title: High-resolution transcript profiling of the atypical biotrophic interaction between Theobroma cacao and the fungal pathogen Moniliophthora perniciosa.
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.
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil.
authors.forename: Paulo José Pereira Lima
authors.initials: PJ
authors.lastname: Teixeira
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil.
authors.forename: Daniela Paula de Toledo
authors.initials: DP
authors.lastname: Thomazella
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil.
authors.forename: Osvaldo
authors.initials: O
authors.lastname: Reis
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil.
authors.forename: Paula Favoretti Vital
authors.initials: PF
authors.lastname: do Prado
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil.
authors.forename: Maria Carolina Scatolin
authors.initials: MC
authors.lastname: do Rio
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil.
authors.forename: Gabriel Lorencini
authors.initials: GL
authors.lastname: Fiorin
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil.
authors.forename: Juliana
authors.initials: J
authors.lastname: José
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil.
authors.forename: Gustavo Gilson Lacerda
authors.initials: GG
authors.lastname: Costa
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil.
authors.forename: Victor Augusti
authors.initials: VA
authors.lastname: Negri
authors.affiliation: Centro de Pesquisa e Desenvolvimento em Recursos Genéticos Vegetais, Instituto Agronômico, Campinas SP 13001-970, Brazil.
authors.forename: Jorge Maurício Costa
authors.initials: JM
authors.lastname: Mondego
authors.affiliation: Department of Genetics, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599.
authors.forename: Piotr
authors.initials: P
authors.lastname: Mieczkowski
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas SP 13083-970, Brazil goncalo@unicamp.br.
authors.forename: Gonçalo Amarante Guimarães
authors.initials: GA
authors.lastname: Pereira
mesh_terms: D000363:Agaricales / Q000472:pathogenicity / Q000502:physiology*; D001483:Base Sequence; D002099:Cacao / Q000166:cytology / Q000235:genetics* / Q000382:microbiology; D016000:Cluster Analysis; D020869:Gene Expression Profiling; D015966:Gene Expression Regulation, Fungal; D018506:Gene Expression Regulation, Plant; D059014:High-Throughput Nucleotide Sequencing; D054884:Host-Pathogen Interactions; D008954:Models, Biological; D008969:Molecular Sequence Data; D025282:Mycelium; D010788:Photosynthesis; D010935:Plant Diseases / Q000382:microbiology*; D010940:Plant Proteins / Q000378:metabolism; D017423:Sequence Analysis, RNA; D059467:Transcriptome; D014774:Virulence
chemical_list: D010940:Plant Proteins