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Published March 6, 2018 | Published
Journal Article Open

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

Abstract

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.

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.

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Created:
August 21, 2023
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