Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

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

Nature Plants volume 4, pages 784–791 (2018)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

Data availability

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

References

  1. Coombe, B. G. The development of fleshy fruits. Annu. Rev. Plant. Physiol. 27, 207–228 (1976).

    Article  CAS  Google Scholar 

  2. Tiffney, B. H. Vertebrate dispersal of seed plants through time. Annu. Rev. Ecol. Evol. Syst. 35, 1–29 (2004).

    Article  Google Scholar 

  3. McMurchie, E. J., McGlasson, W. B., & Eaks, I. L. Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature 237, 235–236 (1972).

    Article  CAS  Google Scholar 

  4. McManus, M. T. The plant hormone ethylene. (Wiley–Blackwell, Hoboken, NJ, 2012).

  5. Barry, C. S., Llop-Tous, M. I., & Grierson, D. The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol. 123, 976–986 (2000).

    Article  Google Scholar 

  6. Giovannoni, J., Nguyen, C., Ampofo, B., Zhong, S., & Fei, Z. The epigenome and transcriptional dynamics of fruit ripening. Annu. Rev. Plant. Biol. 68, 61–84 (2017).

    Article  CAS  Google Scholar 

  7. Manning, K. et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38, 948–952 (2006).

    Article  CAS  Google Scholar 

  8. Vrebalov, J. et al. A MADS-box gene necessary for fruit ripening at the tomato RIPENING INHIBITOR (rin) locus. Science 296, 343–346 (2002).

    Article  CAS  Google Scholar 

  9. Zhong, S. et al. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31, 154–159 (2013).

    Article  CAS  Google Scholar 

  10. Liu, R. et al. A DEMETER-like DNA demethylase governs tomato fruit ripening. Proc. Natl Acad. Sci. USA 112, 10804–10809 (2015).

    Article  CAS  Google Scholar 

  11. Sato, S. et al. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635–641 (2012).

    Article  CAS  Google Scholar 

  12. Vrebalov, J. et al. Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 21, 3041–3062 (2009).

    Article  CAS  Google Scholar 

  13. Lin, Z., Zhong, S., & Grierson, D. Recent advances in ethylene research. J. Exp. Bot. 60, 3311–3336 (2009).

    Article  CAS  Google Scholar 

  14. Guo, H. & Ecker, J. R. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115, 667–677 (2003).

    Article  CAS  Google Scholar 

  15. Lee, T. H., Tang, H., Wang, X. & Paterson, A. H. PGDD: A database of gene and genome duplication in plants. Nucleic Acids Res. 41, 1152–1158 (2013).

    Article  Google Scholar 

  16. Périn, C. et al. Molecular and genetic characterization of a non-climacteric phenotype in melon reveals two loci conferring altered ethylene response in fruit. Plant Physiol. 129, 300–309 (2002).

    Article  Google Scholar 

  17. Kunieda, T. et al. NAC family proteins NARS1/NAC2 and NARS2/NAM in the outer integument regulate embryogenesis in Arabidopsis. Plant Cell Online 20, 2631–2642 (2008).

    Article  CAS  Google Scholar 

  18. Guo, Y., & Gan, S. AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46, 601–612 (2006).

    Article  CAS  Google Scholar 

  19. D’Hont, A. et al. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488, 213–217 (2012).

    Article  Google Scholar 

  20. Golding, J., Shearer, D., Wyllie, S., & McGlasson, W. Application of 1-MCP and propylene to identify ethylene-dependent ripening processes in mature banana fruit. Postharvest. Biol. Technol. 14, 87–98 (1998).

    Article  CAS  Google Scholar 

  21. Liang, C. et al. OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc. Natl Acad. Sci. USA 111, 10013–10018 (2014).

    Article  CAS  Google Scholar 

  22. Roy Choudhury, S., Roy, S., Nag, A., Singh, S. K. & Sengupta, D. N. Characterization of an AGAMOUS-like MADS-box protein, a probable constituent of flowering and fruit ripening regulatory system in banana. PLoS One 7, e44361 (2012).

    Article  Google Scholar 

  23. Elitzur, T. et al. Banana MaMADS transcription factors are necessary for fruit ripening and molecular tools to promote shelf-life and food security. Plant Physiol. 171, 380–391 (2016).

    Article  CAS  Google Scholar 

  24. Primack, R. B. Relationships Among Flowers, Fruits, and Seeds. Annu. Rev. Ecol. Syst. 18, 409–430 (1987).

    Article  Google Scholar 

  25. Tieman, D. M., Ciardi, J. A., Taylor, M. G. & Klee, H. J. Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. Plant J. 26, 47–58 (2001).

    Article  CAS  Google Scholar 

  26. Ríos, P. et al. ETHQV6.3 is involved in melon climacteric fruit ripening and is encoded by a NAC domain transcription factor. Plant J. 91, 671–683 (2017).

    Article  Google Scholar 

  27. Pirona, R. et al. Fine mapping and identification of a candidate gene for a major locus controlling maturity date in peach. BMC Plant Biol. 13, 166 (2013).

    Article  Google Scholar 

  28. Schwartz, Y. B. & Pirrotta, V. Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8, 9–22 (2007).

    Article  CAS  Google Scholar 

  29. He, Y. Chromatin regulation of flowering. Trends. Plant. Sci. 17, 556–562 (2012).

    Article  CAS  Google Scholar 

Download references

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.

Author information

Author notes

  1. These authors contributed equally: Peitao Lü, Sheng Yu, Ning Zhu, Yun-Ru Chen, Biyan Zhou.

Authors and Affiliations

  1. State Key Laboratory of Agrobiotechnology, School of Life Sciences, Chinese University of Hong Kong, Hong Kong, China

    Peitao Lü, Sheng Yu, Ning Zhu, Yun-Ru Chen, David Tzeng & Silin Zhong

  2. College of Horticulture, South China Agricultural University, Guangzhou, China

    Biyan Zhou

  3. College of Horticulture and Landscape Architecture, Southwest University, Chongqing, China

    Yu Pan

  4. Department of Food Science and Experimental Nutrition, FCF, University of Sao Paulo, Sao Paulo, Brazil

    Joao Paulo Fabi

  5. IRTA, Centre for Research in Agricultural Genomics, Barcelona, Spain

    Jason Argyris & Jordi Garcia-Mas

  6. Department of Biology, Hong Kong Baptist University, Hong Kong, China

    Nenghui Ye & Jianhua Zhang

  7. School of Crop Sciences, University of Nottingham, Nottingham, UK

    Donald Grierson

  8. Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Hangzhou, China

    Donald Grierson

  9. Weill Medical College, Cornell University, New York, NY, USA

    Jenny Xiang

  10. US Department of Agriculture—Agricultural Research Service and Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY, USA

    Zhangjun Fei & James Giovannoni

Authors
  1. Peitao Lü
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sheng Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ning Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yun-Ru Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Biyan Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. David Tzeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Joao Paulo Fabi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jason Argyris
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jordi Garcia-Mas
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Nenghui Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jianhua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Donald Grierson
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jenny Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Zhangjun Fei
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. James Giovannoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Silin Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-018-0249-z

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing