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Commonalities and differences of chloroplast translation in a green alga and land plants

Nature Plants volume 4, pages 564–575 (2018)Cite this article

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Abstract

Chloroplast gene expression is a fascinating and highly regulated process, which was mainly studied on specific genes in a few model organisms including the unicellular green alga Chlamydomonas (Chlamydomonas reinhardtii) and the embryophyte (land) plants tobacco (Nicotiana tabacum) and Arabidopsis (Arabidopsis thaliana). However, a direct plastid genome-wide interspecies comparison of chloroplast gene expression that includes translation was missing. We adapted a targeted chloroplast ribosome profiling approach to quantitatively compare RNA abundance and translation output between Chlamydomonas, tobacco and Arabidopsis. The re-analysis of established chloroplast mutants confirmed the capability of the approach by detecting known as well as previously undetected translation defects (including the potential photosystem II assembly-dependent regulation of PsbH). Systematic comparison of the algal and land plant wild-type gene expression showed that, for most genes, the steady-state translation output is highly conserved among the three species, while the levels of transcript accumulation are more distinct. Whereas in Chlamydomonas transcript accumulation and translation output are closely balanced, this correlation is less obvious in embryophytes, indicating more pronounced translational regulation. Altogether, this suggests that green algae and land plants evolved different strategies to achieve conserved levels of protein synthesis.

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Fig. 1: Microarray-based ribosome profiling confirms known and discovers novel effects in established chloroplast gene expression mutants.
Fig. 2: High correlation of transcript accumulation and translation output between photoautotrophically and mixotrophically grown Chlamydomonas cells.
Fig. 3: Chloroplast translation output is conserved between Chlamydomonas, tobacco and Arabidopsis.
Fig. 4: Different degrees of correlation between transcript and FP abundances in Chlamydomonas and land plants.
Fig. 5: Translational adjustments of the protein synthesis output of chloroplast-encoded ATP synthase subunits.
Fig. 6: Translation output is not directly determined by codon usage.
Fig. 7: Ribosome FPs are heterogeneously distributed over ORFs with similar patterns in conserved reading frames of Chlamydomonas and land plants.

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Acknowledgements

We thank J. Nickelsen (Ludwig Maximilian University of Munich) for discussions and for providing dU and nac2 mutant strains and for antibodies against D2 and RBP40. We are grateful to S. Ruf and M.A. Schöttler (both from Max Planck Institute of Molecular Plant Physiology) for providing seeds for the atpB start codon mutants. We thank I. Gerlach for technical assistance, M. Tillich for help with microarray design and J. Gremmels for providing a script for data summary (all Max Planck Institute of Molecular Plant Physiology). For discussions on data analysis we thank J.M. Muino (Humboldt University of Berlin) and D. Walther (Max Planck Institute of Molecular Plant Physiology). We thank A. Barkan (University of Oregon) for critical discussions on the manuscript. For critical reading of this manuscript we thank C. Schmitz-Linneweber (Humboldt University of Berlin) and M. Schroda (University of Kaiserslautern). This work was supported by the German Research Foundation grants ZO 302/4-1 and TRR175-A04 to R.Z., and TRR175-A05 and the Forschungsschwerpunkt BioComp to F.W. R.Z. gratefully acknowledges support by the Max Planck Society.

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  1. These authors contributed equally to this work: R. Zoschke and F. Willmund.

Authors and Affiliations

  1. Molecular Genetics of Eukaryotes, University of Kaiserslautern, Kaiserslautern, Germany

    Raphael Trösch, Vincent Leon Gotsmann & Felix Willmund

  2. Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany

    Rouhollah Barahimipour, Yang Gao & Reimo Zoschke

  3. Instituto Politécnico Nacional-Unidad Profesional Interdisciplinaria de Biotecnología, Mexico City, Mexico

    Jesús Agustín Badillo-Corona

  4. Computational Systems Biology, University of Kaiserslautern, Kaiserslautern, Germany

    David Zimmer & Timo Mühlhaus

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Contributions

R.T. wrote the manuscript, conducted experiments and analysed data. R.B., Y.G. and J.A.B.C. conducted experiments and analysed data. V.L.G. performed experiments. D.Z. and T.M. performed statistical analyses. R.Z. and F.W. designed the experiments, analysed data, assembled figures and wrote the article with contribution from all other authors.

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Correspondence to Reimo Zoschke or Felix Willmund.

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Supplementary Figures 1–15, Supplementary Table 1 and Supplementary References.

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Supplementary Data Set 1

Complete dataset from array-based ribosome profiling experiments.

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Trösch, R., Barahimipour, R., Gao, Y. et al. Commonalities and differences of chloroplast translation in a green alga and land plants. Nature Plants 4, 564–575 (2018). https://doi.org/10.1038/s41477-018-0211-0

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