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.
Highlights
Crop diseases caused by fungi severely limit agricultural productivity, leading to drastic economic losses each year (Fisher et al, 2012)
We evaluated the evolutionary pattern of the M. perniciosa candidate secreted effector proteins (CSEPs) by performing a comparative analysis with Moniliophthora roreri, a recently sequenced cacao pathogen that is closely related to M. perniciosa (Meinhardt et al, 2014)
During the prolonged biotrophic phase of witches’ broom disease (WBD), cacao plants appear to expend large amounts of energy to sustain the exaggerated growth of infected tissues; we found that remarkable transcriptional alterations related to plant carbohydrate metabolism take place in green brooms
Summary
Crop diseases caused by fungi severely limit agricultural productivity, leading to drastic economic losses each year (Fisher et al, 2012). In. Tropical areas have a suitable climate for the cultivation of a large number of crops. Tropical areas have a suitable climate for the cultivation of a large number of crops They are highly prone to the development of a variety of pathogenic microorganisms. The basidiomycete Moniliophthora perniciosa causes witches’ broom disease (WBD) in Theobroma cacao, the chocolate tree (Aime and Phillips-Mora, 2005). This highly destructive disease has negatively affected cacao productivity in many American countries and is a threat to global cocoa production (Purdy and Schmidt, 1996; Meinhardt et al, 2008).
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