Skip to main content

Thank you for visiting 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.

Endogenous Arabidopsis messenger RNAs transported to distant tissues

A Corrigendum to this article was published on 21 November 2016

A Corrigendum to this article was published on 28 May 2015


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.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. Lough, T. J. & Lucas, W. J. Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu. Rev. Plant Biol. 57, 203–232 (2006).

    CAS  Article  Google Scholar 

  2. Melnyk, C. W., Molnar, A. & Baulcombe, D. C. Intercellular and systemic movement of RNA silencing signals. EMBO J. 30, 3553–3563 (2011).

    CAS  Article  Google Scholar 

  3. Molnar, A. et al. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872–875 (2010).

    CAS  Article  Google Scholar 

  4. Liang, D., White, R. G. & Waterhouse, P. M. Gene silencing in Arabidopsis spreads from the root to the shoot, through a gating barrier, by template-dependent, nonvascular, cell-to-cell movement. Plant Physiol. 159, 984–1000 (2012).

    CAS  Article  Google Scholar 

  5. Zhang, W. et al. Graft-transmissible movement of inverted-repeat-induced siRNA signals into flowers. Plant J. 80, 106–121 (2014).

    CAS  Article  Google Scholar 

  6. Xoconostle-Cazares, B., Ruiz-Medrano, R. & Lucas, W. J. Proteolytic processing of CmPP36, a protein from the cytochrome b5 reductase family, is required for entry into the phloem translocation pathway. Plant J. 24, 735–747 (2000).

    CAS  Article  Google Scholar 

  7. Omid, A., Keilin, T., Glass, A., Leshkowitz, D. & Wolf, S. Characterization of phloem-sap transcription profile in melon plants. J. Exp. Bot. 58, 3645–3656 (2007).

    CAS  Article  Google Scholar 

  8. Kragler, F. RNA in the phloem: A crisis or a return on investment? Plant Sci. 178, 99–104 (2010).

    CAS  Article  Google Scholar 

  9. Kehr, J. & Buhtz, A. Long distance transport and movement of RNA through the phloem. J. Exp. Bot. 59, 85–92 (2008).

    CAS  Article  Google Scholar 

  10. Huang, S. et al. The genome of the cucumber, Cucumis sativus L. Nature Genet. 41, 1275–1281 (2009).

    CAS  Article  Google Scholar 

  11. Jones, L., Ratcliff, F. & Baulcombe, D. C. RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr. Biol. 11, 747–757 (2001).

    CAS  Article  Google Scholar 

  12. Haywood, V., Yu, T. S., Huang, N. C. & Lucas, W. J. Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. Plant J. 42, 49–68 (2005).

    CAS  Article  Google Scholar 

  13. Banerjee, A. K. et al. Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18, 3443–3457 (2006).

    CAS  Article  Google Scholar 

  14. Kim, M., Canio, W., Kessler, S. & Sinha, N. Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293, 287–289 (2001).

    CAS  Article  Google Scholar 

  15. Cao, J. et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nature Genet. 43, 956–963 (2011).

    CAS  Article  Google Scholar 

  16. Schmitz, R. J. et al. Patterns of population epigenomic diversity. Nature 495, 193–198 (2013).

    CAS  Article  Google Scholar 

  17. Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627–631 (2010).

    CAS  Article  Google Scholar 

  18. Takenaka, M., Zehrmann, A., Verbitskiy, D., Hartel, B. & Brennicke, A. RNA editing in plants and its evolution. Annu. Rev. Genet. 47, 335–352 (2013).

    CAS  Article  Google Scholar 

  19. Scheible, W. R. et al. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136, 2483–2499 (2004).

    CAS  Article  Google Scholar 

  20. Misson, J. et al. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation . Proc. Natl Acad. Sci. USA 102, 11934–11939 (2005).

    CAS  Article  Google Scholar 

  21. The Gene Ontology's Reference Genome Project. Unified framework for functional annotation across species. PLoS Comput. Biol. 5, e1000431 (2009).

  22. Kim, G., LeBlanc, M. L., Wafula, E. K., dePamphilis, C. W. & Westwood, J. H. Plant science. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345, 808–811 (2014).

    CAS  Article  Google Scholar 

  23. Li, Y., Chen, L., Mu, J. & Zuo, J. LESION SIMULATING DISEASE1 interacts with catalases to regulate hypersensitive cell death in Arabidopsis. Plant Physiol. 163, 1059–1070 (2013).

    CAS  Article  Google Scholar 

  24. Doering-Saad, C., Newbury, H. J., Couldridge, C. E., Bale, J. S. & Pritchard, J. A phloem-enriched cDNA library from Ricinus: insights into phloem function. J. Exp. Bot. 57, 3183–3193 (2006).

    CAS  Article  Google Scholar 

  25. Guo, S. et al. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nature Genet. 45, 51–58 (2013).

    CAS  Article  Google Scholar 

  26. Kanehira, A. et al. Apple phloem cells contain some mRNAs transported over long distances. Tree Genet. Genomes 6, 635–642 (2010).

    Article  Google Scholar 

  27. Deeken, R. et al. Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments. Plant J. 55, 746–759 (2008).

    CAS  Article  Google Scholar 

  28. Bai, X. et al. Transcriptomic signatures of ash (Fraxinus spp.) phloem. PLoS ONE 6, e16368 (2011).

    CAS  Article  Google Scholar 

  29. Oparka, K. J. & Cruz, S. S. THE GREAT ESCAPE: phloem transport and unloading of macromolecules. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 323–347 (2000).

    CAS  Article  Google Scholar 

  30. Franco-Zorrilla, J. M. et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genet 39, 1033–1037 (2007).

    CAS  Article  Google Scholar 

  31. Pant, B. D., Buhtz, A., Kehr, J. & Scheible, W. R. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 53, 731–738 (2008).

    CAS  Article  Google Scholar 

  32. McGarry, R. C. & Kragler, F. Phloem-mobile signals affecting flowers: applications for crop breeding. Trends Plant Sci. 18, 198–206 (2013).

    CAS  Article  Google Scholar 

  33. Fuentes, I., Stegemann, S., Golczyk, H., Karcher, D. & Bock, R. Horizontal genome transfer as an asexual path to the formation of new species. Nature 511, 232–235 (2014).

    CAS  Article  Google Scholar 

Download references


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.

Author information

Authors and Affiliations



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.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Thieme, C., Rojas-Triana, M., Stecyk, E. et al. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nature Plants 1, 15025 (2015).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI:

Further reading


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