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Transcriptome dynamics at Arabidopsis graft junctions reveal an intertissue recognition mechanism that activates vascular regeneration

Melnyk, Charles W. and Gabel, Alexander and Hardcastle, Thomas J. and Robinson, Sarah and Miyashima, Shunsuke and Grosse, Ivo and Meyerowitz, Elliot M. (2018) Transcriptome dynamics at Arabidopsis graft junctions reveal an intertissue recognition mechanism that activates vascular regeneration. Proceedings of the National Academy of Sciences of the United States of America, 115 (10). E2447-E2456. ISSN 0027-8424. PMCID PMC5878008.

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The ability for cut tissues to join and form a chimeric organism is a remarkable property of many plants; however, grafting is poorly characterized at the molecular level. To better understand this process, we monitored genome-wide gene expression changes in grafted Arabidopsis thaliana hypocotyls. We observed a sequential activation of genes associated with cambium, phloem, and xylem formation. Tissues above and below the graft rapidly developed an asymmetry such that many genes were more highly expressed on one side than on the other. This asymmetry correlated with sugar-responsive genes, and we observed an accumulation of starch above the graft junction. This accumulation decreased along with asymmetry once the sugar-transporting vascular tissues reconnected. Despite the initial starvation response below the graft, many genes associated with vascular formation were rapidly activated in grafted tissues but not in cut and separated tissues, indicating that a recognition mechanism was activated independently of functional vascular connections. Auxin, which is transported cell to cell, had a rapidly elevated response that was symmetric, suggesting that auxin was perceived by the root within hours of tissue attachment to activate the vascular regeneration process. A subset of genes was expressed only in grafted tissues, indicating that wound healing proceeded via different mechanisms depending on the presence or absence of adjoining tissues. Such a recognition process could have broader relevance for tissue regeneration, intertissue communication, and tissue fusion events.

Item Type:Article
Related URLs:
URLURL TypeDescription Paper CentralArticle
Melnyk, Charles W.0000-0003-3251-800X
Hardcastle, Thomas J.0000-0002-9328-5011
Grosse, Ivo0000-0001-5318-4825
Meyerowitz, Elliot M.0000-0003-4798-5153
Additional Information:© 2018 the Author(s). This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Edited by Dominique C. Bergmann, Stanford University, Stanford, CA, and approved January 19, 2018 (received for review October 19, 2017). We thank Niko Geldner, Dolf Weijers, Paul Tarr, Yka Helariutta, Ruth Stadler, Li-Jia Qu, and the Nottingham Arabidopsis Stock Centre for providing seeds. Funding for this work was provided by Gatsby Charitable Trust Grants GAT3272/C and GAT3273-PR1; by Knut and Alice Wallenberg Academy Fellowship KAW2016.0274 (to C.W.M.); by a SKW Stickstoffwerke Piesteritz GmbH Research Foundation Grant (to A.G. and I.G.); by German Science Foundation (DFG) Grants GR 3526/2, GR 3526/6, and FZT 118 (to I.G.); and by Howard Hughes Medical Institute and Gordon and Betty Moore Foundation Grant GBMF3406 (to E.M.M.). This article is a PNAS Direct Submission. Author contributions: C.W.M., A.G., T.J.H., and E.M.M. designed research; C.W.M., A.G., T.J.H., and S.R. performed research; S.M. contributed new reagents/analytic tools; C.W.M., A.G., T.J.H., S.R., I.G., and E.M.M. analyzed data; and C.W.M., A.G., T.J.H., S.R., S.M., and E.M.M. wrote the paper. The authors declare no conflict of interest.
Funding AgencyGrant Number
Gatsby Charitable TrustGAT3272/C
Gatsby Charitable TrustGAT3273-PR1
Knut and Alice Wallenberg AcademyKAW2016.0274
SKW Stickstoffwerke Piesteritz GmbH Research FoundationUNSPECIFIED
Deutsche Forschungsgemeinschaft (DFG)GR 3526/2
Deutsche Forschungsgemeinschaft (DFG)GR 3526/6
Deutsche Forschungsgemeinschaft (DFG)FZT 118
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationGBMF3406
Subject Keywords:plant grafting; regeneration; auxin; vascular tissue; wound healing
Issue or Number:10
PubMed Central ID:PMC5878008
Record Number:CaltechAUTHORS:20180214-151343479
Persistent URL:
Official Citation:Transcriptome dynamics of the Arabidopsis graft Charles W. Melnyk, Alexander Gabel, Thomas J. Hardcastle, Sarah Robinson, Shunsuke Miyashima, Ivo Grosse, Elliot M. Meyerowitz Proceedings of the National Academy of Sciences Mar 2018, 115 (10) E2447-E2456; DOI: 10.1073/pnas.1718263115
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:84837
Deposited By: Ruth Sustaita
Deposited On:14 Feb 2018 23:53
Last Modified:03 Oct 2019 19:23

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