Azolla ferns testify: seed plants and ferns share a common ancestor for leucoanthocyanidin reductase enzymes

Erbil Güngör, Paul Brouwer, Laura W. Dijkhuizen, Dally Chaerul Shaffar, Klaas G.J. Nierop, C.H. de Vos, Javier Sastre Toraño, Ingrid M. van der Meer, Henriette Schluepmann*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

3 Citations (Scopus)

Abstract

Questions about in vivo substrates for proanthocyanidin (PA) biosynthesis and condensation have not been resolved and wide gaps in the understanding of transport and biogenesis in ‘tannosomes’ persist. Here we examined the evolution of PA biosynthesis in ferns not previously reported, asking what PAs are synthesised and how.
Chemical and gene‐expression analyses were combined to characterise PA biosynthesis, leveraging genome annotation from the floating fern Azolla filiculoides. In vitro assay and phylogenomics of PIP‐dehydrogenases served to infer the evolution of leucoanthocyanidin reductase (LAR).
Sporophyte‐synthesised (epi)catechin polymers, averaging only seven subunits, accumulated to 5.3% in A. filiculoides, and 8% in A. pinnata biomass dry weight. Consistently, a LAR active in vitro was highly expressed in A. filiculoides. LAR, and paralogous fern WLAR‐enzymes with differing substrate binding sites, represent an evolutionary innovation of the common ancestor of fern and seed plants.
The specific ecological niche of Azolla ferns, a floating plant–microbe mat massively fixing CO2 and N2, shaped their metabolism in which PA biosynthesis predominates and employs novel fern LAR enzymes. Characterisation of in vivo substrates of these LAR, will help to shed light on the recently assigned and surprising dual catalysis of LAR from seed plants.
Original languageEnglish
Pages (from-to)1118-1132
JournalNew Phytologist
Volume229
Issue number2
Early online date28 Aug 2020
DOIs
Publication statusPublished - Jan 2021

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