Evolutionary Implications of a Peroxidase with High Affinity for Cinnamyl Alcohols from Physcomitrium patens, a Non-Vascular Plant.

Teresa Martínez-Cortés,Federico Pomar,Esther Novo-Uzal

doi:10.3390/plants10071476

Teresa Martínez-Cortés, Federico Pomar + Show 1 more

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https://doi.org/10.3390/plants10071476

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Abstract

Physcomitrium (Physcomitrella) patens is a bryophyte highly tolerant to different stresses, allowing survival when water supply is a limiting factor. This moss lacks a true vascular system, but it has evolved a primitive water-conducting system that contains lignin-like polyphenols. By means of a three-step protocol, including ammonium sulfate precipitation, adsorption chromatography on phenyl Sepharose and cationic exchange chromatography on SP Sepharose, we were able to purify and further characterize a novel class III peroxidase, PpaPrx19, upregulated upon salt and H2O2 treatments. This peroxidase, of a strongly basic nature, shows surprising homology to angiosperm peroxidases related to lignification, despite the lack of true lignins in P. patens cell walls. Moreover, PpaPrx19 shows catalytic and kinetic properties typical of angiosperm peroxidases involved in oxidation of monolignols, being able to efficiently use hydroxycinnamyl alcohols as substrates. Our results pinpoint the presence in P. patens of peroxidases that fulfill the requirements to be involved in the last step of lignin biosynthesis, predating the appearance of true lignin.

Highlights

Land colonization by plants and their subsequent diversification was one of the most important events in the history of life
We pursued the purification and further characterization of a strongly basic peroxidase that was induced by H2O2 and salt, two major stresses faced by the first plants that colonized land
The cell wall is characteristic of all plant cells, its composition varies depending on the cell type, the lineage and environmental conditions

Summary

Introduction

Land colonization by plants and their subsequent diversification was one of the most important events in the history of life. Plants developed different strategies to accumulate water in their tissues, to supply it or to minimize its loss. These first land plants, such as mosses, were poikilohydric, whose water potential was equilibrated with surrounding water sources [1]. The first evolutionary radiation among land plants is related to the diversification of tracheids, which appeared in vascular plants (tracheophytes), about 450 million years ago and they have been defined as single-celled conduits with lignin in their cell wall [2]. Lignins are mainly formed from the oxidative coupling of three p-hydroxycinnamyl alcohols: p-coumaryl, coniferyl and sinapyl alcohols (monolignols). The cross-coupling reaction of monolignol radicals produces a hydrophobic heteropolymer composed of p-hydroxyphenyl (H), guaiacyl (G) and syringyl (S) units [3]

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