Adaptive evolution of Moniliophthora PR-1 proteins towards its pathogenic lifestyle

Author(s):Show less -

Vasconcelos, Adrielle A. ^[1] ; Jose, Juliana ^[1] ; Tokimatu, Paulo M. ^[1] ; Camargo, Antonio P. ^[1] ; Teixeira, Paulo J. P. L. ^[2] ; Thomazella, Daniela P. T. ^[1] ; do Prado, V, Paula F. ; Fiorin, Gabriel L. ^[3] ; Costa, Juliana L. ^[4] ; Figueira, Antonio ^[4] ; Carazzolle, Marcelo F. ^[3] ; Pereira, Goncalo A. G. ^[3] ; Baroni, Renata M. ^[3]

Affiliation

^[1] Univ Estadual Campinas, Inst Biol, Dept Genet Evolucao Microbiol & Imunol, Campinas, SP - Brazil

^[2] Univ Sao Paulo, Dept Ciencias Biol, Escola Super Agr Luiz de Queiroz ESALQ, Piracicaba, SP - Brazil

^[3] do Prado, Paula F., V, Univ Estadual Campinas, Inst Biol, Dept Genet Evolucao Microbiol & Imunol, Campinas, SP - Brazil

^[4] Univ Sao Paulo, Ctr Energia Nucl Agr, Piracicaba, SP - Brazil

• Document type: Journal article
• Source: BMC ECOLOGY AND EVOLUTION; v. 21, n. 1 MAY 14 2021.
• Web of Science Citations: 0

Abstract

Background Plant 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. Results Phylogenetic 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. Conclusions Based 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. (AU)

• FAPESP's process: 16/10498-4 - Investigation of strategies of adaptation to the pathogenic life style of fungi from the Moniliophthora genus at various levels of biological organizations: species, biotypes, and geographic lineages
• Grantee: Antonio Vargas de Oliveira Figueira
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 18/04240-0 - Metagenomic investigation of the microbiomes of plants adapted to phosphorus nutritional limitation
• Grantee: Antônio Pedro de Castello Branco da Rocha Camargo
• Support Opportunities: Scholarships in Brazil - Doctorate
• FAPESP's process: 14/06181-0 - Development of a CRISPR/Cas9-based methodology for genome engineering in the fungus Moniliophthora perniciosa, the causal agent of witches' broom disease of cacao
• Grantee: Gabriel Lorencini Fiorin
• Support Opportunities: Scholarships in Brazil - Master
• FAPESP's process: 13/09878-9 - Functional characterization of a chitinase-like protein of Moniliophthora perniciosa with a potential role in fungal pathogenicity during the development of the witches' broom disease of cacao
• Grantee: Gabriel Lorencini Fiorin
• Support Opportunities: Scholarships abroad - Research Internship - Scientific Initiation
• FAPESP's process: 13/08293-7 - CCES - Center for Computational Engineering and Sciences
• Grantee: Munir Salomao Skaf
• Support Opportunities: Research Grants - Research, Innovation and Dissemination Centers - RIDC
• FAPESP's process: 17/13015-7 - Investigation of global transcriptional alterations in the Theobroma cacao x Moniliophthora perniciosa pathosystem during the progression of Witches Broom Disease of cacao
• Grantee: Adrielle Ayumi de Vasconcelos
• Support Opportunities: Scholarships in Brazil - Doctorate (Direct)
• FAPESP's process: 14/00802-2 - Molecular characterization of strobilurin resistance mechanisms in Moniliophthora perniciosa, the causal agent of the devastating witches' broom disease of cacao
• Grantee: Paula Favoretti Vital Do Prado
• Support Opportunities: Scholarships abroad - Research Internship - Master's degree
• FAPESP's process: 17/13319-6 - Identification of MpPR1-I protein ligands and structural and functional analyses of MpPR-1s of Moniliophthora perniciosa in vitro
• Grantee: Renata Moro Baroni
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 13/05979-5 - Molecular characterization of mechanisms of strobilurin resistance in Moniliophthora perniciosa, the causal agent of witches' broom disease of cacao
• Grantee: Paula Favoretti Vital Do Prado
• Support Opportunities: Scholarships in Brazil - Master
• FAPESP's process: 13/04309-6 - Functional analysis of cacao signalling and defense genes in the interaction Moniliophthora perniciosa x Solanum lycopersicum
• Grantee: Juliana Leles Costa
• Support Opportunities: Scholarships in Brazil - Doctorate
• FAPESP's process: 11/23315-1 - Functional characterization of a chitinase-like protein of Moniliophthora perniciosa with a potential role in fungal pathogenicity during the development of the witches' broom disease of cacao
• Grantee: Gabriel Lorencini Fiorin
• Support Opportunities: Scholarships in Brazil - Scientific Initiation