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Whole-genome DNA methylation patterns and complex associations with gene expression associated with anthocyanin biosynthesis in apple fruit skin

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Abstract

Main conclusion

DNA methylation of anthocyanin biosynthesis-related genes and MYB/bHLH transcription factors was associated with apple fruit skin color revealed by whole-genome bisulfite sequencing.

Abstract

DNA methylation is a common feature of epigenetic regulation and is associated with various biological processes. Anthocyanins are among the secondary metabolites that contribute to fruit colour, which is a key appearance and nutrition quality attribute of apple fruit. Although few studies reported that DNA methylation in the promoter of MYB transcription factor was associated with fruit skin color, there is a general lack of understanding of the dynamics of global and genic DNA methylation in apple fruit. Here, whole-genome bisulfite sequencing was carried out in fruit skin of apple (Malus domestica Borkh.) cv. ‘Red Delicious’ (G0) and its four-generation bud sport mutants, including ‘Starking Red’ (G1), ‘Starkrimson’ (G2), ‘Campbell Redchief’ (G3) and ‘Vallee spur’ (G4) at color break stage. Correlation and linear-regression analysis between DNA methylation level and anthocyanin content, as well as the transcription levels of genes related to anthocyanin biosynthesis were carried out. The results showed that the number of differentially methylated regions (DMRs) and differentially methylated genes (DMGs) was considerably increased from G1 to G4 versus the number observed in G0. The mCHH context was dominant in apple, but the levels of mCG and mCHG of DMGs were significantly higher than that of the mCHH. Genetic variation of bud sport mutants from ‘Red Delicious’ was associated with differential DNA methylation. Additionally, hypomethylation of mCG and mCHG contexts in flavonoid biosynthesis pathway genes (PAL, 4CL, CYP98A, PER, CCoAOMT, CHS, and F3′H), mCHG context in MYB10 at upstream, led to transcriptional activation and was conductive to anthocyanin accumulation. However, hypermethylation of mCG context in bHLH74 at upstream led to transcriptional inhibition, inhibiting anthocyanin accumulation.

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Abbreviations

DMGs:

Different methylation genes

DMRs:

Different methylation regions

GO:

Gene Ontology

KEGG:

Kyoto Encyclopedia of Genes and Genomes

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Acknowledgements

This work was financially supported by the Discipline Construction Fund Project of Gansu Agricultural University (GSAU-XKJS-2018-230), the Fostering Foundation for the Excellent Ph.D. Dissertation of Gansu Agricultural University (2017002), and the Science and Technology Major Project of Gansu Province (18ZD2NA006).

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  1. College of Horticulture, Gansu Agricultural University, 730070, Lanzhou, People’s Republic of China

    Wen-Fang Li, Gai-Xing Ning, Juan Mao, Zhi-Gang Guo, Qi Zhou & Bai-Hong Chen

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  1. Wen-Fang Li
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Fig. S1

DNA methylation levels of annotated DMGs involved in phenylpropanoid/flavonoid biosynthesis pathway in regions of a upstream, b genebody and c downstream used as a test group in total methylation level

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Li, WF., Ning, GX., Mao, J. et al. Whole-genome DNA methylation patterns and complex associations with gene expression associated with anthocyanin biosynthesis in apple fruit skin. Planta 250, 1833–1847 (2019). https://doi.org/10.1007/s00425-019-03266-4

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