Plant biomechanics and resilience to environmental changes are controlled by specific lignin chemistries in each vascular cell type and morphotype

Abstract

The biopolymer lignin is deposited in the cell walls of vascular cells and is essential for long-distance water conduction and structural support in plants. Different vascular cell types contain distinct and conserved lignin chemistries, each with specific aromatic and aliphatic substitutions. Yet, the biological role of this conserved and specific lignin chemistry in each cell type remains unclear. Here, we investigated the roles of this lignin biochemical specificity for cellular functions by producing single cell analyses for three cell morphotypes of tracheary elements, which all allow sap conduction but differ in their morphology. We determined that specific lignin chemistries accumulate in each cell type. Moreover, lignin accumulated dynamically, increasing in quantity and changing in composition, to alter the cell wall biomechanics during cell maturation. For similar aromatic substitutions, residues with alcohol aliphatic functions increased stiffness whereas aldehydes increased flexibility of the cell wall. Modifying this lignin biochemical specificity and the sequence of its formation impaired the cell wall biomechanics of each morphotype and consequently hindered sap conduction and drought recovery. Together, our results demonstrate that each sap-conducting vascular cell type distinctly controls their lignin biochemistry to adjust their biomechanics and hydraulic properties to face developmental and environmental constraints.

Downregulation of barley ferulate 5-hydroxylase dramatically alters straw lignin structure without impact on mechanical properties

“…However, in wheat, lignin content was not associated with straw breaking force but a lower proportion of S lignin appeared to increase it ( Muhammad et al., 2020 ). In Arabidopsis fah1 F5H mutants, stiffness was increased compared to wild type in apical and middle stem segments, but flexibility was unaltered between fah1 and wild type plants ( Ménard et al., 2022 ). Differences in stem architecture between dicots and grasses and indeed between individual species are likely to complicate any simplistic generalized interpretation of the effects of lignin characteristics on plant mechanical properties since even different morphotypes of tracheary element have different lignin chemistries and mechanical properties ( Ménard et al., 2022 ).…”

“…In Arabidopsis fah1 F5H mutants, stiffness was increased compared to wild type in apical and middle stem segments, but flexibility was unaltered between fah1 and wild type plants ( Ménard et al., 2022 ). Differences in stem architecture between dicots and grasses and indeed between individual species are likely to complicate any simplistic generalized interpretation of the effects of lignin characteristics on plant mechanical properties since even different morphotypes of tracheary element have different lignin chemistries and mechanical properties ( Ménard et al., 2022 ). In our work, it is promising to see that radical changes to lignin composition and structure in HvF5H1 suppressed plants is not accompanied by any change to straw strength.…”

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

“…Lignin is a complex, heterogeneous phenolic polymer that is deposited in the cell walls of specialized cell types ( Meents et al, 2018 ). Associated with the evolutionary emergence of the plant vasculature and the transition to terrestrial habitats, lignin confers structural rigidity, and hydrophobicity to the vascular system ( Eriksson et al, 1991 ; Ménard et al, 2022 ). Lignin deposition proceeds in three steps: biosynthesis of phenolic monomers, mostly phenylpropanoids, in the cytoplasm ( Barros et al, 2015 ); their export into the apoplast ( Perkins et al, 2019 ); and their subsequent oxidative polymerization by radical coupling catalyzed by laccases (LACs) and class III peroxidases (PRXs) in the cell wall ( Blaschek and Pesquet, 2021 ).…”

“…Lignin is essential for structural support at the organ level, as drastic reductions in lignin content lead to dwarf plants unable to stand upright and lodging ( Bonawitz and Chapple, 2010 ; Muszynska et al, 2021 ). Lignin is equally crucial at the cellular level, as reductions in lignin levels impair the biomechanical capacity of TEs to withstand the negative pressures required to transport water ( Ménard et al, 2022 ). In addition, most angiosperms and some gnetales also develop lignified xylem fibers located within (xylary fibers, XFs) or between (interfascicular fibers, IFs) vascular bundles, which fine-tune the mechanical properties of plant organs ( Zhong and Ye, 1999 ).…”

“…Lignin concentration is generally higher in the secondary cell walls (SCWs) of TEs than in the SCWs of fibers, as well as generally higher in primary cell walls/middle lamella (CML) and cell corners (CCs) than SCWs ( Serk et al, 2015 ). However, large variations are also observed between different TE morphotypes, with early forming protoxylem (PX) TEs being far less lignified than later forming metaxylem (MX) TEs ( Ménard et al, 2022 ). Lignin composition, depending in part on the proportion of monomers with different phenolic ring substitutions, varies drastically between cell types and cell wall layers, with fiber SCWs enriched in S residues, TE SCWs enriched in G residues, and CML/CCs at the interface of these two cell types enriched in H residues ( Terashima and Fukushima, 1988 ; Fukushima and Terashima, 1990 ).…”