High-Resolution Transcript Profiling of the Atypical Biotrophic Interaction between Theobroma cacao and the Fungal Pathogen Moniliophthora perniciosa[C][W][OPEN]

P. Teixeira,D. P. Thomazella,O. Reis,P. F. D. do Prado,M. C. S. do Rio,G. L. Fiorin,J. José,G. G. Costa,V. A. Negri,J. M. Mondego,P. Mieczkowski,G. Pereira

Published 2014 in The Plant Cell

ABSTRACT

This work dissects the intriguing biotrophic interaction between Theobroma cacao and the fungus Moniliophthora perniciosa in the devastating witches’ broom disease. Infection by M. perniciosa leads to massive genetic reprogramming in cacao tissues, which culminates in the onset of premature senescence. A detailed molecular model of this peculiar plant-pathogen interaction is presented. 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.

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