Control of Vein Pattern Formation by the GNOM gene of Arabidopsis
Creators: Nguyen, Linh M
Publisher: name: University of Alberta Library
Year: 2022

<p>To form tissue networks, animal cells migrate and interact through proteins protruding from their plasma membranes. Plant cells can do neither, yet plants form vein networks. How plants do so is unclear, but the prevailing hypothesis proposes that GNOM — a regulator of vesicle formation in membrane trafficking — positions transporters of the plant hormone auxin to the correct side of the plasma membrane. The resulting cell-to-cell, polar transport of auxin would then induce vein formation. I tested that hypothesis and — contrary to its predictions — found that vein formation occurs in the absence of polar auxin transport and that the residual auxin-transport-independent vein-patterning activity relies on auxin signaling. My results suggest that a GNOM-dependent signal acts upstream of both auxin transport and signaling in vein patterning. However, plants inhibited in both auxin transport and signaling still formed veins. Patterning of vascular cells into veins was instead prevented in gnom mutants, suggesting the existence of at least one more GNOM-dependent vein-patterning pathway. I showed that such a pathway depends on the movement of auxin or an auxin-dependent signal through plasmodesmata intercellular channels. Plasmodesma permeability was high where veins were forming, lowered between veins and nonvascular tissues, but remained high between vein cells. Impaired ability to regulate plasmodesma aperture led to defects in auxin transport and signaling, ultimately leading to vein patterning defects that were enhanced by inhibition of auxin transport or signaling. GNOM controlled plasmodesma aperture regulation, and simultaneous inhibition of auxin signaling, polar auxin transport, and regulated plasmodesma aperture phenocopied gnom mutants. Therefore, veins are patterned by the coordinated action of three GNOM-dependent pathways: auxin signaling, polar auxin transport, and movement of auxin or an auxin-dependent signal through plasmodesmata. I next addressed the question whether — and if so, where and when in leaf development — GNOM controlled the production, the movement, or the interpretation of a vein patterning signal. My results suggest that GNOM controls the production, propagation, or interpretation of a vein patterning signal in the leaf inner tissues. For that function, GNOM expression was required in all the inner tissues of the leaf throughout leaf development, but stronger GNOM expression seemed to be required where new veins were forming. By contrast, if a signal with vein patterning function were produced in the leaf epidermis, the production of such a signal would be independent of GNOM. I finally addressed the question whether GNOM-dependent, high plasmodesma permeability were required for vein patterning in all or only some of the tissues of the developing leaf. I found that wide plasmodesma aperture is required in newly formed veins and in all the inner cells in areas of the leaf where new veins are forming. By contrast, wide plasmodesma aperture was dispensable in the epidermis and in the nonvascular inner tissue surrounding newly formed veins. My results suggest that the epidermis is a sink for signals that are produced in inner cells and move there through plasmodesmata to promote vein formation. Therefore — contrary to widespread belief — the epidermis is not a source of auxin signals that diffuse or are transported into the inner tissues to induce vein formation. In conclusion, my results suggest an unprecedented mechanism of tissue network formation in multicellular organisms.</p>