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.
Subscribe to Journal
Get full journal access for 1 year
only $5.42 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Lough, T. J. & Lucas, W. J. Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu. Rev. Plant Biol. 57, 203–232 (2006).
Melnyk, C. W., Molnar, A. & Baulcombe, D. C. Intercellular and systemic movement of RNA silencing signals. EMBO J. 30, 3553–3563 (2011).
Molnar, A. et al. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872–875 (2010).
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).
Zhang, W. et al. Graft-transmissible movement of inverted-repeat-induced siRNA signals into flowers. Plant J. 80, 106–121 (2014).
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).
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).
Kragler, F. RNA in the phloem: A crisis or a return on investment? Plant Sci. 178, 99–104 (2010).
Kehr, J. & Buhtz, A. Long distance transport and movement of RNA through the phloem. J. Exp. Bot. 59, 85–92 (2008).
Huang, S. et al. The genome of the cucumber, Cucumis sativus L. Nature Genet. 41, 1275–1281 (2009).
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).
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).
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).
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).
Cao, J. et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nature Genet. 43, 956–963 (2011).
Schmitz, R. J. et al. Patterns of population epigenomic diversity. Nature 495, 193–198 (2013).
Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627–631 (2010).
Takenaka, M., Zehrmann, A., Verbitskiy, D., Hartel, B. & Brennicke, A. RNA editing in plants and its evolution. Annu. Rev. Genet. 47, 335–352 (2013).
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).
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).
The Gene Ontology's Reference Genome Project. Unified framework for functional annotation across species. PLoS Comput. Biol. 5, e1000431 (2009).
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).
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).
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).
Guo, S. et al. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nature Genet. 45, 51–58 (2013).
Kanehira, A. et al. Apple phloem cells contain some mRNAs transported over long distances. Tree Genet. Genomes 6, 635–642 (2010).
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).
Bai, X. et al. Transcriptomic signatures of ash (Fraxinus spp.) phloem. PLoS ONE 6, e16368 (2011).
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).
Franco-Zorrilla, J. M. et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genet 39, 1033–1037 (2007).
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).
McGarry, R. C. & Kragler, F. Phloem-mobile signals affecting flowers: applications for crop breeding. Trends Plant Sci. 18, 198–206 (2013).
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).
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.
The authors declare no competing financial interests.
About this article
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). https://doi.org/10.1038/nplants.2015.25
Trends in Biochemical Sciences (2020)
The circadian clock coordinates plant development through specificity at the tissue and cellular level
Current Opinion in Plant Biology (2020)
A constitutive and drought-responsive mRNA undergoes long-distance transport in pear (Pyrus betulaefolia) phloem
Plant Science (2020)
Loss of function of Arabidopsis NADP‐malic enzyme 1 results in enhanced tolerance to aluminum stress
The Plant Journal (2020)