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Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening

Abstract

Fleshy fruits using ethylene to regulate ripening have developed multiple times in the history of angiosperms, presenting a clear case of convergent evolution whose molecular basis remains largely unknown. Analysis of the fruitENCODE data consisting of 361 transcriptome, 71 accessible chromatin, 147 histone and 45 DNA methylation profiles reveals three types of transcriptional feedback circuits controlling ethylene-dependent fruit ripening. These circuits are evolved from senescence or floral organ identity pathways in the ancestral angiosperms either by neofunctionalisation or repurposing pre-existing genes. The epigenome, H3K27me3 in particular, has played a conserved role in restricting ripening genes and their orthologues in dry and ethylene-independent fleshy fruits. Our findings suggest that evolution of ripening is constrained by limited hormone molecules and genetic and epigenetic materials, and whole-genome duplications have provided opportunities for plants to successfully circumvent these limitations.

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Fig. 1: Three types of transcriptional feedback circuits controlling climacteric fruit ripening.
Fig. 2: Tomato and peach ripening genes are associated with tissue-specific epigenetic marks.
Fig. 3: Recreation of the positive feedback circuits for autocatalytic ethylene synthesis in tobacco.
Fig. 4: Chromatin and epigenome features of the banana ripening genes.
Fig. 5: Fruit ripening gene orthologues in non-climacteric and dry fruit species are associated with tissue-specific H3K27me3.
Fig. 6: Speciation, fruit ripening types and polyploidization in different angiosperms lineages.

Data availability

All data that support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

This work is supported by Hong Kong UGC GRF-14119814/14104515 and Area of Excellence Scheme AoE/M-403/16 to S.Z., Shenzhen Peacock-KQTD201101 to J.Z., Spanish Ministry of Economy and Competitively grant AGL2015-64625-C2-1-R, Centro de Excelencia Severo Ochoa 2016-2020 and the CERCA Programme/Generalitat de Catalunya to J.G.-M., and National Science Foundation IOS-1339287 to Z.F. and J.G.

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Authors

Contributions

S.Z. designed the research; P.L., N.Z., Y.C., B.Z., Y.P., J.F., J.A., N.Y. and J.Z. performed the experiments. S.Y., D.T., S.Z. and J.X. analysed the data. D.G., J.G.-M., Z.F., J.G. and S.Z. wrote the paper.

Corresponding author

Correspondence to Silin Zhong.

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The authors declare no competing interests.

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Supplementary Information

Supplementary Text, Supplementary Methods, Supplementary References and Supplementary Figs. 1–27.

Reporting Summary

Supplementary Tables 1–18

Supplementary Table 1: Summary of genome assembly and annotation used in this study. Supplementary Table 2: Sample description, sequencing and mapping statistics of paired-end RNA-Seq data. Supplementary Table 3: Sample description, sequencing and mapping statistics of single-end RNA-Seq data. Supplementary Table 4: Summary of differentially expressed genes (DEGs). Supplementary Table 5: Summary of DNase-seq data. Supplementary Table 6: Summary of DHS data and associated genes. Supplementary Table 7: Distribution of DHS in different genome features. Supplementary Table 8: Statistics of tissue-specific DHS. Supplementary Table 9: Sample description, sequencing and mapping statistics of BS-Seq data. Supplementary Table 10: Statistics of differentially methylated regions (DMRs). Supplementary Table 11: Summary of ripening genes associated with promoter DNA hypomethylation and ripe fruit tissue-specific DHS. Supplementary Table 12: List of ripe-specific DEGs that are associated with promoter DHS and DNA hypomethylation. Supplementary Table 13: Summary of histone modification and transcription factor ChIP-Seq. Supplementary Table 14: Number of genes assocaited with H3K27me3. Supplementary Table 15: Summary of genes associated with differentially methylated H3K27me3. Supplementary Table 16: Expression of DNA demethylases in different plant species. Supplementary Table 17: Expression of ethylene biosynthesis genes in different plant species. Supplementary Table 18: List of published datasets used in this study.

Supplementary Tables 19–34

Supplementary Table 19: Normalized expression (FPKM) of apple genes. Supplementary Table 20: Normalized expression (RPKM) of banana genes. Supplementary Table 21: Normalized expression (FPKM) of cucumber genes. Supplementary Table 22: Normalized expression (FPKM) of grape genes. Supplementary Table 23: Normalized expression (FPKM) of Melon genes. Supplementary Table 24: Normalized expression (FPKM) of papaya genes. Supplementary Table 25: Normalized expression (FPKM) of peach genes. Supplementary Table 26: Normalized expression (FPKM) of pear genes. Supplementary Table 27: Normalized expression (FPKM) of strawberry genes. Supplementary Table 28: Normalized expression (FPKM) of tomato genes. Supplementary Table 29: Normalized expression (FPKM) of watermelon genes. Supplementary Table 30: Tomato genes associated with RIN ChIP-Seq peak. Supplementary Table 31: Tomato genes associated with TAGL1 ChIP-Seq peak. Supplementary Table 32: Tomato genes associated with EIN3 ChIP-Seq peak. Supplementary Table 33: Peach genes associated with NAC ChIP-Seq peak. Supplementary Table 34: Genes associated with tissue-specific H3K27me3.

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Lü, P., Yu, S., Zhu, N. et al. Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening. Nature Plants 4, 784–791 (2018). https://doi.org/10.1038/s41477-018-0249-z

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