Lignin accumulates in the cell walls of specialized cell types to enable plants to stand upright and conduct water and minerals, withstand abiotic stresses, and defend themselves against pathogens. These functions depend on specific lignin concentrations and subunit composition in different cell types and cell wall layers. However, the mechanisms controlling the accumulation of specific lignin subunits, such as coniferaldehyde, during the development of these different cell types are still poorly understood. We herein validated the Wiesner test (phloroglucinol/HCl) for the restrictive quantitative in situ analysis of coniferaldehyde incorporation in lignin. Using this optimized tool, we investigated the genetic control of coniferaldehyde incorporation in the different cell types of genetically-engineered herbaceous and woody plants with modified lignin content and/or composition. Our results demonstrate that the incorporation of coniferaldehyde in lignified cells is controlled by (a) autonomous biosynthetic routes for each cell type, combined with (b) distinct cell-to-cell cooperation between specific cell types, and (c) cell wall layer-specific accumulation capacity. This process tightly regulates coniferaldehyde residue accumulation in specific cell types to adapt their property and/or function to developmental and/or environmental changes.
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.
prepared the samples for metabolomic analysis. R.V. and G.G. analyzed the metabolites in different mulberry cultivars and interpreted the data. N.T. and T.I. contributed to histochemical analysis and pulp preparation, respectively. M.Y. and N. prepared milled wood samples and M.Y. analyzed lignin structure by thioacidolysis. S.L., H.K., and J.R. prepared samples for NMR and performed NMR analysis and interpretation of the data. S.S. and N.M. analyzed the monomeric composition of cell wall polysaccharides. N and M.U. managed cultivated plants. S.K. wrote the
Lignin
is a phenolic polymer accumulating in the cell walls of
specific plant cell types to confer unique properties such as hydrophobicity,
mechanical strengthening, and resistance to degradation. Different
cell types accumulate lignin with specific concentration and composition
to support their specific roles in the different plant tissues. Yet
the genetic mechanisms controlling lignin quantity and composition
differently between the different lignified cell types and tissues
still remain poorly understood. To investigate this tissue-specific
genetic regulation, we validated both the target molecular structures
as well as the linear semiquantitative capacity of Raman microspectroscopy
to characterize the total lignin amount, S/G ratio, and coniferyl
alcohol content in situ directly in plant biopsies.
Using the optimized method on stems of multiple lignin biosynthesis
loss-of-function mutants revealed that the genetic regulation of lignin
is tissue specific, with distinct genes establishing nonredundant
check-points to trigger specific compensatory adjustments affecting
either lignin composition and/or cell wall polymer concentrations.
We previously succeeded in enhancing wood formation of wood in transgenic poplar plants by overexpressing secondary wall NAM/ATAF/CUC (NAC) domain protein 1 from Oryza sativa (OsSWN1), a transcription factor 'master regulator' of secondary cell wall formation in rice, under control of the fiber preferential NST3/SND1 promoter from Arabidopsis. Transgenic plants had an increased cell wall thickness and cell wall density of individual cells in the secondary xylem of stems as well as an increased wood density. OsSWN1 triggers the induction of polysaccharide and lignin biosynthetic gene expressions, however, resulting in no significant impact on the lignin content in the transgenic plants. In contrast, wet and dry chemical analyses of lignin revealed changes in S/G ratio and in the composition of lignin interunit linkages in transgenic lines. The results from gene expression analysis suggest that the structural changes in lignin were due to an unbalanced induction of lignin biosynthetic genes in transgenic lines. Our present data indicate that the overexpression of the chimeric transcription factor causes accelerated deposition of secondary cell wall components including lignin and polysaccharides through an acquired mechanism.
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