A Molecular Blueprint of Lignin Repression

doi:10.1016/j.tplants.2019.07.006

Trends in Plant Science

Volume 24, Issue 11, November 2019, Pages 1052-1064

https://doi.org/10.1016/j.tplants.2019.07.006 Get rights and content

Highlights

Negative regulators of lignin biosynthesis are promising tools to tailor biomass properties to meet human requirements.
The Mediator complex adds another level of transcription regulation to the several transcription factors that are known to repress lignification.
Targeted transcript or protein degradation, as well as protein–protein interactions, fine-tune the spatiotemporal pattern of lignification.
Understanding the interactions between genes, non-coding RNAs, and proteins opens new avenues towards understanding secondary cell wall formation.

Although lignin is essential to ensure the correct growth and development of land plants, it may be an obstacle to the production of lignocellulosics-based biofuels, and reduces the nutritional quality of crops used for human consumption or livestock feed. The need to tailor the lignocellulosic biomass for more efficient biofuel production or for improved plant digestibility has fostered considerable advances in our understanding of the lignin biosynthetic pathway and its regulation. Most of the described regulators are transcriptional activators of lignin biosynthesis, but considerably less attention has been devoted to the repressors of this pathway. We provide a comprehensive overview of the molecular factors that negatively impact on the lignification process at both the transcriptional and post-transcriptional levels.

Section snippets

Challenging Lignin

Lignin is a major cell wall component that fulfills fundamental functions in plant development as well as in defense against pests and pathogens. This heteropolymer impregnates the compound middle lamella and the secondary cell walls (SCWs) of cells genetically programmed to be lignified, such as xylem tracheary elements as well as xylem and phloem fibers. Lignin biosynthesis spans the phenylpropanoid and the monolignol pathways, from phenylalanine to p-coumaryl, coniferyl, and sinapyl

Transcriptional Repression of Lignin Biosynthesis

The roles of transcriptional activators promoting lignin biosynthesis have been well documented in various plants, such as thale cress (Arabidopsis thaliana) (reviewed in [12]) and tree species (reviewed in 13, 14). The negative regulators of lignin biosynthesis and their underlying directing networks are tightly controlled.

Post-Transcriptional Repression of Monolignol Biosynthesis and Lignin Polymerization

In addition to the numerous mechanisms of transcriptional regulation that land plants have established to repress monolignol biosynthesis and hence lignification in different tissues and developmental stages, additional post-transcriptional mechanisms have been observed. Post-transcriptional modifications typically affect a restricted number of transcripts/proteins, allowing precise control of the output of a metabolic pathway such as lignin biosynthesis.

Concluding Remarks and Future Perspectives

Further advances in synthetic and molecular biology combine with our growing knowledge about the molecular factors (mainly genes and proteins) driving SCW formation in various tissues and plant species to overcome the possible growth penalty of constitutive overexpression of genes repressing lignification (see Outstanding Questions). As proof of concept, lignin deposition in thale cress was restricted to vessels by controlling the expression of the monolignol biosynthetic gene C4H with the

Acknowledgments

M. Behr is supported by Belgian Fonds de la Recherche Scientifique (FRS-FNRS) research project T.0068.18, and M. Baucher is a Senior Research Associate of the FRS-FNRS. G. Guerriero acknowledges support from the Fonds National de la Recherche, Luxembourg (grant number C16/SR/11289002). J. Grima-Pettenati acknowledges support from the CNRS, the Université Paul Sabatier Toulouse III, and the Laboratoire d'Excellence (Labex) TULIP (ANR-10-LABX-41; ANR-11- IDEX-0002-02).

Glossary

Cis-element: a cis-element is a conserved nucleotide sequence (e.g., the G-box) that is generally found in the promoter region of the regulated gene, and is recognized by a specific family or subfamily of transcription factors (TFs; e.g., MYBs). These TFs are trans-regulating elements because they tune the expression of specific genes through intermolecular interactions. Mediator proteins are also trans-regulating elements.
Differentiation: a suite of incremental cellular and molecular modifications

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The appearance of lignin, 400 million-years ago, has been crucial for the successful land colonization by plants. This complex phenolic polymer which confers hydrophobicity and resistance to degradation to secondary cell walls, is also neosynthesized in response to both biotic and abiotic stresses. Lignin biosynthesis during development is regulated by a complex hierarchical transcriptional gene regulatory network. Notably, distinct abiotic stresses can co-opt different genes of this network, leading to different lignification patterns. Co-optation of this developmental network is a mean to facilitate adaptation to stress by promoting functional adaptation. Supporting this hypothesis, a growing number of transcription factors known to be involved in the regulation of secondary cell wall, were shown to integrate both developmental and environmental signals leading to an increased tolerance to abiotic stresses, such as drought or salinity. On the other hand, some transcription factors known to be involved in stress response were shown to impact lignin biosynthesis as part of the functional adaptation performed by plants to cope with natural constraints. In this review, we focus on the most recent findings on the cross-talk between stress-signaling pathways and regulation of lignin biosynthesis in response to abiotic stress and to a lesser extent to biotic stresses. We consider the transcriptional regulation level which has received much attention and the emerging roles of posttranscriptional and posttranslational regulations in the control of lignin biosynthesis in response to stresses. We end discussing future outlines and challenges to fill gaps in this emerging and exciting research field.
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Citation Excerpt :
SCWs are made of three main components, polysaccharides, lignin and proteins, in proportions depending of the cell type (Kumar, Campbell, & Turner, 2016; Zhong et al., 2019a). The cellular program leading to biogenesis of SCWs is under strong transcriptional and post-transcriptional regulation to allow their precise deposition in targeted cell types (Behr, Guerriero, Grima-Pettenati, & Baucher, 2019; Kumar et al., 2016). Albeit traces of lignin oligomers have been detected in particular red (Calliarthron cheilosporoides) and green (Coleochaete sp.) algae as well as in a bryophyte (Marchantia polymorpha), lignified SCWs are only present in vascular plants (Behr, El Jaziri, & Baucher, 2021).
Primary cell walls are synthesized during plant cell division and elongation whereas secondary cell walls (SCWs) provide rigidity to plant specific tissues that have completed their growth. The cell wall matrix is rich in cellulose, hemicelluloses and pectin polysaccharides as well as various aromatic compounds and proteins. Lignin of the SCW is mainly polymerized after the deposition of the polysaccharide framework. This local environment may affect lignin structure and properties. Hence, the biosynthesis and the function of SCW depend on a large variety of sugar moieties as well as glycosylation reactions. Cellulose is polymerized at the plasma membrane by cellulose synthase complexes while hemicelluloses such as xylan are synthesized in the Golgi and exported to the thickening cell wall. Among other biological processes, cell wall glycoproteins such as arabinogalactan proteins are involved in SCW deposition and structure, as well as sensing of developmental and environmental signals. Finally, in addition to transcriptional regulation, the pools of monolignols and the polymerization of lignin are also modulated through glycosylation reaction. Overall, this chapter illustrates the roles of glucan polymerization and of the de/glycosylation of carbohydrates, proteins and monolignols in the building of SCW matrix, as well as in the regulation of monolignol homeostasis and lignification. We illustrate how the glycosylation of laccases and peroxidases modifies their enzymatic activities. We also point out the differential accumulation of monolignol glucosides in angiosperms and gymnosperms and sum up the main reasons for such a divergence. We explain how glycosylation reactions at the basis of polysaccharides biosynthesis and monolignols' fate partake in the dynamics of the SCW to reach the advanced stages of cellular differentiation characterizing the vascular cells, a specificity of the plant kingdom.
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Lodging is a major problem limiting maize yield worldwide. However, the mechanisms of lodging resistance remain incompletely understood for maize. Here, we evaluated 443 maize accessions for lodging resistance in the field. Five lodging-resistant accessions and five lodging-sensitive accessions were selected for further research. The leaf number, plant height, stem diameter, and rind penetrometer resistance were similar between lodging-resistant and -sensitive inbred lines. The average thickness of sclerenchymatous hypodermis layer was thicker and the vascular area was larger in the lodging-resistant lines compared with lodging-sensitive lines. Although total lignin content in stem tissue did not significantly differ between lodging-resistant and -sensitive lines, phloroglucinol staining revealed that the lignin content of the cell wall in the stem cortex and in the stem vascular tissue near the cortex was higher in the lodging-resistant lines than in the lodging-sensitive lines. Analysis of strand-specific RNA-seq transcriptome showed that a total of 793 genes were up-regulated and 713 genes were down-regulated in lodging-resistant lines relative to lodging-sensitive lines. The up-regulated genes in lodging-resistant lines were enriched in cell wall biogenesis. These results indicated that modification of cell wall biosynthesis would contribute to lodging resistance of maize.
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Trends in Plant Science

ReviewA Molecular Blueprint of Lignin Repression

Highlights

Section snippets

Challenging Lignin

Transcriptional Repression of Lignin Biosynthesis

Post-Transcriptional Repression of Monolignol Biosynthesis and Lignin Polymerization

Concluding Remarks and Future Perspectives

Acknowledgments

Glossary

Trends Plant Sci.

Agric. Ecosyst. Environ.

Adv. Bot. Res.

Mol. Plant

Sci. Rep.

Adv. Bot. Res.

Trends Plant Sci.

Mol. Plant

Mol. Plant

Plant Physiol. Biochem.

Plant Sci.

Gene

J. Proteome

Curr. Biol.

Mol. Cell

J. Biol. Chem.

Cell

J. Plant Physiol.

Plant Gene

Lignin: genetic engineering and impact on pulping

Crit. Rev. Biochem. Mol. Biol.

Down-regulation of cinnamyl alcohol dehydrogenase in transgenic alfalfa (Medicago sativa L.) and the effect on lignin composition and digestibility

Plant Mol. Biol.

Combining enhanced biomass density with reduced lignin level for improved forage quality

Plant Biotechnol. J.

Lignocellulosic biomass: biosynthesis, degradation, and industrial utilization

Eng. Life Sci.

Genes and gene clusters related to genotype and drought-induced variation in saccharification potential, lignin content and wood anatomical traits in Populus nigra

Tree Physiol.

A collection of genetically engineered Populus trees reveals wood biomass traits that predict glucose yield from enzymatic hydrolysis

Sci. Rep.

Abiotic and biotic stresses and changes in the lignin content and composition in plants

J. Integr. Plant Biol.

Long cold exposure induces transcriptional and biochemical remodelling of xylem secondary cell wall in Eucalyptus

Tree Physiol.

Current models for transcriptional regulation of secondary cell wall biosynthesis in grasses

Front. Plant Sci.

Biosynthesis and regulation of phenylpropanoids in plants

CRC. Crit. Rev. Plant Sci.

Recent advances in the transcriptional regulation of secondary cell wall biosynthesis in the woody plants

Front. Plant Sci.

NAC–MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants

Front. Plant Sci.

Xylem tissue specification, patterning, and differentiation mechanisms

J. Exp. Bot.

Navigating the transcriptional roadmap regulating plant secondary cell wall deposition

Front. Plant Sci.

XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem

Plant J.

XYLEM NAC DOMAIN1, an angiosperm NAC transcription factor, inhibits xylem differentiation through conserved motifs that interact with RETINOBLASTOMA-RELATED

New Phytol.

VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis

Plant Cell

Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity

Proc. Natl. Acad. Sci. U. S. A.

FtSAD2 and FtJAZ1 regulate activity of the FtMYB11 transcription repressor of the phenylpropanoid pathway in Fagopyrum tataricum

New Phytol.

Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants

Proc. Natl. Acad. Sci.

Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa

Proc. Natl. Acad. Sci.

Arabidopsis Kelch repeat F-box proteins regulate phenylpropanoid biosynthesis via controlling the turnover of phenylalanine ammonia-lyase

Plant Cell

PtrWRKY19, a novel WRKY transcription factor, contributes to the regulation of pith secondary wall formation in Populus trichocarpa

Sci. Rep.

Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa

Proc. Natl. Acad. Sci. U. S. A.

MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes

Plant Cell Physiol.

Analysis of the DNA-binding activities of the Arabidopsis R2R3-MYB transcription factor family by one-hybrid experiments in yeast

Review
A Molecular Blueprint of Lignin Repression