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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: Findings implicate important roles for MYB transcription factors in coordinated regulation of grass lignin biosynthesis including γ-acylated and tricin-incorporated lign in biosynthesis.

19 citations

Journal ArticleDOI
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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Journal ArticleDOI
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: It is shown that miR857 was involved in the regulation of lignin content and consequently morphogenesis of the secondary xylem and was activated by SQUAMOSA PROMOTER BINDING PROTEIN-LIKE7 in response to low copper conditions.
Abstract: MicroRNAs (miRNAs) are endogenous small RNAs that repress target gene expression posttranscriptionally, and are critically involved in various developmental processes and responses to environmental stresses in eukaryotes. MiRNA857 is not widely distributed in plants and is encoded by a single gene, AtMIR857, in Arabidopsis (Arabidopsis thaliana). The functions of miR857 and its mechanisms in regulating plant growth and development are still unclear. Here, by means of genetic analysis coupled with cytological studies, we investigated the expression pattern and regulation mechanism of miR857 and its biological functions in Arabidopsis development. We found that miR857 regulates its target gene, Arabidopsis LACCASE7, at the transcriptional level, thereby reducing laccase activity. Using stimulated Raman scattering and x-ray microtomography three-dimensional analyses, we showed that miR857 was involved in the regulation of lignin content and consequently morphogenesis of the secondary xylem. In addition, miR857 was activated by SQUAMOSA PROMOTER BINDING PROTEIN-LIKE7 in response to low copper conditions. Collectively, these findings demonstrate the role of miR857 in the regulation of secondary growth of vascular tissues in Arabidopsis and reveal a unique control mechanism for secondary growth based on the miR857 expression in response to copper deficiency.

64 citations


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

  • ...of the SPL7 (SQUAMOSA promoter-binding protein like 7) TF to the GTAC motifs contained in the miRNA857 promoter [94]....

    [...]

  • ...been described in thale cress, wheremiRNA857 andmiRNA397bmodulate the abundance ofAtLAC7 and AtLAC4 transcripts, respectively [94,99]....

    [...]

  • ...and SCW thickness in response to decreasedAtLAC7 transcript quantity, resulting in lower lignin content, and potentially reducing plant yield [94]....

    [...]

  • ...Their expression is developmentally regulated and/or under the control of external stimuli such as abiotic stress or nutrient availability [93,94]....

    [...]

Journal ArticleDOI
20 Oct 2015-PLOS ONE
TL;DR: A comprehensive in vivo analysis of R2R3-MYB binding activities is provided that should help in predicting new DNA motifs and identifying new putative target genes for each member of this very large family of TFs.
Abstract: The control of growth and development of all living organisms is a complex and dynamic process that requires the harmonious expression of numerous genes. Gene expression is mainly controlled by the activity of sequence-specific DNA binding proteins called transcription factors (TFs). Amongst the various classes of eukaryotic TFs, the MYB superfamily is one of the largest and most diverse, and it has considerably expanded in the plant kingdom. R2R3-MYBs have been extensively studied over the last 15 years. However, DNA-binding specificity has been characterized for only a small subset of these proteins. Therefore, one of the remaining challenges is the exhaustive characterization of the DNA-binding specificity of all R2R3-MYB proteins. In this study, we have developed a library of Arabidopsis thaliana R2R3-MYB open reading frames, whose DNA-binding activities were assayed in vivo (yeast one-hybrid experiments) with a pool of selected cis-regulatory elements. Altogether 1904 interactions were assayed leading to the discovery of specific patterns of interactions between the various R2R3-MYB subgroups and their DNA target sequences and to the identification of key features that govern these interactions. The present work provides a comprehensive in vivo analysis of R2R3-MYB binding activities that should help in predicting new DNA motifs and identifying new putative target genes for each member of this very large family of TFs. In a broader perspective, the generated data will help to better understand how TF interact with their target DNA sequences.

59 citations

Journal ArticleDOI
TL;DR: Jasmonate-responsive repressors of FtMYBs can be degraded by the 26S proteasome in a COI1-dependent manner in Fagopyrum tataricum and act together with FtSAD2 or FtJAZ1 in the phenylpropanoid pathway.
Abstract: Jasmonates are plant hormones that induce the accumulation of many secondary metabolites, such as rutin in buckwheat, via regulation of jasmonate-responsive transcription factors. Here, we report on the identification of a clade of jasmonate-responsive subgroup 4 MYB transcription factors, FtMYB13, FtMYB14, FtMYB15, and FtMYB16, which directly repress rutin biosynthesis in Fagopyrum tataricum. Immunoblot analysis showed that FtMYB13, FtMYB14, and FtMYB15 could be degraded via the 26S proteasome in the COI1-dependent jasmonate signaling pathway, and that this degradation is due to the SID motif in their C-terminus. Yeast two-hybrid and bimolecular fluorescence complementation assays revealed that FtMYB13, FtMYB14, and FtMYB15 interact with the importin protein Sensitive to ABA and Drought 2 (FtSAD2) in stem and inflorescence. Furthermore, the key repressor of jasmonate signaling FtJAZ1 specifically interacts with FtMYB13. Point mutation analysis showed that the conserved Asp residue of the SID domain contributes to mediating protein-protein interaction. Protoplast transient activation assays demonstrated that FtMYB13, FtMYB14, and FtMYB15 directly repress phenylalanine ammonia lyase (FtPAL) gene expression, and FtSAD2 and FtJAZ1 significantly promote the repressing activity of FtMYBs. These findings may ultimately be promising for further engineering of plant secondary metabolism.

58 citations


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

  • ...through the 26S proteasome pathway [23,43]....

    [...]

  • ...The interaction between SAD2 and members of subgroup 4 occurs through their SID domain GXXDFxxxG/DL, which is also a signature for protein degradation through the 26S proteasome pathway [43]....

    [...]

Journal ArticleDOI
TL;DR: A lignin biosynthesis associated transcription factor from Populus, LTF1, is identified, which binds to the promoter of 4-coumarate-CoA ligase (4CL), a key lign in biosynthetic gene.

57 citations

Journal ArticleDOI
TL;DR: A transcriptomic close-up of the key events accompanying bast fibre development in textile hemp, a fibre crop of great importance, shows that the fibres sampled at each stem region are characterized by a specific transcriptomic signature and that the major changes in cell wall-related processes take place at the internode containing the snap point.
Abstract: Bast fibres are long extraxylary cells which mechanically support the phloem and they are divided into xylan- and gelatinous-type, depending on the composition of their secondary cell walls. The former, typical of jute/kenaf bast fibres, are characterized by the presence of xylan and a high degree of lignification, while the latter, found in tension wood, as well as flax, ramie and hemp bast fibres, have a high abundance of crystalline cellulose. During their differentiation, bast fibres undergo specific developmental stages: the cells initially elongate rapidly by intrusive growth, subsequently they cease elongation and start to thicken. The goal of the present study is to provide a transcriptomic close-up of the key events accompanying bast fibre development in textile hemp (Cannabis sativa L.), a fibre crop of great importance. Bast fibres have been sampled from different stem regions. The developmental stages corresponding to active elongation and cell wall thickening have been studied using RNA-Seq. The results show that the fibres sampled at each stem region are characterized by a specific transcriptomic signature and that the major changes in cell wall-related processes take place at the internode containing the snap point. The data generated also identify several interesting candidates for future functional analysis.

55 citations


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

  • ...The hemp ortholog of KFB39 is upregulated in mature bast fibers, suggesting a role for KFBs in the hypolignification of this cell type [83]....

    [...]