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Woody Formation and Lignin Biosynthesis in Plants

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (30 September 2019) | Viewed by 24148

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Special Issue Editor

Dr. Jacqueline Grima-Pettenati

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Guest Editor

Universite de Toulouse III, CNRS Toulouse, France
Interests: wood formation; lignin biosynthesis; trees genomics; bioenergy; transcriptional regulation; post-transcriptional regulation; chromatin remodeling; auxin; abiotic stresses

Special Issue Information

Dear Colleagues,

Wood, also called secondary xylem, is a highly specialized vascular tissue characterized by the presence of thick, heavily lignified secondary cell walls. While fulfilling crucial roles in trees, wood also has a tremendous importance at both the ecological and economical levels. It is the most abundant plant biomass on earth, an immense reservoir of fixed carbon and humankind's oldest renewable resource for a myriad of end-uses. Wood formation, initiated by the division of cambial initials, is a remarkable example of differentiation in vascular plants, controlled by both internal and external signals. Although massive efforts were devoted to unveiling the transcriptional network regulating the biosynthetic pathways, leading to the three main secondary cell wall polymers, many questions still remain unanswered.

We welcome research and review articles that will increase our understanding of wood formation during development and in response to environmental changes. The topics of this Special Issue will focus but are not limited to new findings on the regulation of wood formation at the transcriptional, posttranscriptional, and posttranslational levels, including chromatin remodeling and epigenetic regulation. The molecular mechanisms underlying the hormonal control of wood formation, as well as those conferring wood plasticity and their role in adaptation to biotic or abiotic stresses, are welcome. Significant results on lignin biosynthesis, monolignol transport, and polymerization as well as on the crosstalk with other branches of the phenylpropanoid pathway are also of interest. System biology approaches integrating different layers of information will be considered as priorities and significant technological advances to study wood formation will also be included.

Dr. Jacqueline Grima-Pettenati
Guest Editor

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Keywords

Wood
Secondary cell wall
Lignin
Transcriptional regulation
Environmental stresses
Omics
Trees
Posttranscriptional regulation
Hormonal regulation
Integrative studies

Published Papers (7 papers)

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Research

22 pages, 2436 KiB

Open AccessArticle

Implementing the CRISPR/Cas9 Technology in Eucalyptus Hairy Roots Using Wood-Related Genes

by Ying Dai, Guojian Hu, Annabelle Dupas, Luciano Medina, Nils Blandels, Hélène San Clemente, Nathalie Ladouce, Myriam Badawi, Guillermina Hernandez-Raquet, Fabien Mounet, Jacqueline Grima-Pettenati and Hua Cassan-Wang

Int. J. Mol. Sci. 2020, 21(10), 3408; https://doi.org/10.3390/ijms21103408 - 12 May 2020

Cited by 25 | Viewed by 4297

Abstract

Eucalypts are the most planted hardwoods worldwide. The availability of the Eucalyptus grandis genome highlighted many genes awaiting functional characterization, lagging behind because of the lack of efficient genetic transformation protocols. In order to efficiently generate knock-out mutants to study the function of eucalypts genes, we implemented the powerful CRISPR/Cas9 gene editing technology with the hairy roots transformation system. As proofs-of-concept, we targeted two wood-related genes: Cinnamoyl-CoA Reductase1 (CCR1), a key lignin biosynthetic gene and IAA9A an auxin dependent transcription factor of Aux/IAA family. Almost all transgenic hairy roots were edited but the allele-editing rates and spectra varied greatly depending on the gene targeted. Most edition events generated truncated proteins, the prevalent edition types were small deletions but large deletions were also quite frequent. By using a combination of FT-IR spectroscopy and multivariate analysis (partial least square analysis (PLS-DA)), we showed that the CCR1-edited lines, which were clearly separated from the controls. The most discriminant wave-numbers were attributed to lignin. Histochemical analyses further confirmed the decreased lignification and the presence of collapsed vessels in CCR1-edited lines, which are characteristics of CCR1 deficiency. Although the efficiency of editing could be improved, the method described here is already a powerful tool to functionally characterize eucalypts genes for both basic research and industry purposes. Full article

(This article belongs to the Special Issue Woody Formation and Lignin Biosynthesis in Plants)

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17 pages, 3903 KiB

Open AccessArticle

Wood Architecture and Composition Are Deeply Remodeled in Frost Sensitive Eucalyptus Overexpressing CBF/DREB1 Transcription Factors

by Phi Bang Cao, Raphaël Ployet, Chien Nguyen, Annabelle Dupas, Nathalie Ladouce, Yves Martinez, Jacqueline Grima-Pettenati, Christiane Marque, Fabien Mounet and Chantal Teulières

Int. J. Mol. Sci. 2020, 21(8), 3019; https://doi.org/10.3390/ijms21083019 - 24 Apr 2020

Cited by 9 | Viewed by 3189

Abstract

Eucalypts are the most planted trees worldwide, but most of them are frost sensitive. Overexpressing transcription factors for CRT-repeat binding factors (CBFs) in transgenic Eucalyptus confer cold resistance both in leaves and stems. While wood plays crucial roles in trees and is affected by environmental cues, its potential role in adaptation to cold stress has been neglected. Here, we addressed this question by investigating the changes occurring in wood in response to the overexpression of two CBFs, taking advantage of available transgenic Eucalyptus lines. We performed histological, biochemical, and transcriptomic analyses on xylem samples. CBF ectopic expression led to a reduction of both primary and secondary growth, and triggered changes in xylem architecture with smaller and more frequent vessels and fibers exhibiting reduced lumens. In addition, lignin content and syringyl/guaiacyl (S/G) ratio increased. Consistently, many genes of the phenylpropanoid and lignin branch pathway were upregulated. Most of the features of xylem remodeling induced by CBF overexpression are reminiscent of those observed after long exposure of Eucalyptus trees to chilling temperatures. Altogether, these results suggest that CBF plays a central role in the cross-talk between response to cold and wood formation and that the remodeling of wood is part of the adaptive strategies to face cold stress. Full article

(This article belongs to the Special Issue Woody Formation and Lignin Biosynthesis in Plants)

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18 pages, 3145 KiB

Open AccessArticle

Differential Gene Profiling of the Heartwood Formation Process in Taiwania cryptomerioides Hayata Xylem Tissues

by Ting-Feng Yeh, Jui-Hua Chu, Li-Yuan Liu and Shih-Yin Chen

Int. J. Mol. Sci. 2020, 21(3), 960; https://doi.org/10.3390/ijms21030960 - 31 Jan 2020

Cited by 12 | Viewed by 2476

Abstract

Taiwania (Taiwania cryptomerioides) is an important tree species in Taiwan because of the excellent properties of its wood and fascinating color qualities of its heartwood (HW), as well as the bioactive compounds therein. However, limited information is available as to the HW formation of this species. The objective of this research is to analyze the differentially expressed genes (DEGs) during the HW formation process from specific Taiwania xylem tissues, and to obtain genes that might be closely associated with this process. The results indicated that our analyses have captured DEGs representative to the HW formation process of Taiwania. DEGs related to the terpenoid biosynthesis pathway were all up-regulated in the transition zone (TZ) to support the biosynthesis and accumulation of terpenoids. Many DEGs related to lignin biosynthesis, and two DEGs related to pinoresinol reductase (PrR)/pinoresinol lariciresinol reductase (PLR), were up-regulated in TZ. These DEGs together are likely involved in providing the precursors for the subsequent lignan biosynthesis. Several transcription factor-, nuclease-, and protease-encoding DEGs were also highly expressed in TZ, and these DEGs might be involved in the regulation of secondary metabolite biosynthesis and the autolysis of the cellular components of ray parenchyma cells in TZ. These results provide further insights into the process of HW formation in Taiwania. Full article

(This article belongs to the Special Issue Woody Formation and Lignin Biosynthesis in Plants)

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19 pages, 662 KiB

Open AccessArticle

Molecular Changes Concomitant with Vascular System Development in Mature Galls Induced by Root-Knot Nematodes in the Model Tree Host Populus tremula × P. alba

by Fabien Baldacci-Cresp, Marc Behr, Annegret Kohler, Nelly Badalato, Kris Morreel, Geert Goeminne, Adeline Mol, Janice de Almeida Engler, Wout Boerjan, Mondher El Jaziri and Marie Baucher

Int. J. Mol. Sci. 2020, 21(2), 406; https://doi.org/10.3390/ijms21020406 - 09 Jan 2020

Cited by 9 | Viewed by 3651

Abstract

One of the most striking features occurring in the root-knot nematode Meloidogyne incognita induced galls is the reorganization of the vascular tissues. During the interaction of the model tree species Populus and M. incognita, a pronounced xylem proliferation was previously described in mature galls. To better characterise changes in expression of genes possibly involved in the induction and the formation of the de novo developed vascular tissues occurring in poplar galls, a comparative transcript profiling of 21-day-old galls versus uninfected root of poplar was performed. Genes coding for transcription factors associated with procambium maintenance and vascular differentiation were shown to be differentially regulated, together with genes partaking in phytohormones biosynthesis and signalling. Specific signatures of transcripts associated to primary cell wall biosynthesis and remodelling, as well as secondary cell wall formation (cellulose, xylan and lignin) were revealed in the galls. Ultimately, we show that molecules derived from the monolignol and salicylic acid pathways and related to secondary cell wall deposition accumulate in mature galls. Full article

(This article belongs to the Special Issue Woody Formation and Lignin Biosynthesis in Plants)

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10 pages, 2747 KiB

Open AccessArticle

Functional Characteristics of Caffeoyl Shikimate Esterase in Larix Kaempferi and Monolignol Biosynthesis in Gymnosperms

by Xuechun Wang, Nan Chao, Meng Zhang, Xiangning Jiang and Ying Gai

Int. J. Mol. Sci. 2019, 20(23), 6071; https://doi.org/10.3390/ijms20236071 - 02 Dec 2019

Cited by 14 | Viewed by 3063

Abstract

Caffeoyl shikimate esterase (CSE) has been reported to be involved in lignin biosynthesis; however, studies of CSE in gymnosperms are lacking. In this study, CSE was successfully cloned from Larix kaempferi (LkCSE) based on Larix laricina transcriptome screening. LkCSE was likely to have catalytic activity based on homologous sequence alignment and phylogenetic analyses of CSEs from different species. In vitro assays with the recombinant enzyme validated the catalytic activity of LkCSE, indicating its function in converting caffeoyl shikimate into caffeate and shikimate. Additionally, the optimum reaction pH and temperature of LkCSE were determined to be 6.0 and 30 °C, respectively. The values of K_m and V_max of CSE for caffeoyl shikimate were 98.11 μM and 14.44 nM min⁻¹, respectively. Moreover, LkCSE was observed to have tissue expression specificity and was abundantly expressed in stems and leaves, especially stems, which was 50 times higher than the expression levels of roots. Lastly, translational fusion assays using LkCSE fused with green fluorescent proteins (GFP) in tobacco leaves indicated that LkCSE was localized in the plasma membrane and endoplasmic reticulum (ER). These results revealed that CSE clearly functions in gymnosperms and it is possible for LkCSE to interact with other ER-resident proteins and regulate mass flux in the monolignol biosynthesis pathway. Full article

(This article belongs to the Special Issue Woody Formation and Lignin Biosynthesis in Plants)

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16 pages, 2415 KiB

Open AccessArticle

Analysis of Orthologous SECONDARY WALL-ASSOCIATED NAC DOMAIN1 (SND1) Promotor Activity in Herbaceous and Woody Angiosperms

by Libert B. Tonfack, Steven G. Hussey, Adri Veale, Alexander A. Myburg and Eshchar Mizrachi

Int. J. Mol. Sci. 2019, 20(18), 4623; https://doi.org/10.3390/ijms20184623 - 18 Sep 2019

Cited by 2 | Viewed by 3038

Abstract

SECONDARY WALL-ASSOCIATED NAC DOMAIN1 (SND1) is a master regulator of fibre secondary wall deposition in Arabidopsis thaliana (Arabidopsis), with homologs in other angiosperms and gymnosperms. However, it is poorly understood to what extent the fibre-specific regulation of the SND1 promoter, and that of its orthologs, is conserved between diverged herbaceous and woody lineages. We performed a reciprocal reporter gene analysis of orthologous SND1 promoters from Arabidopsis (AthSND1), Eucalyptus grandis (EgrNAC61) and Populus alba × P. grandidentata (PagWND1A) relative to secondary cell wall-specific Cellulose Synthase4 (CesA4) and CesA7 promoters, in both a non-woody (Arabidopsis) and a woody (poplar) system. β-glucuronidase (GUS) reporter analysis in Arabidopsis showed that the SND1 promoter was active in vascular tissues as previously reported and showed interfascicular and xylary fibre-specific expression in inflorescence stems, while reporter constructs of the woody plant-derived promoters were partial to the (pro)cambium-phloem and protoxylem. In transgenic P. tremula × P. alba plants, all three orthologous SND1 promoters expressed the GUS reporter similarly and preferentially in developing secondary xylem, ray parenchyma and cork cambium. Ours is the first study to reciprocally test orthologous SND1 promoter specificity in herbaceous and woody species, revealing diverged regulatory functions in the herbaceous system. Full article

(This article belongs to the Special Issue Woody Formation and Lignin Biosynthesis in Plants)

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18 pages, 2841 KiB

Open AccessArticle

Histone Deacetylase HDT1 is Involved in Stem Vascular Development in Arabidopsis

by Yongzhuo Zhang, Bin Yin, Jiaxue Zhang, Ziyi Cheng, Yadi Liu, Bing Wang, Xiaorui Guo, Xiatong Liu, Di Liu, Hui Li and Hai Lu

Int. J. Mol. Sci. 2019, 20(14), 3452; https://doi.org/10.3390/ijms20143452 - 13 Jul 2019

Cited by 8 | Viewed by 4021

Abstract

Histone acetylation and deacetylation play essential roles in eukaryotic gene regulation. HD2 (HD-tuins) proteins were previously identified as plant-specific histone deacetylases. In this study, we investigated the function of the HDT1 gene in the formation of stem vascular tissue in Arabidopsis thaliana. The height and thickness of the inflorescence stems in the hdt1 mutant was lower than that of wild-type plants. Paraffin sections showed that the cell number increased compared to the wild type, while transmission electron microscopy showed that the size of individual tracheary elements and fiber cells significantly decreased in the hdt1 mutant. In addition, the cell wall thickness of tracheary elements and fiber cells increased. We also found that the lignin content in the stem of the hdt1 mutants increased compared to that of the wild type. Transcriptomic data revealed that the expression levels of many biosynthetic genes related to secondary wall components, including cellulose, lignin biosynthesis, and hormone-related genes, were altered, which may lead to the altered phenotype in vascular tissue of the hdt1 mutant. These results suggested that HDT1 is involved in development of the vascular tissue of the stem by affecting cell proliferation and differentiation. Full article

(This article belongs to the Special Issue Woody Formation and Lignin Biosynthesis in Plants)

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