Paralogues of the PXY and ER receptor kinases enforce radial patterning in plant vascular tissue.

Abstract

Plant cell walls do not allow cells to migrate, thus plant growth and development is entirely the consequence of changes to cell division and cell elongation. Where tissues are arranged in concentric rings, expansion of inner tissue, such as that which occurs during vascular development, must be coordinated with cell division and/or expansion of the outer tissue layers, endodermis, cortex, and epidermis, in order for tissue integrity to be maintained. Little is known of how coordination between cell layers occurs, but non-cell autonomous signalling could provide an explanation. Endodermis-derived EPIDERMAL PATTERNING FACTOR-LIKE (EPFL) ligands have been shown to signal to the ERECTA (ER) receptor kinase present in the phloem. ER interacts with PHLOEM INTERCALLATED WITH XYLEM (PXY), a receptor present in the procambium. The PXY ligand, TRACHEARY ELEMENT DIFFERENTIATION INHIBITORY FACTOR (TDIF) is derived from CLE41 which is expressed in the phloem. These factors therefore represent a mechanism by which intertissue signalling could occur to control radial expansion between vascular and non-vascular tissue in plant stems. Here we show that ER regulates expression of PXY paralogues, PXL1 and PXL2, and that in turn PXY, PXL1 and PXL2 together with ER, regulate the expression of ERL1 and ERL2, genes paralogous to ER. PXY, PXL1, PXL2 and ER also regulate the expression of ER-ligands. Genetic analysis of these six receptor kinase genes demonstrated that they are required to control organisation, proliferation and cell size across multiple tissue layers. Taken together, our experiments demonstrate that ER signalling attenuates PXL expression in the stem, thus influencing vascular expansion and patterning. We anticipate that similar regulatory relationships, where tissue growth is controlled via cell signals moving across different tissue layers, will coordinate tissue layer expansion throughout the plant body.