Substrate Specificity of LACCASE8 Facilitates Polymerization of Caffeyl Alcohol for C-Lignin Biosynthesis in the Seed Coat of <i>Cleome hassleriana</i>

Wang, Xin; Zhuo, Chunliu; Xiao, Xirong; Docampo-Palacios, Maite; Chen, Fang; Dixon, Richard A.

doi:10.1105/tpc.20.00598

Cited by 44 publications

(61 citation statements)

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“…Together with previous findings (Hiraide et al, 2014, 2016), our current data demonstrated that precise localisation of a laccase, CoLac1, with a prominent PA‐polymerisation ability facilitates the S 2 L‐specific deposition of H‐type lignin units during compression wood formation in the coniferous gymnosperm C. obtusa . Similarly, it was recently shown that, in the seed coat of Cleome hassleriana , the seed‐coat‐specific deposition of atypical catechol (C)‐type lignin polymers (catechyl lignin) is mediated by a laccase, ChLac8, which shows a preferential oxidation ability towards C‐type lignin monomer (caffeyl alcohol) (Wang et al, 2020). Collectively, these findings provide evidence that not only the spatial localisation of laccases, but also their biochemical characteristics, impact the spatial patterning of lignin polymerisation in planta .…”

Section: Discussionmentioning

confidence: 99%

Localised laccase activity modulates distribution of lignin polymers in gymnosperm compression wood

et al. 2021

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Summary The woody stems of coniferous gymnosperms produce specialised compression wood to adjust the stem growth orientation in response to gravitropic stimulation. During this process, tracheids develop a compression‐wood‐specific S2L cell wall layer with lignins highly enriched with p‐hydroxyphenyl (H)‐type units derived from H‐type monolignol, whereas lignins produced in the cell walls of normal wood tracheids are exclusively composed of guaiacyl (G)‐type units from G‐type monolignol with a trace amount of H‐type units. We show that laccases, a class of lignin polymerisation enzymes, play a crucial role in the spatially organised polymerisation of H‐type and G‐type monolignols during compression wood formation in Japanese cypress (Chamaecyparis obtusa). We performed a series of chemical‐probe‐aided imaging analysis on C. obtusa compression wood cell walls, together with gene expression, protein localisation and enzymatic assays of C. obtusa laccases. Our data indicated that CoLac1 and CoLac3 with differential oxidation activities towards H‐type and G‐type monolignols were precisely localised to distinct cell wall layers in which H‐type and G‐type lignin units were preferentially produced during the development of compression wood tracheids. We propose that, not only the spatial localisation of laccases, but also their biochemical characteristics dictate the spatial patterning of lignin polymerisation in gymnosperm compression wood.

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Section: Discussionmentioning

confidence: 99%

Localised laccase activity modulates distribution of lignin polymers in gymnosperm compression wood

et al. 2021

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“…In C. hassleriana , accumulation of ChLAC8 parallels that of C‐lignin during seed coat development, and ChLAC8 polymerizes caffeyl alcohol instead of coniferyl alcohol to generate dimers or trimers of caffeyl alcohol in vitro . The accumulation of C‐lignin in the seed coats of transgenic Cleome plants is clearly repressed as a result of inhibition of ChLAC8 expression, implying that ChLAC8 is required for the polymerization of C‐lignin in C. hassleriana (Wang et al, 2020g). In A. thaliana , the lac4 lac11 lac17 triple mutant exhibits a lack of lignification in the vascular and dampened plant growth, whereas lignification of the Casparian strip, which is catalyzed by peroxidase, is not disrupted.…”

Section: Biosynthesis Of Phenylpropanoid Metabolitesmentioning

confidence: 99%

Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions

Dong

Lin

2021

JIPB

729

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Phenylpropanoid metabolism is one of the most important metabolisms in plants, yielding more than 8,000 metabolites contributing to plant development and plant-environment interplay. Phenylpropanoid metabolism materialized during the evolution of early freshwater algae that were initiating terrestrialization and land plants have evolved multiple branches of this pathway, which give rise to metabolites including lignin, flavonoids, lignans, phenylpropanoid esters, hydroxycinnamic acid amides, and sporopollenin. Recent studies have revealed that many factors participate in the regulation of phenylpropanoid metabolism, and modulate phenylpropanoid homeostasis when plants undergo successive developmental processes and are subjected to stressful environments. In this review, we summarize recent progress on elucidating the contribution of phenylpropanoid metabolism to the coordination of plant development and plantenvironment interaction, and metabolic flux redirection among diverse metabolic routes. In addition, our review focuses on the regulation of phenylpropanoid metabolism at the transcriptional, post-transcriptional, post-translational, and epigenetic levels, and in response to phytohormones and biotic and abiotic stresses.

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“…To address this open question, we generated a comprehensive phylogeny of all LACs from 10 taxonomically diverse species with published reference genomes (Figure 5). In contrast to previous phylogenies (McCaig et al, 2005;Turlapati et al, 2011;Zhao et al, 2013;Wang X. et al, 2020;Yonekura-Sakakibara et al, 2020), we used only full-length sequences (to avoid partial homology due to incomplete sequences) and included ascorbate oxidases as an outgroup to distinguish between the two families of multicopper oxidases. We moreover chose a bayesian FIGURE 5 | Phylogenetic analysis of LAC homologs.…”

Section: Laccases Distribution Of Laccases Among Kingdoms and Speciesmentioning

confidence: 99%

Phenoloxidases in Plants—How Structural Diversity Enables Functional Specificity

Blaschek

Pesquet

2021

Front. Plant Sci.

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The metabolism of polyphenolic polymers is essential to the development and response to environmental changes of organisms from all kingdoms of life, but shows particular diversity in plants. In contrast to other biopolymers, whose polymerisation is catalysed by homologous gene families, polyphenolic metabolism depends on phenoloxidases, a group of heterogeneous oxidases that share little beyond the eponymous common substrate. In this review, we provide an overview of the differences and similarities between phenoloxidases in their protein structure, reaction mechanism, substrate specificity, and functional roles. Using the example of laccases (LACs), we also performed a meta-analysis of enzyme kinetics, a comprehensive phylogenetic analysis and machine-learning based protein structure modelling to link functions, evolution, and structures in this group of phenoloxidases. With these approaches, we generated a framework to explain the reported functional differences between paralogs, while also hinting at the likely diversity of yet undescribed LAC functions. Altogether, this review provides a basis to better understand the functional overlaps and specificities between and within the three major families of phenoloxidases, their evolutionary trajectories, and their importance for plant primary and secondary metabolism.

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Substrate Specificity of LACCASE8 Facilitates Polymerization of Caffeyl Alcohol for C-Lignin Biosynthesis in the Seed Coat of Cleome hassleriana

Abstract: LACCASE8 from the model system Cleome hassleriana possesses the unusual property of oxidizing caffeyl alcohol but not coniferyl alcohol and plays a critical role in initiating C-lignin polymerization.

Cited by 44 publications

References 80 publications

Localised laccase activity modulates distribution of lignin polymers in gymnosperm compression wood

Localised laccase activity modulates distribution of lignin polymers in gymnosperm compression wood

Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions

Phenoloxidases in Plants—How Structural Diversity Enables Functional Specificity

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