Ancient origin of the biosynthesis of lignin precursors

Abstract

BackgroundLignin plays an important role in plant structural support and water transport, and is considered one of the hallmarks of land plants. The recent discovery of lignin or its precursors in various algae has raised questions on the evolution of its biosynthetic pathway, which could be much more ancient than previously thought. To determine the taxonomic distribution of the lignin biosynthesis genes, we screened all publicly available genomes of algae and their closest non-photosynthetic relatives, as well as representative land plants. We also performed phylogenetic analysis of these genes to decipher the evolution and origin(s) of lignin biosynthesis.ResultsEnzymes involved in making p-coumaryl alcohol, the simplest lignin monomer, are found in a variety of photosynthetic eukaryotes, including diatoms, dinoflagellates, haptophytes, cryptophytes as well as green and red algae. Phylogenetic analysis of these enzymes suggests that they are ancient and spread to some secondarily photosynthetic lineages when they acquired red and/or green algal endosymbionts. In some cases, one or more of these enzymes was likely acquired through lateral gene transfer (LGT) from bacteria.ConclusionsGenes associated with p-coumaryl alcohol biosynthesis are likely to have evolved long before the transition of photosynthetic eukaryotes to land. The original function of this lignin precursor is therefore unlikely to have been related to water transport. We suggest that it participates in the biological defense of some unicellular and multicellular algae.ReviewersThis article was reviewed by Mark Ragan, Uri Gophna, Philippe Deschamps.

The Evolution of Flavonoid Biosynthesis: A Bryophyte Perspective

“…The core steps of the phenylpropanoid pathway through to the first flavonoids (the chalcones) are conserved across land plants (Tohge et al, 2013), including the presence of PAL, C4H, 4CL, CHS, and CHIL gene sequences in hornworts. Sequences relating to some of these genes are present in the genome sequences of charophyte and chlorophyte algae (Labeeuw et al, 2015;de Vries et al, 2017), but without functional assays the conclusions that can be drawn are limited. Most phenylpropanoid pathway enzymes are thought to have evolved from primary metabolism enzymes (Tohge et al, 2013;Yonekura-Sakakibara et al, 2019), and so related sequences might be expected to be present.…”

“…C4H, which belongs to the CYP73A sub-family of cytochrome P450 monooxygenases (Cyp450s), shows strong sequence conservation across land plants, including characteristic motifs and residues, but no authentic gene sequences are apparent in chlorophyte genomes (Tohge et al, 2013;Davies et al, 2020). In contrast, sequences with similarity to 4CL do occur in rhodophyte and chlorophyte genomes (Labeeuw et al, 2015;de Vries et al, 2017), suggesting the existence of this enzyme in a shared ancestor of land plants and algae before the ancestral divergence of the red algae (Labeeuw et al, 2015). A further aspect yet to be addressed is the presence in fungi of genes with significant sequence similarity to those of the phenylpropanoid pathway (Bilska et al, 2018;Lu et al, 2019).…”

“…However, while MAA production is frequently reported for red algae (Rhodophyta) and other marine organisms, there are few reports for the Chlorophyta (a green algal clade that with Streptophyta form the Viridiplantae) and none for the charophyte algae that is thought to be most closely related to the land plant ancestor. Although genes for the initial steps of the phenylpropanoid pathway may be present in the genomes of extant Rhodophyta, Glaucophyta, Chlorophyta, and charophytes (Labeeuw et al, 2015;de Vries et al, 2017;Davies et al, 2020), there are no substantiated examples of flavonoid-specific genes being identified. Indeed, many metabolite studies on algae report only amounts of "total flavonoids" measured using general assays.…”

Assessing the Viability of Recovery of Hydroxycinnamic Acids from Lignocellulosic Biorefinery Alkaline Pretreatment Waste Streams

“…Hydroxycinnamic acids p-coumaric acid (pCA) and ferulic acid (FA) are high-value chemicals that could be sold as coproducts from the conversion of lignocellulosic biomass into materials, commodity chemicals,a nd liquid fuels. These phenolic acids are presenti na ll plants, [1,2] albeit rarely in the free acid form; usually they are ester-or ether-linked to mono-and disaccharides, [3] betacyanins, [4] glycoproteins, [5] long chain fatty acids (waxes), [6,7] sterols, [8] plant cell wall lignin and/orp olysaccharides, [9][10][11] and many other soluble and insoluble components. Hydroxycinnamic acids have antioxidant, antimicrobial, anti-inflammatory,a ntithrombosis, and anticancer activities;t hey protect against coronary disease and can reduce obesity.…”

Earliest land plants created modern levels of atmospheric oxygen

“…The Carboniferous-Permian peak in coal production has often been attributed to the evolution of lignin synthesis and a lag before the evolution of fungal degradation of lignin (23), but recent work has questioned this (24). Earlier plants possessed lignified "woody" tissue (25), with precursor structures existing in marine algae before the transition to land (26), and lignin-degrading fungi potentially present before the Carboniferous (24). Carboniferous coals are not dominated by lignin; instead, their accumulation was controlled by a combination of climate and tectonics supporting the creation and sedimentary preservation of peat bogs (24,27).…”