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A transposon-induced epigenetic change leads to sex determination in melon

Abstract

Sex determination in plants leads to the development of unisexual flowers from an originally bisexual floral meristem1,2. This mechanism results in the enhancement of outcrossing and promotes genetic variability, the consequences of which are advantageous to the evolution of a species3. In melon, sexual forms are controlled by identity of the alleles at the andromonoecious (a) and gynoecious (g) loci4. We previously showed that the a gene encodes an ethylene biosynthesis enzyme, CmACS-7, that represses stamen development in female flowers5. Here we show that the transition from male to female flowers in gynoecious lines results from epigenetic changes in the promoter of a transcription factor, CmWIP1. This natural and heritable epigenetic change resulted from the insertion of a transposon, which is required for initiation and maintenance of the spreading of DNA methylation to the CmWIP1 promoter. Expression of CmWIP1 leads to carpel abortion, resulting in the development of unisexual male flowers. Moreover, we show that CmWIP1 indirectly represses the expression of the andromonoecious gene, CmACS-7, to allow stamen development. Together our data indicate a model in which CmACS-7 and CmWIP1 interact to control the development of male, female and hermaphrodite flowers in melon.

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Figure 1: Sex determination is due to the insertion of a DNA transposon at the gynoecious locus.
Figure 2: The Gyno-hAT insertion leads to specific spreading of DNA methylation.
Figure 3: CmWIP1 is the gynoecious gene responsible for sex determination.
Figure 4: Integration of CmWIP1 and CmACS-7 in a sex determination model.

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GenBank/EMBL/DDBJ

Data deposits

Sequences have been deposited in GenBank under accession codes GQ870274 and GQ870275.

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Acknowledgements

We thank D. Bradley, M. Purugganan, P. Laufs, J. C. Palauqui and colleagues from Unité de Recherche en Génomique Végétale (URGV) for discussions and comments on the manuscript, and F. Teixeira and V. Colot for helpful assistance on DNA methylation assays. This work was supported by GAP department in INRA and by a grant from Genopole (A.M.).

Author Contributions A.Be., C.D. and M.P. initiated the project. A.M., C.D. and A.Be. designed the experiments. A.M., C.T., A.Bo., M.R., R.F. and H.M. performed the experiments, for which the data were analysed by A.M., C.D. and A.Be. A.M. and A.Be. wrote the paper, which was commented on and improved by all the authors.

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Correspondence to Abdelhafid Bendahmane.

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Martin, A., Troadec, C., Boualem, A. et al. A transposon-induced epigenetic change leads to sex determination in melon. Nature 461, 1135–1138 (2009). https://doi.org/10.1038/nature08498

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