Distribution, mobility, and anchoring of lignin-related oxidative enzymes in Arabidopsis secondary cell walls

Chou, Eva Yi; Schuetz, Mathias; Hoffmann, Natalie; Watanabe, Yoichiro; Sibout, Richard; Samuels, Lacey

doi:10.1093/jxb/ery067

Cited by 76 publications

(78 citation statements)

References 41 publications

(70 reference statements)

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“…As genes encoding many peroxidases and laccases were equally highly expressed in both cell types, it is likely that products of LACCASE and PEROXIDASE genes expressed in ray cells are secreted into the cell wall of ray cells, from where some of them diffuse in the apoplastic fluid into the developing tracheid cell walls, where they function in the oxidative polymerization of coniferyl alcohol. However, a recent study in Arabidopsis showed that a lignification-related laccase, LAC4, was mobile in the primary cell wall but nonmobile in the secondary cell wall, suggesting that it was anchored to the secondary cell wall (Chou et al, 2018). Conifer laccases in native, glycosylated form are larger (70-120 kD; Koutaniemi et al, 2015) than peroxidases (35-60 kD; Koutaniemi et al, 2005).…”

Section: Many Genes Encoding Oxidative Enzymes Are Highly Expressed Imentioning

confidence: 99%

“…It is possible that peroxidases but not laccases are small enough to fit into the cell wall pores of partially lignified cell walls and can therefore move in the apoplastic fluid. Alternatively, laccases may be attached to some secondary cell wall components (Chou et al, 2018). Hence, it seems likely that the parenchymatous ray cells are not only participating in tracheid cell wall lignification by synthesizing monolignols but also by producing the enzymes (e.g.…”

Section: Many Genes Encoding Oxidative Enzymes Are Highly Expressed Imentioning

confidence: 99%

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Ray Parenchymal Cells Contribute to Lignification of Tracheids in Developing Xylem of Norway Spruce

et al. 2019

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A comparative transcriptomic study and a single-cell metabolome analysis were combined to determine whether parenchymal ray cells contribute to the biosynthesis of monolignols in the lignifying xylem of Norway spruce (Picea abies). Ray parenchymal cells may function in the lignification of upright tracheids by supplying monolignols. To test this hypothesis, parenchymal ray cells and upright tracheids were dissected with laser-capture microdissection from tangential cryosections of developing xylem of spruce trees. The transcriptome analysis revealed that among the genes involved in processes typical for vascular tissues, genes encoding cell wall biogenesis-related enzymes were highly expressed in both developing tracheids and ray cells. Interestingly, most of the shikimate and monolignol biosynthesis pathway-related genes were equally expressed in both cell types. Nonetheless, 1,073 differentially expressed genes were detected between developing ray cells and tracheids, among which a set of genes expressed only in ray cells was identified. In situ single cell metabolomics of semi-intact plants by picoliter pressure probe-electrospray ionization-mass spectrometry detected monolignols and their glycoconjugates in both cell types, indicating that the biosynthetic route for monolignols is active in both upright tracheids and parenchymal ray cells. The data strongly support the hypothesis that in developing xylem, ray cells produce monolignols that contribute to lignification of tracheid cell walls.

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Section: Many Genes Encoding Oxidative Enzymes Are Highly Expressed Imentioning

confidence: 99%

Section: Many Genes Encoding Oxidative Enzymes Are Highly Expressed Imentioning

confidence: 99%

Ray Parenchymal Cells Contribute to Lignification of Tracheids in Developing Xylem of Norway Spruce

et al. 2019

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“…Putative nucleation sites for lignin initiation include cellwall-bound hydroxycinnamates, pectin, and cell wall proteins (Ralph et al, 1995;Boerjan et al, 2003). Similarly, laccase or peroxidase enzymes that drive lignin polymerization may be specifically tethered to the cell corners and middle lamellae (Boerjan et al, 2003;Chou et al, 2018;Tobimatsu & Schuetz, 2019), but irrefutable evidence for any one mechanism is still lacking. Moreover, previously observed differences in lignin composition between middle lamellae and adjacent cell walls (Whiting & Goring, 1982) are still unexplained.…”

Section: Challenging the Model Of Lignificationmentioning

confidence: 99%

Atypical lignification in eastern leatherwood (Dirca palustris)

et al. 2020

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Summary Lignin is a complex phenolic biopolymer found mainly in the secondary cell walls of vascular plants, where it contributes to mechanical strength, water conduction, and plant defence. We studied the lignin of eastern leatherwood (Dirca palustris) because this slow‐growing woody shrub is known for its flexible stems. Various analytical techniques and microscopy methods were employed to examine the composition and distribution of lignin and structural polysaccharides in leatherwood xylem in comparison with trembling aspen (Populus tremuloides) and white spruce (Picea glauca). We found that leatherwood has low overall levels of lignin, a high syringyl lignin content, and a unique distribution of lignin. Most remarkably, the cell corners and middle lamellae remain unlignified in mature xylem. These findings help explain the flexibility of leatherwood and also call into question the classical model of lignification, which purports that lignin polymerization begins in the cell corners and middle lamellae. This atypical lignification regime vividly illustrates the diversity in plant secondary cell wall formation that abounds in nature and casts leatherwood as a new model for the study of lignin biogenesis.

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“…LAC4, also called IRREGULAR XYLEM 12 (11) and LAC17 are expressed in vessels and xylary fibers in the stem (12). LAC4 localizes to secondary cell wall domains of proto-and metaxylem vessels, as well as vessels, xylary and interfascicular fibers of inflorescence stems (12)(13)(14)(15). Mutant lines of lac4 and lac4 lac17 have collapsed xylem vessels and reduced lignin content in total stem biomass (12).…”

Section: Introductionmentioning

confidence: 99%

“…In the Arabidopsis stem xylem vessels, mutation of PERs partially impact lignification (19,20). It was proposed that both enzymes act sequentially in the lignin polymerization of a same cell type, although it has not been excluded that they individually lignify different cell types (8,15,21). Cell cultures of the gymnosperm Norway spruce release lignin polymers into the growth medium (22).…”

Section: Introductionmentioning

confidence: 99%

High-order mutants reveal an essential requirement for peroxidases but not laccases in Casparian strip lignification

Rojas-Murcia

Hématy

Lee

et al. 2020

Preprint

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The invention of lignin has been at the heart of plants' capacity to colonize land, allowing them to grow tall, transport water within their bodies and protect themselves against various stresses.Consequently, this polyphenolic polymer, that impregnates the cellulosic plant cell walls, now represents the second most abundant polymer on Earth, after cellulose itself. Yet, despite its great physiological, ecological and economical importance, our knowledge of lignin biosynthesis in vivo, especially the crucial last steps of polymerization within the cell wall, remains vague. Specifically, the respective roles and importance of the two main polymerizing enzymes classes, laccases and peroxidases have remained obscure. One reason for this lies in

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Distribution, mobility, and anchoring of lignin-related oxidative enzymes in Arabidopsis secondary cell walls

Abstract: Laccases and peroxidases localize to different wall domains in Arabidopsis stems. These enzymes are tightly anchored in the secondary cell wall, providing a mechanism for spatial control of lignification.

Cited by 76 publications

References 41 publications

Ray Parenchymal Cells Contribute to Lignification of Tracheids in Developing Xylem of Norway Spruce

Ray Parenchymal Cells Contribute to Lignification of Tracheids in Developing Xylem of Norway Spruce

Atypical lignification in eastern leatherwood (Dirca palustris)

High-order mutants reveal an essential requirement for peroxidases but not laccases in Casparian strip lignification

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