Life Beyond Death: The Formation of Xylem Sap Conduits

Ménard, Delphine; Escamez, Sacha; Tuominen, Hannele; Pesquet, Edouard

doi:10.1007/978-3-319-21033-9_3

Cited by 8 publications

(6 citation statements)

References 89 publications

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“…During their differentiation, TEs reinforce their primary cell walls (PCWs) with patterned secondary cell walls (SCWs), and subsequently remove their intracellular contents by programmed cell death. This hollowing out of TEs triggers their water conducting function, forming unobstructed tubes with thickened and regularly patterned sides ( Derbyshire et al, 2015 ; Ménard et al, 2015 ). As the plant grows, new TEs form, die, and connect both longitudinally and laterally to other TEs to conduct water throughout the plant ( Ménard and Pesquet, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2022

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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.

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Section: Introductionmentioning

confidence: 99%

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

et al. 2022

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“…Biochemical analyses of cell walls using pyrolysis coupled to gas chromatography and mass spectrometry (GC–MS) showed that unlike dividing parenchyma, 14-day-old TEs accumulate large amounts of lignin mainly composed of G residues, H, and minor amounts of S residues ( Figure 1C ) similarly to that previously reported for isolated TEs in other systems ( Yamamura et al, 2011 ; Pesquet et al, 2019 ). We selected candidate LAC paralogs based on high co-expression levels with the SCW formation marker gene CELLULOSE SYNTHASE CATALYTIC SUBUNIT A7 ( CESA7 , also named IRREGULAR XYLEM 3 [ IRX3 ]) as well as the TE autolysis marker gene XYLEM CYSTEIN PROTEASE 2 ( XCP2 ) ( Ménard et al, 2015 ). This approach identified Arabidopsis LAC s 4 , 5 , 10 , 11 , 12 , and 17 as being co-upregulated during TE SCW formation and potentially implicated in vascular lignification ( Figure 1, D and E ).…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2022

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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.

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“…LAC paralogs non-redundantly and synergistically affect stem growth To discriminate which of the 17 laccase paralogs are implicated in the lignification of secondary cell walls in xylem cells, we analysed available gene expression data (micro-array and RNA sequencing) from A. thaliana inducible pluripotent cell cultures triggered to differentiate into TEs (Derbyshire et al 2015). Candidate LAC paralogs were selected based on high co-expression levels with SCW formation marker gene CesA7 /IRX3 and TE autolysis marker gene XCP2 (Ménard et al 2015). This approach identified A. thaliana LACs 4, 5, 10, 11, 12 and 17 as co-up-regulated during TE SCW formation and potentially implicated in vascular lignification (figure S1).…”

Section: Resultsmentioning

confidence: 99%

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

Blaschek

Murozuka

Ménard

et al. 2022

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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 A. 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.

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Life Beyond Death: The Formation of Xylem Sap Conduits

Cited by 8 publications

References 89 publications

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

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

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

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

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