend shelf-life, as these practices often reduce fruit quality. To address this, postharvest handling-induced changes in the fruit DNA methylome and transcriptome, and how they correlate with ripening speed, and ripening indicators such as ethylene, abscisic acid, and carotenoids, were assessed. This study comprehensively connected changes in physiological events with dynamic molecular changes. Ripening fruit that reached ‘Turning’ (T) after dark storage at 20 ℃, 12.5 ℃, or 5 ℃ chilling (followed by 20 ℃ rewarming) were compared to fresh-harvest fruit ‘FHT’. Fruit stored at 12.5 ℃ had the biggest epigenetic marks and alterations in gene expression, exceeding changes induced by postharvest chilling. Fruit physiological and chronological age were uncoupled at 12.5 ℃, as the time-to-ripening was the longest. Fruit ripening to Turning at 12.5 ℃ was not climacteric; there was no respiratory or ethylene burst, rather, fruit were high in abscisic acid. Clear differentiation between postharvest-ripened and ‘FHT’ was evident in the methylome and transcriptome. Higher expression of photosynthetic genes and chlorophyll levels in ‘FHT’ fruit pointed to light as influencing the molecular changes in fruit ripening. Finally, correlative analyses of the -omics data putatively identified genes regulated by DNA methylation. Collectively, these data improve our interpretation of how tomato fruit ripening patterns are altered by postharvest practices, and long-term are expected to help improve fruit quality.

Acknowledgments

J.Z., B.C., and K.A. received fellowships from the University of California Davis Graduate Group of Horticulture & Agronomy, and Henry A. Jastro Graduate Research Awards; K.S. and K.L. thank the Postharvest Technology Innovation Center, Ministry of Higher Education, Science, Research and Innovation, Bangkok, Thailand for support. Work in DB’s lab was supported by the USDA National Institute of Food and Agriculture, Hatch Project CA-D-PLS-2404-H, and a UC Davis ADVANCE Scholar Fellowship. The authors thank Dr. Ioannis S. Minas and David Sterle for use of the DA meter and especially Carlos Crisosto for the generous use of several instruments. Emma Shipman, Dave Tseng, Yichao Xu, Chiu-Ling Yang, and Po-kai Huang are acknowledged for their critical reading of this article, and we are grateful for the technical support of undergraduate interns Roshmund Romero and Annika Uemura and the comments made by Reviewer #2 which enhanced the manuscript.

Author Contributions

J.Z.: conceptualization; methodology; formal analysis; led the bioinformatics analysis, investigation; validation; writing—original draft, review and editing; S.Z.: bioinformatics analysis; review and editing; B.C.: conceptualization; review and editing; K.S.: methodology (carotenoids assay); review and editing; K.L. supervision and funding acquisition; review; K.A. review and editing; funding acquisition; D.B. conceptualization; funding acquisition; methodology; project administration; resources; supervision; writing—original draft, review and editing.

Data availability

The RNASeq and WGBS sequencing data has been uploaded to Sequence Read Archive (SRA) of NCBI, and the BioProject ID PRJNA1026769 https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1026769

Conflict of interest

The authors declare that there is no conflict of interests.

Supplementary Data

Supplementary data is available at Horticulture Research online.

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