A polyvalent apoplastic barrier-integrity signaling pathway: Mechanistic elucidation and physiological implications. – MIND-THE-GAP

Extracellular diffusion barriers are central to plant survival and stress resistance: Large parts of the terrestrial surface of our planet have been successfully colonised by plants. The exit of photo-synthetic organisms from their original, aqueous environment and their transition to the fully dry-land adapted life cycles seen in extant higher plants required numerous evolutionary innovations. Key among these innovations was the development of effective, tissue-spanning diffusion barriers that prevent loss of water and allow maintenance of steep concentration gradients between the organism and its environment. Centrally important diffusion barriers in extant plants are the epidermal cuticle of aerial tissues, the Casparian strip and suberin lamellae of the root endodermis and the sporopollenin layer of pollen coats. These barriers often cover very large surface areas and even small defects in them can lead to strong functional impairments, leading to chronic loss of water, nutrients or entry of pathogens. How plants are able to ensure the effective sealing of their diffusion barriers and monitor their integrity is not understood and – to our knowledge –few attempts have been made to address this question.
Recently, work on Arabidopsis mutants with impaired endodermal diffusion barrier has defined the outlines of a signalling pathway whose role might be to allow diffusion barrier surveillance during Casparian strip formation. Intriguingly, central components of this pathway have been implicated not only in Casparian strip formation, but also in forming an intact embryonic cuticle and - based on our recent, unpublished observations – might also have a role in the formation of pollen coats.

Does a common system of barrier surveillance exist that ensures integrity of the major plant diffusion barriers? These findings lead us to speculate that a common signalling module might exist that is repeatedly employed by the plant in very different circumstances in order to ensure the integrity of its different, extracellular diffusion barriers and to stimulate their formation. Here, we propose a number of coordinated experiments that will explore and substantiate this idea and establish the extent to which identical or homologous components are employed in these very different developmental processes. Our aim is to work out whether a common regulatory logic underlies these very diverse barrier formation events. The great fundamental interest of this proposal resides in the opportunity to contextualise a plant signalling pathway and study its modularity and the mechanism underlying its functional adaptation to different developmental circumstances. A more applied interest of our proposal lies in the identification of agonists and antagonists that regulate crucially important diffusion barrier formation in plants and might open avenues for the inducible alteration of these barriers in order to enhance plant resistance to diverse environmental insults.