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Expansion of the redox-sensitive proteome coincides with the plastid endosymbiosis

Abstract

The redox-sensitive proteome (RSP) consists of protein thiols that undergo redox reactions, playing an important role in coordinating cellular processes. Here, we applied a large-scale phylogenomic reconstruction approach in the model diatom Phaeodactylum tricornutum to map the evolutionary origins of the eukaryotic RSP. The majority of P. tricornutum redox-sensitive cysteines (76%) is specific to eukaryotes, yet these are encoded in genes that are mostly of a prokaryotic origin (57%). Furthermore, we find a threefold enrichment in redox-sensitive cysteines in genes that were gained by endosymbiotic gene transfer during the primary plastid acquisition. The secondary endosymbiosis event coincides with frequent introduction of reactive cysteines into existing proteins. While the plastid acquisition imposed an increase in the production of reactive oxygen species, our results suggest that it was accompanied by significant expansion of the RSP, providing redox regulatory networks the ability to cope with fluctuating environmental conditions.

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Figure 1: Examples of ancestral sequence reconstruction.
Figure 2: Cys gains along the ancestral lineages leading to P. tricornutum.
Figure 3: Prokaryotic gene ancestry of RSCys gains via gene origin in the six ancestral lineages.

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Acknowledgements

The authors thank A. Kupzok, J. Ilhan, J. Weissenbach, C. Walda, A. Mrnjavac and T. Wein for critical comments on the manuscript. This project was supported by the European Research Council (Grant No. 281357 awarded to T.D. and 280991 awarded to A.V.), the Israeli Science Foundation (Grant 25 No. 712233 awarded to A.V.) and the cluster of excellence, The Future Ocean (funded within the framework of the Excellence Initiative by the Deutsche Forschungsgemeinschaft (DFG) on behalf of the German federal and state governments).

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C.W., G.L., S.R., A.V. and T.D. conceived the study. T.D., G.L. and C.W. designed the research strategy. C.W., G.L. and S.R. performed the analyses. All authors were involved in the interpretation of results and writing of the article.

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Correspondence to Christian Woehle or Shilo Rosenwasser.

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Woehle, C., Dagan, T., Landan, G. et al. Expansion of the redox-sensitive proteome coincides with the plastid endosymbiosis. Nature Plants 3, 17066 (2017). https://doi.org/10.1038/nplants.2017.66

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