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Endogenous Arabidopsis messenger RNAs transported to distant tissues

Nature Plants volume 1, Article number: 15025 (2015) Cite this article

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A Corrigendum to this article was published on 21 November 2016

A Corrigendum to this article was published on 28 May 2015

Abstract

The concept that proteins and small RNAs can move to and function in distant body parts is well established. However, non-cell-autonomy of small RNA molecules raises the question: To what extent are protein-coding messenger RNAs (mRNAs) exchanged between tissues in plants? Here we report the comprehensive identification of 2,006 genes producing mobile RNAs in Arabidopsis thaliana. The analysis of variant ecotype transcripts that were present in heterografted plants allowed the identification of mRNAs moving between various organs under normal or nutrient-limiting conditions. Most of these mobile transcripts seem to follow the phloem-dependent allocation pathway transporting sugars from photosynthetic tissues to roots via the vasculature. Notably, a high number of transcripts also move in the opposite, root-to-shoot direction and are transported to specific tissues including flowers. Proteomic data on grafted plants indicate the presence of proteins from mobile RNAs, allowing the possibility that they may be translated at their destination site. The mobility of a high number of mRNAs suggests that a postulated tissue-specific gene expression profile might not be predictive for the actual plant body part in which a transcript exerts its function.

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Figure 1: Hypocotyl-grafting of the distantly related Arabidopsis thaliana ecotypes Col-0 and Ped-0 exposed to nutritional stresses and number of identified mobile transcripts.
Figure 2: Mobile transcripts transported from PED roots into flowering COL shoots after grafting.
Figure 3: Analysis of mobile transcripts found in Cuscuta reflexa and in A. thaliana grafts.
Figure 4: Tissue expression biases analysis of transcripts and heterologous proteins identified in grafted plants.

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Acknowledgements

We would like to thank Dana Schindelasch and Marina Stratmann (MPI-MPP-Golm) for technical support; Nadine Andresen for characterizing mutant plants. Mark Stitt (MPI-MPP-Golm) for support, discussions and corrections relating to the manuscript. This work was partially supported by Max Planck Society funds to M.S., F.K. and W-R.S., and by the Spanish Ministry of Economy and Competitiveness (grant BIO2011-29085) to J.P-A.

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Author notes

  1. Christoph J. Thieme, Monica Rojas-Triana, Ewelina Stecyk, Christian Schudoma and Wenna Zhang: These authors contributed equally to this work.

Authors and Affiliations

  1. Max Planck Institute of Molecular Plant Physiology, Wissenschaftspark Golm, Am Mühlenberg 1, Potsdam, 14476, Germany

    Christoph J. Thieme, Ewelina Stecyk, Christian Schudoma, Wenna Zhang, Lei Yang, Dirk Walther, Wolf-Rüdiger Scheible & Friedrich Kragler

  2. Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, 73401, Oklahoma, USA

    Monica Rojas-Triana & Wolf-Rüdiger Scheible

  3. Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología–Consejo Superior de Investigaciones Cientificas, Campus de Cantoblanco, Madrid, 28049, Spain

    Miguel Miñambres & Javier Paz-Ares

  4. Department of Plant Systems Biology, University of Hohenheim, Stuttgart, 70593, Germany

    Waltraud X. Schulze

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  1. Christoph J. Thieme
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Contributions

C.J.T., C.S. and D.W. devised and implemented the bioinformatic methodology and analysis; E.S. and M.R-T. performed ecotype-grafting experiments and analysed data; W.Z. and L.Y. performed A. thaliana grafting and C. reflexa experiments and analysed data; M.M. provided constructs; W.X.S. performed protein identification and annotation analysis; J.P-A. supervised M.M.; F.K. supervised W.Z., L.Y. and E.S.; W-R.S. supervised E.S. and M.R-T.; D.W. supervised C.J.T. and C.S.; F.K. wrote, supported by all co-authors, the manuscript; W-R.S. and F.K. analysed results and implemented ideas; J.P-A.,W-R.S. and F.K. are co-principal investigators who conceived the study.

Corresponding author

Correspondence to Friedrich Kragler.

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Thieme, C., Rojas-Triana, M., Stecyk, E. et al. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nature Plants 1, 15025 (2015). https://doi.org/10.1038/nplants.2015.25

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