Abstract

BackgroundPlant inducible immunity includes the accumulation of a set of defense proteins during infection called pathogenesis-related (PR) proteins, which are grouped into families termed PR-1 to PR-17. The PR-5 family is composed of thaumatin-like proteins (TLPs), which are responsive to biotic and abiotic stress and are widely studied in plants. TLPs were also recently discovered in fungi and animals. In the poplar genome, TLPs are over-represented compared with annual species and their transcripts strongly accumulate during stress conditions.ResultsOur analysis of the poplar TLP family suggests that the expansion of this gene family was followed by diversification, as differences in expression patterns and predicted properties correlate with phylogeny. In particular, we identified a clade of poplar TLPs that cluster to a single 350 kb locus of chromosome I and that are up-regulated by poplar leaf rust infection. A wider phylogenetic analysis of eukaryote TLPs - including plant, animal and fungi sequences - shows that TLP gene content and diversity increased markedly during land plant evolution. Mapping the reported functions of characterized TLPs to the eukaryote phylogenetic tree showed that antifungal or glycan-lytic properties are widespread across eukaryote phylogeny, suggesting that these properties are shared by most TLPs and are likely associated with the presence of a conserved acidic cleft in their 3D structure. Also, we established an exhaustive catalog of TLPs with atypical architectures such as small-TLPs, TLP-kinases and small-TLP-kinases, which have potentially developed alternative functions (such as putative receptor kinases for pathogen sensing and signaling).ConclusionOur study, based on the most recent plant genome sequences, provides evidence for TLP gene family diversification during land plant evolution. We have shown that the diverse functions described for TLPs are not restricted to specific clades but seem to be universal among eukaryotes, with some exceptions likely attributable to atypical protein structures. In the perennial plant model Populus, we unravelled the TLPs likely involved in leaf rust resistance, which will provide the foundation for further functional investigations.

Highlights

  • Plant inducible immunity includes the accumulation of a set of defense proteins during infection called pathogenesis-related (PR) proteins, which are grouped into families termed PR-1 to PR-17

  • The gene structure of poplar thaumatin-like protein (TLP) is well conserved within clades 1-3, with genes belonging to clade 1 formed by a single exon, TLPs from clade 2 by two exons and TLPs of clade 3 by three exons (Figure 1); clade 4 is an exception with genes composed of one, two or three exons

  • TLPs are eukaryote proteins that constitute small and monophyletic families in invertebrate animals and fungi whereas they are more diverse and are organized in large multigene families in plants. Regardless of their origin, it appears that many typical TLPs possess an antifungal activity, which is probably linked to a conserved acidic cleft in their 3D structure

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Summary

Introduction

Plant inducible immunity includes the accumulation of a set of defense proteins during infection called pathogenesis-related (PR) proteins, which are grouped into families termed PR-1 to PR-17. The PR-5 family is composed of thaumatin-like proteins (TLPs), which are responsive to biotic and abiotic stress and are widely studied in plants. Plants respond to challenge from pathogens by activating an inducible protein-based defense system that includes 17 families of pathogenesis-related (PR) proteins termed PR-1 to PR-17 [1,2]. Other functional properties have been reported for TLPs, including antifreeze activity [15], protection from abiotic stress [16] and binding to proteins such as actin, viral CMV-1 protein, yeast glycoproteins and G-Protein Coupled Receptor (GPCR) or to hormones such as cytokinins [7]

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