Abstract
BackgroundPlant pathogenesis related-1 (PR-1) proteins belong to the CAP superfamily and have been characterized as markers of induced defense against pathogens. Moniliophthora perniciosa and Moniliophthora roreri are hemibiotrophic fungi that respectively cause the witches’ broom disease and frosty pod rot in Theobroma cacao. Interestingly, a large number of plant PR-1-like genes are present in the genomes of both species and many are up-regulated during the biotrophic interaction. In this study, we investigated the evolution of PR-1 proteins from 22 genomes of Moniliophthora isolates and 16 other Agaricales species, performing genomic investigation, phylogenetic reconstruction, positive selection search and gene expression analysis.ResultsPhylogenetic analysis revealed conserved PR-1 genes (PR-1a, b, d, j), shared by many Agaricales saprotrophic species, that have diversified in new PR-1 genes putatively related to pathogenicity in Moniliophthora (PR-1f, g, h, i), as well as in recent specialization cases within M. perniciosa biotypes (PR-1c, k, l) and M. roreri (PR-1n). PR-1 families in Moniliophthora with higher evolutionary rates exhibit induced expression in the biotrophic interaction and positive selection clues, supporting the hypothesis that these proteins accumulated adaptive changes in response to host–pathogen arms race. Furthermore, although previous work showed that MpPR-1 can detoxify plant antifungal compounds in yeast, we found that in the presence of eugenol M. perniciosa differentially expresses only MpPR-1e, k, d, of which two are not linked to pathogenicity, suggesting that detoxification might not be the main function of most MpPR-1.ConclusionsBased on analyses of genomic and expression data, we provided evidence that the evolution of PR-1 in Moniliophthora was adaptive and potentially related to the emergence of the parasitic lifestyle in this genus. Additionally, we also discuss how fungal PR-1 proteins could have adapted from basal conserved functions to possible roles in fungal pathogenesis.
Highlights
Pathogenesis related-1 (PR-1) proteins are part of the CAP superfamily, known as SCP/ TAPS proteins, and are present throughout the eukaryotic kingdom [1, 2]
The sequences corresponding to MpPR-1l in the five S-biotype isolates from Minas Gerais were found in another orthogroup, in which MpPR-1l was fused to the adjacent gene in the genome with no start codon found between the two domains
We found that the MpPR-1i gene and, its predicted protein is truncated in almost all S-biotype isolates from MG (Fig. 4)
Summary
Pathogenesis related-1 (PR-1) proteins are part of the CAP (cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1) superfamily, known as SCP/ TAPS proteins (sperm-coating protein/Tpx-1/Ag5/PR-1/ Sc7), and are present throughout the eukaryotic kingdom [1, 2]. PR-1 proteins are regarded as markers of induced defense responses against pathogens [3]. (See figure on page.) Fig. 1 Characterization of PR-1 gene families in M. perniciosa and M. roreri genomes. A Heatmap of the number of gene copies per family of PR-1-like candidates per Moniliophthora isolate. B Amplification by PCR of MpPR-1c and MpPR-1d genes in the genomic DNA of eight M. perniciosa isolates. C Synteny analysis of a 10 Kb portion of the genome where the MpPR-1j, c, d genes are found in the three biotypes of M. perniciosa and M. roreri. Plant pathogenesis related-1 (PR-1) proteins belong to the CAP superfamily and have been characterized as markers of induced defense against pathogens. A large number of plant PR-1-like genes are present in the genomes of both species and many are up-regulated during the biotrophic interaction. We investigated the evolution of PR-1 proteins from 22 genomes of Moniliophthora isolates and 16 other Agaricales species, performing genomic investigation, phylogenetic reconstruction, positive selection search and gene expression analysis
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