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Journal ArticleDOI

A Molecular Blueprint of Lignin Repression

TL;DR: This work provides a comprehensive overview of the molecular factors that negatively impact on the lignification process at both the transcriptional and post-transcriptional levels.
About: This article is published in Trends in Plant Science.The article was published on 2019-11-01 and is currently open access. It has received 20 citations till now. The article focuses on the topics: Lignocellulosic biomass.

Summary (3 min read)

Review

  • The Mediator complex adds another level of transcription regulation to the several transcription factors that are known to repress.
  • The need to tailor the lignocellulosic biomass for more efficient biofuel production or for improved plant digestibility has fostered considerable advances in their understanding of the lignin biosynthetic pathway and its regulation.
  • The authors provide a comprehensive overview of the molecular factors that negatively impact on the lignification process at both the transcriptional and post-transcriptional levels.
  • Understanding the interactions between genes, non-coding RNAs, and proteins opens new avenues towards understanding secondary cell wall formation.

Transcriptional Repression of Lignin Biosynthesis

  • Negative regulation of lignin biosynthesis is achieved through diverse mechanisms ranging from DNA accessibility to targeted proteolysis.
  • The process, the timing, and the location of differentiation are under stringent genetic regulation.
  • Usually TFs, also known as Heterodimer.
  • An RNA that is not translated into protein, also known as Non-coding RNA.

NAC TFs, the Two Sides of SCW Regulation

  • Members of the NAC family act as first- and second-level master switches in the regulation of a battery of downstream TFs and SCW biosynthetic genes [15–18].
  • VND-INTERACTING 2 (VNI2) is a transcriptional repressor reported to regulate the timing and spatial regulation of xylem cell development [21].
  • The SCW activator NST2 is negatively transcriptionally regulated by WRKY12 , which binds to the W-box cis-element in theNST2 promoter region (Table 1) [25].
  • An intron-retained (IR) splice variant PtrVND6C1IR negatively regulates the expression of PtrMYB021 (a poplar ortholog of AtMYB46) by forming heterodimers with the full-size PtrVND6s, suppressing their positive transcriptional activity .
  • In addition, PtrVND6-C1IR downregulates the expression of five full-size PtrVND6s.

Key Figure

  • PtrhAT PtrMYB021 Transcriptional complex LAC AtVNDs AtVND7 AtVNI2 AtXND1 Active PtrAldOMT2 P Ser 123 Ser125 Inactive PtrAldOMT2 LTF1 Phosphorylated LTF1 U EgH1.3 TrendsinPlantScience.
  • In this review the authors describe alternatively spliced proteins regulating the expression of closely related coding genes.

R2R3 MYBs, the Gatekeepers of SCW Formation and Lignification

  • Some members of the R2R3-MYB TF family positively regulate gene expression of phenylpropanoid and lignin biosynthetic genes containing AC-rich cis-elements in their promoters [30], such as the 7 bp sequence ACC(A/T)A(A/C)(T/C), termed the secondary wall MYB-responsive element (SMRE) [31,32].
  • The importance of MYBs as repressors of phenylpropanoid metabolism has been highlighted in a recent review [33].
  • AtMYB4 belongs to subgroup 4 and, as the other proteins from this subgroup (AtMYB3, AtMYB7, and AtMYB32), contains an EARlike repression motif in its C-terminus [36].
  • AtMYB4 is downregulated in thale cress ectopic lignification de-etiolated 3, pom-pom 1, and ectopic lignification 1 mutants [38], suggesting that it could negatively regulate lignin biosynthesis.
  • Notably, PtrEPSP-TF harbors an additional N-terminal HTH DNA-binding motif that partially targets this protein to the nucleus, where it acts as a transcriptional repressor of its direct target PtrhAT, a hAT transposase family gene.

KNOX, BELL, and Homeodomain: from Cell Division to Fiber SCW Thickening

  • Some members of the THREE AMINO ACID LOOP EXTENSION (TALE) family of homeodomain (HD) proteins may play a role in the repression of lignin biosynthesis .
  • The cooperative heterodimer becomes completely contained in the nucleus, and the expression of the target genes is dramatically reduced relative to individual BELL or KNOX proteins [22,71].
  • The heterodimer KNAT7–BLH6 negatively regulates the commitment to SCW formation in interfascicular fibers of thale cress through repression of REVOLUTA , which encodes a HD-leucine zipper TF binding to the sequence GTAATNATTAC [65,72].
  • Indeed, the athb15 mutant showed increased xylan and lignin contents in the pith as well as higher expression of SCW genes [81].
  • Of note, KNOX are also part of the transcriptional network regulating the formation of tension wood in poplar [85] that is characterized by the presence of a thick, weakly lignified, cellulose-rich gelatinous layer.

Mediator, a Molecular Hub Coordinating Lignin Biosynthesis with Plant Growth

  • The ’mediator of RNA polymerase II transcription’, or Mediator complex (MED), is essential to transduce signals (both positively and negatively regulating gene expression) to the transcription machinery via direct interactions with specific TFs [86].
  • Among the 27 MED subunits identified in thale cress [87], several negatively regulate the phenylpropanoid and monolignol biosynthetic pathways, contributing to the homeostasis of this family of secondary metabolites.
  • The lignin monomeric composition is drastically modified in the triple mutant, consisting almost exclusively of H-lignin subunits (95% vs <2% in the wild type), suggesting that MED5a and MED5b are likely to have other functions [90].
  • Dolan and colleagues [91] have also demonstrated that the MED5b phenotype requires functional MED2, MED16, and MED23, which probably physically and functionally interact with MED5, as do their homologs in humans [92].

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.

Non-Coding RNAs, Emerging Regulators for Genetic Control of Lignin Deposition

  • MicroRNAs are small non-coding RNAs that post-transcriptionally regulate many aspects of plant development.
  • Their expression is developmentally regulated and/or under the control of external stimuli such as abiotic stress or nutrient availability [93,94].
  • Overexpression of ptr-miR397a significantly reduces the expression of 17 of the 34 LAC found in poplar differentiating xylem, the global LAC activity of this tissue, and the lignin content of the whole plant [26].
  • Similarly, 18 conserved miRNAs targeting 80 genes were found in hemp, where they may have similar functions to flax miRNAs [98].
  • These lncRNAs may be directly functional or serve as precursors for miRNA sequences such asmiR397 [101], and provide a further level of complexity in the regulation of lignin biosynthesis.

Protein Ubiquitination: the Signaling Wave to the Grave

  • PAL catalyzes the rate-limiting step of the phenylpropanoid pathway and thus constitutes an ideal target for regulating the flux of derived secondary metabolites.
  • Thale cress KFB01, KFB20, KFB39, and KFB50 physically interact with the four PAL isozymes, thereby regulating the biosynthesis of phenylpropanoids during plant development and in response to environmental stimuli [27,103].
  • The hemp ortholog of KFB39 is upregulated in mature bast fibers, suggesting a role for KFBs in the hypolignification of this cell type [83].

Switching On/Off Enzymatic Activity with Phosphorylation

  • Phosphorylation is a widespread post-translational modification which may impact on the lignification process.
  • Monophosphorylation of PtrAldOMT2 (that catalyzes the methylation of 5-hydroxyconiferaldehyde to sinapaldehyde) at either Ser123 or Ser125 inhibits its activity [105], in line with the observation that the pool of monolignol biosynthetic enzymes is usually not phosphorylated in vivo [106].
  • The biological significance of this switch remains unknown.
  • Alternatively, phosphorylation may also constitute a signal for protein degradation through proteasome activity.
  • By screening TFs binding to the poplar 4CL promoter, Gui and colleagues identified a lignin biosynthesis-associated factor, LTF1, that represses several genes from this pathway (PAL2, C4H1, C3H2, 4CL1, CAld5H, COMT2, and CCoAOMT1) and decreases lignin content in overexpressing lines [107].

Concluding Remarks and Future Perspectives

  • Further advances in synthetic and molecular biology combine with their 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).
  • Similarly, the dwarf thale cress ccr1 mutant was rescued by driving the expression of CCR1 in metaxylem and protoxylem vessels through a proSNBE promoter transcriptionally activated by VND6 and VND7 [109].
  • Targeted lignin biosynthesis repression may thus be achieved through temporal and/or spatial restriction of the activity of a selected gene using suitable promoters.
  • Omics-based predictive analysis of variables determining wood quality following targeted gene downregulation [110] constitutes a valuable tool to optimize strategies.
  • DNA methylation contributes to the regulation of cotton fiber development and can modulate the production of reactive oxygen species or the biosynthesis of lipids, flavonoids, and ascorbate [111].

Acknowledgments

  • 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 TULIP (ANR-10-LABX-41; ANR-11- IDEX0002-02).

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Journal ArticleDOI
TL;DR: Overexpression of VlbZIP30 improves drought tolerance, characterized by a reduction in the water loss rate, maintenance of an effective photosynthesis rate, and increased lignin content in leaves under drought conditions.
Abstract: Drought stress severely affects grapevine quality and yield, and recent reports have revealed that lignin plays an important role in protection from drought stress. Since little is known about lignin-mediated drought resistance in grapevine, we investigated its significance. Herein, we show that VlbZIP30 mediates drought resistance by activating the expression of lignin biosynthetic genes and increasing lignin deposition. Transgenic grapevine plants overexpressing VlbZIP30 exhibited lignin deposition (mainly G and S monomers) in the stem secondary xylem under control conditions, which resulted from the upregulated expression of VvPRX4 and VvPRX72. Overexpression of VlbZIP30 improves drought tolerance, characterized by a reduction in the water loss rate, maintenance of an effective photosynthesis rate, and increased lignin content (mainly G monomer) in leaves under drought conditions. Electrophoretic mobility shift assay, luciferase reporter assays, and chromatin immunoprecipitation-qPCR assays indicated that VlbZIP30 directly binds to the G-box cis-element in the promoters of lignin biosynthetic (VvPRX N1) and drought-responsive (VvNAC17) genes to regulate their expression. In summary, we report a novel VlbZIP30-mediated mechanism linking lignification and drought tolerance in grapevine. The results of this study may be of value for the development of molecular breeding strategies to produce drought-resistant fruit crops.

43 citations

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TL;DR: Results indicated that modification of cell wall biosynthesis would contribute to lodging resistance of maize.
Abstract: 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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TL;DR: The results provide evidence that both OsWRKY36 andOsWRKY102 are associated with repression of rice lignification, and relative abundances of guaiacyl and p-coumarate units were slightly higher and lower, respectively, in the WRKY mutant lignins compared with those in the wild-type lign ins.

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References
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Journal ArticleDOI
TL;DR: An Arabidopsis thaliana line that is mutant for the R2R3 MYB gene, AtMYB4, shows enhanced levels of sinapate esters in its leaves, indicating that derepression is an important mechanism for acclimation to UV‐B in A.thaliana.
Abstract: An Arabidopsis thaliana line that is mutant for the R2R3 MYB gene, AtMYB4, shows enhanced levels of sinapate esters in its leaves. The mutant line is more tolerant of UV-B irradiation than wild type. The increase in sinapate ester accumulation in the mutant is associated with an enhanced expression of the gene encoding cinnamate 4-hydroxylase, which appears to be the principal target of AtMYB4 and an effective rate limiting step in the synthesis of sinapate ester sunscreens. AtMYB4 expression is downregulated by exposure to UV-B light, indicating that derepression is an important mechanism for acclimation to UV-B in A.thaliana. The response of target genes to AtMYB4 repression is dose dependent, a feature that operates under physiological conditions to reinforce the silencing effect of AtMYB4 at high activity. AtMYB4 works as a repressor of target gene expression and includes a repression domain. It belongs to a novel group of plant R2R3 MYB proteins involved in transcriptional silencing. The balance between MYB activators and repressors on common target promoters may provide extra flexibility in transcriptional control.

794 citations


"A Molecular Blueprint of Lignin Rep..." refers background in this paper

  • ...The knockout of AtMYB4, a thale cress ortholog of AmMYB308, displayed increased amounts of sinapate esters through increased expression of C4H [35]....

    [...]

  • ...The repression mechanism of AtMYB3 is completely different from that of AtMYB4, AtMYB7, and AtMYB32 because it is directly regulated by the corepressors NIGHT LIGHT-INDUCIBLE AND CLOCK-REGULATED 1 (LNK1) and LNK2, which could facilitate binding of AtMYB3 to the C4H promoter [37]....

    [...]

  • ...By screening TFs binding to the poplar 4CL promoter, Gui and colleagues identified a lignin biosynthesis-associated factor, LTF1, that represses several genes from this pathway (PAL2, C4H1, C3H2, 4CL1, CAld5H, COMT2, and CCoAOMT1) and decreases lignin content in overexpressing lines [107]....

    [...]

  • ...Molecular Regulation of Lignin Repression in Dicots at the Chromatin, Transcriptional, Post-Transcriptional, and PostTranslational levels (green boxes) Chromatin–mediated repression EgMYB1 Transcriptional repression AtMED5 AtPAL1/2 AtC4H At4CL1 AtMYB4 AtKFB01/39/50 MYB WRKY NAC Subgroup 4 AtMYB3 AmMYB308 AmMYB330 AtMYB4/EgMYB1/PdMYB221 AtMYB7 AtMYB32 AtγMYB2 AtMYB52 AtMYB75 PttMYB21a PdMYB90, PbMYB167 PdMYB92, PdMYB125 BELL family AtBLH6 KNOX family AtBP PtaARK2 AtKNAT7 Interactions KNAT7 KNAT7–MYB75 KNAT7–DRIF1 KNAT7–OFP KNAT7–BLH6 KNAT7–BLH6–OFP AtWRKY12 / PtrWRKY19 AtNST2 Post–transcriptional repression miR397 Post–translational regulation PAL KFB01 KFB20 KFB39 KFB50 U U PAL 26S proteasome Reduced DNA accessibility through chromatin condensation HD–ZIP TALE AtHB15/PtrPCN/PtrHB11 miR857 PtrVND6–C1IR, PtrSND1–A2IR PtrVND6, PtrSND1 AP2 EjAP2-1–EjbHLH1–EjMYBsPsnSHINE2 PtrhAT PtrMYB021 Transcriptional complex LAC AtVNDs AtVND7 AtVNI2 AtXND1 Active PtrAldOMT2 P Ser 123 Ser125 Inactive PtrAldOMT2 LTF1 Phosphorylated LTF1 U EgH1....

    [...]

  • ...Members of subgroup 4 repress the phenylpropanoid pathway, the lignin pathway, and/or the biosynthesis of pigments (Figure 1) [35,37]....

    [...]

Journal ArticleDOI
TL;DR: In this paper, a review focuses on recent literature reporting on the main types of abiotic and biotic stresses that alter the biosynthesis of lignin in plants and how a stressor modulates expression of the genes related with ligninsynthesis.
Abstract: Lignin is a polymer of phenylpropanoid compounds formed through a complex biosynthesis route, represented by a metabolic grid for which most of the genes involved have been sequenced in several plants, mainly in the model-plants Arabidopsis thaliana and Populus. Plants are exposed to different stresses, which may change lignin content and composition. In many cases, particularly for plant-microbe interactions, this has been suggested as defence responses of plants to the stress. Thus, understanding how a stressor modulates expression of the genes related with lignin biosynthesis may allow us to develop study-models to increase our knowledge on the metabolic control of lignin deposition in the cell wall. This review focuses on recent literature reporting on the main types of abiotic and biotic stresses that alter the biosynthesis of lignin in plants.

761 citations

Journal ArticleDOI
TL;DR: It is proposed that KNOX proteins may act as general orchestrators of growth-regulator homeostasis at the shoot apex of Arabidopsis by simultaneously activating CK and repressing GA biosynthesis, thus promoting meristem activity.

631 citations


"A Molecular Blueprint of Lignin Rep..." refers background in this paper

  • ...with a lower bioactive pool of gibberellins [67]....

    [...]

Journal ArticleDOI
TL;DR: This review summarizes the current understanding of V-myb myeloblastosis viral oncogene homolog (MYB) proteins and their roles in the regulation of phenylpropanoid metabolism in plants.

569 citations


"A Molecular Blueprint of Lignin Rep..." refers background in this paper

  • ...AtMYB4 belongs to subgroup 4 and, as the other proteins from this subgroup (AtMYB3, AtMYB7, and AtMYB32), contains an EARlike repression motif in its C-terminus [36]....

    [...]

  • ...4 and, as the other proteins from this subgroup (AtMYB3, AtMYB7, and AtMYB32), contains an EARlike repression motif in its C-terminus [36]....

    [...]

Journal ArticleDOI
TL;DR: It is demonstrated that overexpression of two MYB genes from Antirrhinum represses phenolic acid metabolism and lignin biosynthesis in transgenic tobacco plants.
Abstract: MYB-related transcription factors are known to regulate different branches of flavonoid metabolism in plants and are believed to play wider roles in the regulation of phenylpropanoid metabolism in general. Here, we demonstrate that overexpression of two MYB genes from Antirrhinum represses phenolic acid metabolism and lignin biosynthesis in transgenic tobacco plants. The inhibition of this branch of phenylpropanoid metabolism appears to be specific to AmMYB308 and AmMYB330, suggesting that they recognize their normal target genes in these transgenic plants. Experiments with yeast indicate that AmMYB308 can act as a very weak transcriptional activator so that overexpression may competitively inhibit the activity of stronger activators recognizing the same target motifs. The effects of the transcription factors on inhibition of phenolic acid metabolism resulted in complex modifications of the growth and development of the transgenic plants. The inhibition of monolignol production resulted in plants with at least 17% less lignin in their vascular tissue. This reduction is of importance when designing strategies for the genetic modification of woody crops.

502 citations


"A Molecular Blueprint of Lignin Rep..." refers background in this paper

  • ...The first MYB factors shown to repress lignin biosynthesis were AmMYB308 and AmMYB330 from Antirrhinum majus [34]....

    [...]