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ARS Home » Northeast Area » Ithaca, New York » Robert W. Holley Center for Agriculture & Health » Plant, Soil and Nutrition Research » Research » Publications at this Location » Publication #288412
Title: Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening

Author
item ZHONG, SILIN - Boyce Thompson Institute
item FEI, ZHANGJUN - Boyce Thompson Institute
item CHEN, YUN-RU - Boyce Thompson Institute
item VREBALOV, JULIA - Boyce Thompson Institute
item MCQUINN, RYAN - Cornell University
item GAPPER, NIGEL - Cornell University
item Giovannoni, James

Submitted to: Nature Biotechnology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/22/2012
Publication Date: 1/27/2013
Citation: Zhong, S., Fei, Z., Chen, Y., Vrebalov, J., Mcquinn, R., Gapper, N., Giovannoni, J.J. 2013. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nature Biotechnology. 31:154-159.

Interpretive Summary: Tomato (Solanum lycopersicum) is an important vegetable crop with a genome that has been recently sequenced. It is the primary model plant for studying the development of fleshy fruits. Fleshy fruits are unique in that following seed maturation, they typically undergo a ripening process involving irreversible changes in color, texture, sugar content, aroma and flavor, to become succulent and appealing to seed dispersal organisms, including humans. Tight regulatory oversight of this process is required to insure accurate control of a developmental transition that would be highly detrimental if deployed in the wrong tissue or stage of fruit maturity. Here we show that changes in DNA methylation are associated with the transition to ripening. We also show which specific genes are impacted and provide data that a regulatory protein known as RIN operates at the sites of this differential methylation. These results suggest that genetic attributes in addition to differences in DNA sequence alone may be important regulators of crop development and may provide additional targets for breeding for optimal crop outcomes.

Technical Abstract: Fruits are differentiated floral tissues evolved to aid seed dispersal, and have become an important part of human diets. Ethylene triggers tomato fruit ripening, but its effect is restricted to matured fruits with viable seeds by an unknown developmental cue. We show that fruits ripen prematurely when exposed to methyltransferase inhibitor 5-azacytidine. Genome bisulfite sequencing reveals that epigenome reprogramming occurs during wild-type fruit development and is limited in ripening-deficient mutants. Ripening transcription factor RIN binding sites are specifically associated with the demethylated regions in the promoters of key ripening genes. This study shows the epigenome is not static during development, and was likely selected by evolution to insure fidelity and constraint of irreversible and potentially harmful developmental processes such as ripening. It also highlights the importance of considering crop improvement strategies that not only focus on DNA sequence variation, but also the information encoded in the epigenome.