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

Melnyk, Charles W.; Gabel, Alexander; Hardcastle, Thomas J.; Robinson, Sarah; Miyashima, Shunsuke; Grosse, Ivo; 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 - PNAS, 115(10), E2447-E2456. National Academy of Sciences NAS 10.1073/pnas.1718263115

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Plant grafting is an ancient and agriculturally important technique. Despite its widespread use, little is known about how plants graft. Here, we perform a genome-wide transcriptome analysis of tissues above and below graft junctions. We observed a sequential activation of genes important for vascular development including cambium-, phloem-, and xylem-related genes. Massive changes in gene expression that rapidly differentiate the top of the graft from the bottom occur. These changes disappear as the graft heals and the vasculature reconnects. Many genes below the junction rapidly respond to the presence of attached tissues including genes involved in vascular differentiation and cell division. This intertissue communication process occurs independently of functional vascular connections and acts as a signal to activate vascular regeneration.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.

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