<i>p</i>HBMT1, a BAHD-family monolignol acyltransferase, mediates lignin acylation in poplar

Vries, Lisanne de; MacKay, Heather A.; Smith, Rebecca A.; Mottiar, Yaseen; Karlen, Steven D.; Unda, Faride; Muirragui, Emilia; Bingman, C.A.; Meulen, Kirk Vander; Beebe, Emily T.; Fox, Brian G.; Ralph, John; Mansfield, Shawn D.

doi:10.1093/plphys/kiab546

Cited by 28 publications

(39 citation statements)

References 76 publications

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“…p ‐Hydroxybenzoylation of lignin occurs via the incorporation of acylated monolignols rather than by post‐polymerization acylation (Lu et al ., 2015). And, the gene encoding this specific p ‐hydroxybenzoyl‐coenzyme A (CoA) monolignol transferase has recently been identified and functionally tested in poplar in two independent studies (Zhao et al ., 2021; de Vries et al ., 2022). In QsuB ‐poplar, we observed significant reductions in p HBA released from the cell wall following alkaline hydrolysis.…”

Section: Discussionmentioning

confidence: 99%

A new approach to zip‐lignin: 3,4‐dihydroxybenzoate is compatible with lignification

et al. 2022

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Renewed interests in the development of bioenergy, biochemicals, and biomaterials have elicited new strategies for engineering the lignin of biomass feedstock plants. This study shows, for the first time, that 3,4-dihydroxybenzoate (DHB) is compatible with the radical coupling reactions that assemble polymeric lignin in plants.We introduced a bacterial 3-dehydroshikimate dehydratase into hybrid poplar (Populus alba 9 grandidentata) to divert carbon flux away from the shikimate pathway, which lies upstream of lignin biosynthesis.Transgenic poplar wood had up to 33% less lignin with p-hydroxyphenyl units comprising as much as 10% of the lignin. Mild alkaline hydrolysis of transgenic wood released fewer ester-linked p-hydroxybenzoate groups than control trees, and revealed the novel incorporation of cell-wall-bound DHB, as well as glycosides of 3,4-dihydroxybenzoic acid (DHBA). Two-dimensional nuclear magnetic resonance (2D-NMR) analysis uncovered DHBA-derived benzodioxane structures suggesting that DHB moieties were integrated into the lignin polymer backbone. In addition, up to 40% more glucose was released from transgenic wood following ionic liquid pretreatment and enzymatic hydrolysis.This work highlights the potential of diverting carbon flux from the shikimate pathway for lignin engineering and describes a new type of 'zip-lignin' derived from the incorporation of DHB into poplar lignin.

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Section: Discussionmentioning

confidence: 99%

A new approach to zip‐lignin: 3,4‐dihydroxybenzoate is compatible with lignification

et al. 2022

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“…These results are in line with those of previous reports suggesting that the level of p ‐hydroxybenzoate was negatively correlated with the amount of S units in lignin of natural poplar variants (Yoo et al ., 2018) and of a F5H ‐overexpressing transgenic poplar (Stewart et al ., 2009); however, the p ‐hydroxybenzoate ester occurs almost exclusively on S‐lignin units in poplar (Regner et al ., 2018). Recently, an acyltransferase gene ( PHBMT1 , Potri.001G448000) responsible for biosynthesis of γ‐ p ‐hydroxybenzoylated monolignols has been identified in poplar (de Vries et al ., 2021b; Zhao et al ., 2021). Overexpression of PHBMT1 in the transgenic poplar led to an increase in p ‐hydroxybenzoylated lignin units and changes in solvent dissolution rate of the lignin in cell walls.…”

Section: Discussionmentioning

confidence: 99%

Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen

et al. 2022

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Lignin is a phenolic polymer deposited in the plant cell wall, and is mainly polymerized from three canonical monomers (monolignols), i.e. p-coumaryl, coniferyl and sinapyl alcohols. After polymerization, these alcohols form different lignin substructures. In dicotyledons, monolignols are biosynthesized from phenylalanine, an aromatic amino acid. Shikimate acts at two positions in the route to the lignin building blocks. It is part of the shikimate pathway that provides the precursor for the biosynthesis of phenylalanine, and is involved in the transesterification of p-coumaroyl-CoA to p-coumaroyl shikimate, one of the key steps in the biosynthesis of coniferyl and sinapyl alcohols. The shikimate residue in p-coumaroyl shikimate is released in later steps, and the resulting shikimate becomes available again for the biosynthesis of new p-coumaroyl shikimate molecules. In this study, we inhibited cytosolic shikimate recycling in transgenic hybrid aspen by accelerated phosphorylation of shikimate in the cytosol through expression of a bacterial shikimate kinase (SK). This expression elicited an increase in p-hydroxyphenyl units of lignin and, by contrast, a decrease in guaiacyl and syringyl units. Transgenic plants with high SK activity produced a lignin content comparable to that in wild-type plants, and had an increased processability via enzymatic saccharification. Although expression of many genes was altered in the transgenic plants, elevated SK activity did not exert a significant effect on the expression of the majority of genes responsible for lignin biosynthesis. The present results indicate that cytosolic shikimate recycling is crucial to the monomeric composition of lignin rather than for lignin content.

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“…Arabidopsis has been widely used as a model system for basic plant research and is a valuable model to study lignification ( Meinke et al, 1998 ; Humphreys and Chapple, 2002 ; Koornneef and Meinke, 2010 ). The lignin biosynthetic pathways in Arabidopsis and the bioenergy crop poplar are similar, although poplar also incorporates additional units, like coniferyl and sinapyl p -hydroxybenzoates, into its lignin polymer ( Lu et al, 2004 , 2015 ; Morreel et al, 2004 ; Vanholme et al, 2019 ; Zhao et al, 2021 ; de Vries et al, 2022 ). Several lignin engineering strategies gave similar results in Arabidopsis and poplar.…”

Section: Discussionmentioning

confidence: 99%

“…The severe reduction in the amount of p -hydroxybenzoates in ProCesA8-B:DCS_CURS2 lignin (see also below) might also lead/contribute to the decreased health of the transgenic trees. To date, the biological function of lignin acylation remains unknown ( de Vries et al, 2022 ). However, phbmt1 poplars with nearly depleted p -hydroxybenzoates in stem lignin also display compromised early-stage growth in soil, although no shoot tip necrosis was observed ( Zhao et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…The polysaccharides present in the plant cell wall, cellulose and hemicelluloses, can be hydrolyzed into fermentable primary sugars by a process called saccharification. These monomers can be further processed into bulk chemicals, such as bioethanol, levulinic acid, and 2,5-furandicarboxylic acid (Bozell et al, 2007;Corma et al, 2007;Vanholme et al, 2013a;Isikgor and Becer, 2015;de Vries et al, 2021b). However, the saccharification process is hindered by the presence of lignin.…”

Section: Introductionmentioning

confidence: 99%

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Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass Yield

et al. 2022

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Lignocellulosic biomass is recalcitrant toward deconstruction into simple sugars mainly due to the presence of lignin. By engineering plants to partially replace traditional lignin monomers with alternative ones, lignin degradability and extractability can be enhanced. Previously, the alternative monomer curcumin has been successfully produced and incorporated into lignified cell walls of Arabidopsis by the heterologous expression of DIKETIDE-CoA SYNTHASE (DCS) and CURCUMIN SYNTHASE2 (CURS2). The resulting transgenic plants did not suffer from yield penalties and had an increased saccharification yield after alkaline pretreatment. Here, we translated this strategy into the bio-energy crop poplar. Via the heterologous expression of DCS and CURS2 under the control of the secondary cell wall CELLULOSE SYNTHASE A8-B promoter (ProCesA8-B), curcumin was also produced and incorporated into the lignified cell walls of poplar. ProCesA8-B:DCS_CURS2 transgenic poplars, however, suffered from shoot-tip necrosis and yield penalties. Compared to that of the wild-type (WT), the wood of transgenic poplars had 21% less cellulose, 28% more matrix polysaccharides, 23% more lignin and a significantly altered lignin composition. More specifically, ProCesA8-B:DCS_CURS2 lignin had a reduced syringyl/guaiacyl unit (S/G) ratio, an increased frequency of p-hydroxyphenyl (H) units, a decreased frequency of p-hydroxybenzoates and a higher fraction of phenylcoumaran units. Without, or with alkaline or hot water pretreatment, the saccharification efficiency of the transgenic lines was equal to that of the WT. These differences in (growth) phenotype illustrate that translational research in crops is essential to assess the value of an engineering strategy for applications. Further fine-tuning of this research strategy (e.g., by using more specific promoters or by translating this strategy to other crops such as maize) might lead to transgenic bio-energy crops with cell walls more amenable to deconstruction without settling in yield.

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pHBMT1, a BAHD-family monolignol acyltransferase, mediates lignin acylation in poplar

Cited by 28 publications

References 76 publications

A new approach to zip‐lignin: 3,4‐dihydroxybenzoate is compatible with lignification

A new approach to zip‐lignin: 3,4‐dihydroxybenzoate is compatible with lignification

Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen

Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass Yield

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