Different combinations of laccase paralogs non-redundantly control the lignin amount and composition of specific cell types and cell wall layers in Arabidopsis

Vascular plants reinforce the cell walls of the different xylem cell types with lignin, a phenolic polymer. Specific lignin chemistries are conserved between the cell wall layers of each cell type to support their functions. Yet the mechanisms controlling the tight spatial localisation of specific lignin chemistries remain unclear. Current hypotheses focus on a control by monomer biosynthesis and/or export, while their cell wall polymerisation is viewed as random and non-limiting. Here we show that cell wall polymerisation using combinations of multiple different laccases (LACs) non-redundantly and specifically control the lignin chemistry in different cell types and their distinct cell wall layers. We dissected the roles of Arabidopsis thaliana LAC4, 5, 10, 12 and 17 by generating quadruple and quintuple loss-of-function mutants. Different combinatory loss of these LACs lead to specific changes in lignin chemistry affecting both residue ring structures and/or aliphatic tails in specific cell types and cell wall layers. We moreover showed that the LAC-mediated lignification had distinct functions in specific cell types. Altogether, we propose that the spatial control of lignin chemistry depends on different combinations of LACs with non-redundant activities immobilised in specific cell types and cell wall layers.