Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae

Marie-Line Kuhn,Franck Panabières,Jo-Yanne Le Berre,Naima Kebdani-Minet

doi:10.3390/microorganisms10020281

Abstract

Oomycetes, of the genus Phytophthora, comprise of some of the most devastating plant pathogens. Parasitism of Phytophthora results from evolution from an autotrophic ancestor and adaptation to a wide range of environments, involving metabolic adaptation. Sequence mining showed that Phytophthora spp. display an unusual repertoire of glycolytic enzymes, made of multigene families and enzyme replacements. To investigate the impact of these gene duplications on the biology of Phytophthora and, eventually, identify novel functions associated to gene expansion, we focused our study on the first glycolytic step on P. nicotianae, a broad host range pathogen. We reveal that this step is committed by a set of three glucokinase types that differ by their structure, enzymatic properties, and evolutionary histories. In addition, they are expressed differentially during the P. nicotianae life cycle, including plant infection. Last, we show that there is a strong association between the expression of a glucokinase member in planta and extent of plant infection. Together, these results suggest that metabolic adaptation is a component of the processes underlying evolution of parasitism in Phytophthora, which may possibly involve the neofunctionalization of metabolic enzymes.

Highlights

Oomycetes constitutes a group of lower eukaryotes that comprise of saprobes, as well as highly successful parasites of plant and animals [1]
Using a combination of phylogenetic, enzymatic, and transcriptional analyses, we reveal that this multigene family has a complex, innovative evolutionary history that is restricted to the genus Phytophthora among oomycetes
We propose that the evolution and diversification of the glucokinase gene family led to the acquisition of particular functions for its various members, as evidence of neofunctionalization

Summary

Introduction

Oomycetes constitutes a group of lower eukaryotes that comprise of saprobes, as well as highly successful parasites of plant and animals [1]. Considered as fungi, on the basis of filamentous morphology, osmotrophic uptake of nutrients, and shared ecological niches, oomycetes are currently placed together with diatoms and brown algae within stramenopiles [2,3]. They are thought to have evolved from marine environments and adapted to a wide range of niches and lifestyles [4]. Peronosporales include animal, plant, fungal, and oomycete parasites, as well as a non-pathogenic species. This large order includes several thousands of both formal and provisional species.

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Conclusion