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Research ArticleLARGE-SCALE BIOLOGY ARTICLE
Open Access

High-Resolution Transcript Profiling of the Atypical Biotrophic Interaction between Theobroma cacao and the Fungal Pathogen Moniliophthora perniciosa

Paulo José Pereira Lima Teixeira, Daniela Paula de Toledo Thomazella, Osvaldo Reis, Paula Favoretti Vital do Prado, Maria Carolina Scatolin do Rio, Gabriel Lorencini Fiorin, Juliana José, Gustavo Gilson Lacerda Costa, Victor Augusti Negri, Jorge Maurício Costa Mondego, Piotr Mieczkowski, Gonçalo Amarante Guimarães Pereira
Paulo José Pereira Lima Teixeira
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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Daniela Paula de Toledo Thomazella
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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Osvaldo Reis
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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Paula Favoretti Vital do Prado
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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Maria Carolina Scatolin do Rio
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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Gabriel Lorencini Fiorin
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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Juliana José
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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Gustavo Gilson Lacerda Costa
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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Victor Augusti Negri
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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Jorge Maurício Costa Mondego
Centro de Pesquisa e Desenvolvimento em Recursos Genéticos Vegetais, Instituto Agronômico, Campinas SP 13001-970, Brazil
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Piotr Mieczkowski
Department of Genetics, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599
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Gonçalo Amarante Guimarães Pereira
Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil
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  • For correspondence: goncalo@unicamp.br

Published November 2014. DOI: https://doi.org/10.1105/tpc.114.130807

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  • © 2014 American Society of Plant Biologists. All rights reserved.

Abstract

Witches’ broom disease (WBD), caused by the hemibiotrophic fungus Moniliophthora perniciosa, is one of the most devastating diseases of Theobroma cacao, the chocolate tree. In contrast to other hemibiotrophic interactions, the WBD biotrophic stage lasts for months and is responsible for the most distinctive symptoms of the disease, which comprise drastic morphological changes in the infected shoots. Here, we used the dual RNA-seq approach to simultaneously assess the transcriptomes of cacao and M. perniciosa during their peculiar biotrophic interaction. Infection with M. perniciosa triggers massive metabolic reprogramming in the diseased tissues. Although apparently vigorous, the infected shoots are energetically expensive structures characterized by the induction of ineffective defense responses and by a clear carbon deprivation signature. Remarkably, the infection culminates in the establishment of a senescence process in the host, which signals the end of the WBD biotrophic stage. We analyzed the pathogen’s transcriptome in unprecedented detail and thereby characterized the fungal nutritional and infection strategies during WBD and identified putative virulence effectors. Interestingly, M. perniciosa biotrophic mycelia develop as long-term parasites that orchestrate changes in plant metabolism to increase the availability of soluble nutrients before plant death. Collectively, our results provide unique insight into an intriguing tropical disease and advance our understanding of the development of (hemi)biotrophic plant-pathogen interactions.

  • Glossary

    WBD
    witches’ broom disease
    qPCR
    quantitative real-time PCR
    PCA
    principal component analysis
    FDR
    false discovery rate
    RPKM
    reads per kilobase per million mapped reads
    CSEP
    candidate secreted effector protein
    GO
    Gene Ontology
    ROS
    reactive oxygen species
    • Received September 1, 2014.
    • Revised September 1, 2014.
    • Accepted October 15, 2014.
    • Published November 4, 2014.

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    High-Resolution Transcript Profiling of the Atypical Biotrophic Interaction between Theobroma cacao and the Fungal Pathogen Moniliophthora perniciosa
    Paulo José Pereira Lima Teixeira, Daniela Paula de Toledo Thomazella, Osvaldo Reis, Paula Favoretti Vital do Prado, Maria Carolina Scatolin do Rio, Gabriel Lorencini Fiorin, Juliana José, Gustavo Gilson Lacerda Costa, Victor Augusti Negri, Jorge Maurício Costa Mondego, Piotr Mieczkowski, Gonçalo Amarante Guimarães Pereira
    The Plant Cell Nov 2014, 26 (11) 4245-4269; DOI: 10.1105/tpc.114.130807

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    High-Resolution Transcript Profiling of the Atypical Biotrophic Interaction between Theobroma cacao and the Fungal Pathogen Moniliophthora perniciosa
    Paulo José Pereira Lima Teixeira, Daniela Paula de Toledo Thomazella, Osvaldo Reis, Paula Favoretti Vital do Prado, Maria Carolina Scatolin do Rio, Gabriel Lorencini Fiorin, Juliana José, Gustavo Gilson Lacerda Costa, Victor Augusti Negri, Jorge Maurício Costa Mondego, Piotr Mieczkowski, Gonçalo Amarante Guimarães Pereira
    The Plant Cell Nov 2014, 26 (11) 4245-4269; DOI: 10.1105/tpc.114.130807
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