Cellular Control and Physiological Importance of Vascular Lignification

Sammanfattning: Lignin is indispensable for vascular plants. It allows their cells to coalesce into gravity-defying giants, hardens them to withstand pressures and predators, and waterproofs them to allow the flow of water only where it is advantageous. Lignin fulfils these different functions as a structural component of specialised cell walls in a wide range of different tissues and cell types. Between them, lignin shows great heterogeneity in its concentration and composition. The biosynthesis of lignin proceeds via monomer biosynthesis in the cell, export of the monomers into the apoplast and oxidative polymerisation by laccases (LACs) and class III peroxidases (PRXs) in the cell wall. In this thesis, I investigated how these processes are regulated to allow distinct lignification programs in different cell types and even adjacent cell wall layers (I–III) and what physiological advantages these differences in lignin amount and composition confer to the plant (IV). In paper I and II, we optimised and validated the histochemical Wiesner test and Raman microspectroscopy for the in situ quantitative analysis of lignin. We then used those techniques to map the cell autonomous and cell–cell cooperative genetic programs that regulate lignin monomer biosynthesis in the vasculature of Arabidopsis thaliana and Populus. Because lignin monomers are mobile in the cell wall prior to polymerisation, the sophisticated, cell type-specific genetic regulation of lignin monomer biosynthesis alone cannot explain the lignin differences observed between adjacent cell wall layers. In paper III, we therefore characterised five LACs paralogs involved in lignification, showing that they fine-tuned lignification at the nanoscale through distinct patterns of activity and substrate specificity. But what is the advantage of such a complex, layered control of lignification? In paper IV we began to answer this question by showing that different cell types – and even the same cell type in different developmental contexts – relied on distinct lignin amounts and compositions to withstand the unique stresses they were exposed to. Altogether, the work presented herein highlights how finely lignification is controlled the on cellular and sub-cellular scale, and how this regulation allows plants to fully exploit the versatile functions of lignin.