Mutation in<i>Brachypodium</i>caffeic acid<i>O</i>-methyltransferase 6 alters stem and grain lignins and improves straw saccharification without deteriorating grain quality

Ho-Yue-Kuang, Séverine; Alvarado, Camille; Antelme, Sébastien; Bouchet, Brigitte; Cézard, Laurent; Bris, Philippe Le; Legée, Frédéric; Maia‐Grondard, Alessandra; Yoshinaga, Arata; Saulnier, Luc; Guillon, Fabienne; Sibout, Richard; Lapierre, Catherine; Chateigner‐Boutin, Anne‐Laure

doi:10.1093/jxb/erv446

Cited by 45 publications

(34 citation statements)

References 69 publications

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“…This compares to reductions in Klason lignin content of 25% and 28% when COMT was suppressed in maize (Piquemal et al, 2002) and to reductions of up to 16% of acetyl bromide lignin when COMT was suppressed in perennial ryegrass . Comparisons are complicated, however, The level of incorporation of the 5-OH-G unit was similar to that measured in the maize bm3 mutant (Barri ere et al, 2004), maize antisense RNA transgenic lines (Piquemal et al, 2002) and brachypodium mutants (Dalmais et al, 2013;Ho-Yue-Kuang et al, 2016) and higher than that measured in the Arabidopsis mutant (Goujon et al, 2003). To our knowledge, this is the first reported quantification of the 5-OH-G unit in a temperate cereal.…”

Section: Discussionsupporting

confidence: 58%

“…Reductions in the S/G ratio of ~50% in the barley RNAi lines were less than that in knock‐out mutants in maize and Arabidopsis where S units were reduced by ~70% (Barrière et al ., ) or more (Goujon et al ., ), respectively. The level of incorporation of the 5‐OH‐G unit was similar to that measured in the maize bm3 mutant (Barrière et al ., ), maize antisense RNA transgenic lines (Piquemal et al ., ) and brachypodium mutants (Dalmais et al ., ; Ho‐Yue‐Kuang et al ., ) and higher than that measured in the Arabidopsis mutant (Goujon et al ., ). To our knowledge, this is the first reported quantification of the 5‐OH‐G unit in a temperate cereal.…”

Section: Discussionmentioning

confidence: 51%

“…The existence of brachypodium plants sufficiently deficient in COMT to be expected to develop brown-midrib phenotypes has not been definitively evidenced. A mutant in the brachypodium lignin COMT has been identified but displays only moderately altered lignification and the mutant enzyme is still functional (Ho-Yue-Kuang et al, 2016). Similarly, transgenic plants overexpressing artificial microRNA designed to silence brachypodium COMT did not have significant changes to S lignin (Trabucco et al, 2013) suggesting that they were not sufficiently COMT-suppressed.…”

Section: Discussionmentioning

confidence: 99%

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RNAi‐suppression of barley caffeic acidO‐methyltransferase modifies lignin despite redundancy in the gene family

Daly

McClellan

Maluk

et al. 2018

Plant Biotechnology Journal

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Caffeic acid O-methyltransferase (COMT), the lignin biosynthesis gene modified in many brown-midrib high-digestibility mutants of maize and sorghum, was targeted for downregulation in the small grain temperate cereal, barley (Hordeum vulgare), to improve straw properties. Phylogenetic and expression analyses identified the barley COMT orthologue(s) expressed in stems, defining a larger gene family than in brachypodium or rice with three COMT genes expressed in lignifying tissues. RNAi significantly reduced stem COMT protein and enzyme activity, and modestly reduced stem lignin content while dramatically changing lignin structure. Lignin syringyl-to-guaiacyl ratio was reduced by ~50%, the 5-hydroxyguaiacyl (5-OH-G) unit incorporated into lignin at 10--15-fold higher levels than normal, and the amount of p-coumaric acid ester-linked to cell walls was reduced by ~50%. No brown-midrib phenotype was observed in any RNAi line despite significant COMT suppression and altered lignin. The novel COMT gene family structure in barley highlights the dynamic nature of grass genomes. Redundancy in barley COMTs may explain the absence of brown-midrib mutants in barley and wheat. The barley COMT RNAi lines nevertheless have the potential to be exploited for bioenergy applications and as animal feed.

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Section: Discussionsupporting

confidence: 58%

Section: Discussionmentioning

confidence: 51%

Section: Discussionmentioning

confidence: 99%

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RNAi‐suppression of barley caffeic acidO‐methyltransferase modifies lignin despite redundancy in the gene family

Daly

McClellan

Maluk

et al. 2018

Plant Biotechnology Journal

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“…* BdCOMT6 (Bradi3g16530) was named BdCOMT4 in the paper [63]. However, based on the accession number and naming in other papers [75,76], BdCOMT6 was chosen. RNAi: RNA interference.…”

Section: Biotechnology and Bioengineering Of Monolignol Pathway In Grmentioning

confidence: 99%

Low Lignin Mutants and Reduction of Lignin Content in Grasses for Increased Utilisation of Lignocellulose

Christensen

Rasmussen

2019

Agronomy

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Biomass rich in lignocellulose from grasses is a major source for biofuel production and animal feed. However, the presence of lignin in cell walls limits its efficient utilisation such as in its bioconversion to biofuel. Reduction of the lignin content or alteration of its structure in crop plants have been pursued, either by regulating genes encoding enzymes in the lignin biosynthetic pathway using biotechnological techniques or by breeding naturally-occurring low lignin mutant lines. The aim of this review is to provide a summary of these studies, focusing on lignin (monolignol) biosynthesis and composition in grasses and, where possible, the impact on recalcitrance to bioconversion. An overview of transgenic crops of the grass family with regulated gene expression in lignin biosynthesis is presented, including the effect on lignin content and changes in the ratio of p-hydroxyphenyl (H), guaiacyl (G) and syringyl (S) units. Furthermore, a survey is provided of low-lignin mutants in grasses, including cereals in particular, summarising their origin and phenotypic traits together with genetics and the molecular function of the various genes identified.

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“…The mild alkaline hydrolysis was carried out overnight at room temperature on a carousel. After acidification with 0.2 mL of 6 M HCl, the tubes were centrifuged for 15 min at 2,000g and the supernatant was subjected to solid-phase extraction, then HPLC-diode-array detection analysis of the recovered methanolic extracts was performed as described previously (Ho-Yue-Kuang et al, 2016). To further confirm the occurrence of alkali-released CA or FA from control or transgenic samples, the methanolic extracts were diluted with water and the low-M r phenolics were reextracted with ethyl acetate before GC-MS analyses of their TMS derivatives.…”

Section: Analysis Of Ca and Fa Released By Mild Alkaline Hydrolysis Omentioning

confidence: 99%

Structural Redesigning Arabidopsis Lignins into Alkali-Soluble Lignins through the Expression of p-Coumaroyl-CoA:Monolignol Transferase PMT

et al. 2016

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Grass lignins can contain up to 10% to 15% by weight of p-coumaric esters. This acylation is performed on monolignols under the catalysis of p-coumaroyl-coenzyme A monolignol transferase (PMT). To study the impact of p-coumaroylation on lignification, we first introduced the Brachypodium distachyon Bradi2g36910 (BdPMT1) gene into Arabidopsis (Arabidopsis thaliana) under the control of the constitutive maize (Zea mays) ubiquitin promoter. The resulting p-coumaroylation was far lower than that of lignins from mature grass stems and had no impact on stem lignin content. By contrast, introducing either the BdPMT1 or the Bradi1g36980 (BdPMT2) gene into Arabidopsis under the control of the Arabidopsis cinnamate-4-hydroxylase promoter boosted the p-coumaroylation of mature stems up to the grass lignin level (8% to 9% by weight), without any impact on plant development. The analysis of purified lignin fractions and the identification of diagnostic products confirmed that p-coumaric acid was associated with lignins. BdPMT1-driven p-coumaroylation was also obtained in the fah1 (deficient for ferulate 5-hydroxylase) and ccr1g (deficient for cinnamoyl-coenzyme A reductase) lines, albeit to a lower extent. Lignins from BdPMT1-expressing ccr1g lines were also found to be feruloylated. In Arabidopsis mature stems, substantial p-coumaroylation of lignins was achieved at the expense of lignin content and induced lignin structural alterations, with an unexpected increase of lignin units with free phenolic groups. This higher frequency of free phenolic groups in Arabidopsis lignins doubled their solubility in alkali at room temperature. These findings suggest that the formation of alkali-leachable lignin domains rich in free phenolic groups is favored when p-coumaroylated monolignols participate in lignification in a grass in a similar manner.

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Mutation inBrachypodiumcaffeic acidO-methyltransferase 6 alters stem and grain lignins and improves straw saccharification without deteriorating grain quality

Abstract: HighlightThe first evaluation of lignification in Brachypodium distachyon grain is reported. Moderately down-regulated BdCOMT6 alters grain and stem lignification, which improves stem saccharification without major detrimental effects on grain development and composition.

Cited by 45 publications

References 69 publications

RNAi‐suppression of barley caffeic acidO‐methyltransferase modifies lignin despite redundancy in the gene family

RNAi‐suppression of barley caffeic acidO‐methyltransferase modifies lignin despite redundancy in the gene family

Low Lignin Mutants and Reduction of Lignin Content in Grasses for Increased Utilisation of Lignocellulose

Structural Redesigning Arabidopsis Lignins into Alkali-Soluble Lignins through the Expression of p-Coumaroyl-CoA:Monolignol Transferase PMT

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