Parallels in lignin biosynthesis: A study in Selaginella moellendorffii reveals convergence across 400 million years of evolution

Abstract

A hallmark of vascular plants is the development of a complex water-conducting system, which is physically reinforced by the heterogeneous aromatic polymer lignin. Syringyl lignin, a major building block of lignin, is often thought to be uniquely characteristic of angiosperms; however, it was demonstrated over fifty years ago that that syringyl lignin is found in another group of plants, known as the lycophytes, the ancestors of which diverged from all the other vascular plant lineages 400 million years ago.1 To determine the biochemical basis for this common biosynthetic ability, we isolated and characterized cytochrome P450-dependent monooxygenases (P450s) from the lycophyte Selaginella moellendorffii and compared them to the enzyme that is required for syringyl lignin synthesis in angiosperms. Our results showed that one of these P450s encodes an enzyme that is functionally analogous to but phylogenetically independent from its angiosperm counterpart. Here, we discuss the evolution of lignin biosynthesis in vascular plants and the role of Selaginella moellendorffii in plant comparative biology and genomics.

Keywords: F5H; Selaginella; biofuel; convergent evolution; cytochrome P450; lycophyte; syringyl lignin.

Figure 1

Selaginella moellendorffii represents an ancient land plant lineage. (A) A simplified cladogram illustrating the evolutionary position of Selaginella in the plant kingdom. Species with fully sequenced genomes are noted in brackets. (B) The aerial part of Selaginella moellendorffii showing dichotomous branching at the shoot. (C) Selaginella root with dichotomous branching pattern. (D) Selaginella microphylls with a single, unbranched vein emerged from the stele. (E) A cross-section of Selaginella stem showing protostelic vasculature.

Figure 2

DFRC GC analysis of lignin monomer diversity in vascular plants. Arabidopsis Columbia wild type (top) and the fah 1–2 mutant (middle) serve as positive and negative controls for the presence of syringyl lignin. DFRC lignin analysis was performed as previously described. DFRC analysis of a sample of Podocarpus macrophyllus (bottom) collected from the Chicago Botanic Garden reveals the presence of syringyl lignin in this gymnosperm. G/S, guaiacyl/syringyl lignin derivative; c/t: cis/trans; IS, internal standard.