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

• Published in: The Plant cell Vol. 26; no. 11; pp. 4245 - 4269
• Main Authors: Teixeira, Paulo José Pereira Lima, de Toledo Thomazella, Daniela Paula, Reis, Osvaldo, do Prado, Paula Favoretti Vital, do Rio, Maria Carolina Scatolin, Fiorin, Gabriel Lorencini, José, Juliana, Costa, Gustavo Gilson Lacerda, Negri, Victor Augusti, Mondego, Jorge Maurício Costa, Mieczkowski, Piotr, Pereira, Gonçalo Amarante Guimarães
• Format: Journal Article
• Language: English
• Published: United States American Society of Plant Biologists 01-11-2014
• Subjects: Agaricales - pathogenicity; Agaricales - physiology; Base Sequence; Brooms; Cacao; Cacao - cytology; Cacao - genetics; Cacao - microbiology; Cluster Analysis; Datasets; Fungi; Gene Expression Profiling; Gene Expression Regulation, Fungal; Gene Expression Regulation, Plant; Genes; High-Throughput Nucleotide Sequencing; Host-Pathogen Interactions; Infections; Large-Scale Biology; LARGE-SCALE BIOLOGY ARTICLE; Models, Biological; Molecular Sequence Data; Mycelium; Pathogens; Photosynthesis; Plant cells; Plant Diseases - microbiology; Plant Proteins - metabolism; Plants; Sequence Analysis, RNA; Theobroma cacao; Transcriptome; Transcriptomes; Virulence
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1105/tpc.114.130807

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.