Coordination of tissue cell polarity by auxin transport and signaling

Abstract

Coordination of polarity between cells in tissues is key to multicellular organism development. In animals, coordination of this tissue cell polarity often requires direct cell-cell interactions and cell movements, which are precluded in plants by a wall that separates cells and holds them in place; yet plants coordinate the polarity of hundreds of cells during the formation of the veins in their leaves. Overwhelming experimental evidence suggests that the plant signaling molecule auxin coordinates tissue cell polarity to induce vein formation, but how auxin does so is unclear. The prevailing hypothesis proposes that GNOM, a regulator of vesicle formation during protein trafficking, positions auxin transporters of the PIN-FORMED family to the correct side of the plasma membrane. The resulting cell-to-cell, polar transport of auxin would coordinate tissue cell polarity and would induce vein formation. Here we tested this hypothesis by means of a combination of cellular imaging, molecular genetic analysis, and chemical induction and inhibition. Contrary to predictions of the hypothesis, we find that auxin-induced vein formation occurs in the absence of PIN-FORMED proteins or any known intercellular auxin transporter, that the residual auxin-transport-independent vein-patterning activity relies on auxin signaling, and that a GNOM-dependent signal that coordinates tissue cell polarity to induce vein formation acts upstream of both auxin transport and signaling. Our results reveal synergism between auxin transport and signaling, and their unsuspected control by GNOM, in the coordination of tissue cell polarity during vein patterning, one of the most spectacular and informative expressions of tissue cell polarization in plants.