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

Abstract

Vascular plants reinforce the cell walls of the different xylem cell types with lignin phenolic polymers. Distinct lignin chemistries differ between each cell wall layer and each cell type to support their specific functions. Yet the mechanisms controlling the tight spatial localization of specific lignin chemistries remain unclear. Current hypotheses focus on control by monomer biosynthesis and/or export, while cell wall polymerization is viewed as random and non-limiting. Here we show that combinations of multiple individual laccases (LACs) are nonredundantly and specifically required to set 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. Loss of these LACs in different combinations led to specific changes in lignin chemistry affecting both residue ring structures and/or aliphatic tails in specific cell types and cell wall layers. Moreover, we showed that LAC-mediated lignification has distinct functions in specific cell types, waterproofing fibers and strengthening vessels. Altogether, we propose that the spatial control of lignin chemistry depends on different combinations of LACs with nonredundant activities immobilized in specific cell types and cell wall layers.

Modulation of lignin biosynthesis for drought tolerance in plants

“…For example, AtPRX2 and AtPRX71 prefer the S unit over the G unit for oxidation ( Shigeto et al., 2014 ). Similarly, genetic analysis using multiple LAC mutants brought further support to the idea that lignin deposition is mediated by cell type–specific LACs ( Blaschek et al., 2023 ). Mutation of LAC4 , LAC11 , and LAC17 , which are highly expressed in lignifying tissue, significantly reduced lignin accumulation in stems and roots ( Zhao et al., 2013 ).…”

“…It is also worth mentioning that LAC4 , LAC5 , LAC10 , LAC12 , and LAC17 are less important for lignin accumulation in protoxylem than other lignified cell types. Similarly, mutation of the above five LAC s did not affect mechanical strengthening of secondary xylem TEs ( Blaschek et al., 2023 ). These results indicate that additional LAC s are involved in lignin accumulation in protoxylem and secondary xylem.…”

“…More specifically, LAC4 plays a prominent role in lignin deposition in metaxylem, while LAC17 is important for lignin deposition in interfascicular and xylary fibers. In addition to these LAC genes, LAC5 , LAC10 , and LAC12 nonredundantly alter lignin accumulation in different lignified cell types ( Blaschek et al., 2023 ). It is also worth mentioning that LAC4 , LAC5 , LAC10 , LAC12 , and LAC17 are less important for lignin accumulation in protoxylem than other lignified cell types.…”

“…These results indicate that additional LAC s are involved in lignin accumulation in protoxylem and secondary xylem. In addition to lignin accumulation, LAC affects cell type specific ring structure and terminal residue composition in lignin ( Blaschek et al., 2023 ). LAC4 and LAC17 predominantly regulate accumulation of S residue in interfascicular fibers, while LAC4 , LAC12 , and LAC17 are involved in accumulation of S residue in xylary fibers.…”

Integrated QTL Mapping, Meta-Analysis, and RNA-Sequencing Reveal Candidate Genes for Maize Deep-Sowing Tolerance

“…In GWAS, Chen et al [61] identified GRMZM2G035506 (POD7), which was located near the PZE-105098349 marker and regulated the growth of deep-sowing maize seedlings. Leonard et al [62] proposed that the spatial control of lignin chemistry depends on different combinations of laccase (LAC) with nonredundant activities immobilized in specific cell types and cell wall layers. In this study, we also identified two LAC genes (i.e., GRMZM2G447271 and GRMZM2G336337) in MQTL8-1 region that were annotated to the lignin catabolic process (GO:0046274).…”