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As American cartoonist Charles Schulz once put it: “All you need is love. But a little chocolate now and then doesn’t hurt.” An aggressive and intractable hemibiotrophic fungus, Moniliophthora perniciosa, is ravaging chocolate tree (Theobroma cacao) plantations in many American countries, threatening livelihoods and the billion dollar cacao industry, and jeopardizing the world’s most beloved treat. M. perniciosa is the causal agent of witches’ broom disease, which results in yield reductions of 50 to 90% in infected regions (Meinhardt et al., 2008). Once the fungus enters a susceptible tree through stomata or wounds, it slowly grows between living plant cells. A key feature of the biotrophic stage of the disease is that the infected shoots lose apical dominance and morph into swollen structures called green brooms (see figure), which divert the plant’s energy from effective growth. Two to three months after infection, the disease enters the necrotrophic stage of development (Evans, 1980). The brooms become brown and eventually perish, giving rise to small, pink basidiocarps, which release millions of fungal spores capable of repeating the cycle in neighboring trees. M. perniciosa can tolerate high levels of fungicides, and there is no known treatment for witches’ broom disease.
M. perniciosa infection triggers loss of apical dominance and the formation of green brooms. A healthy plant is shown in the left panel and a green broom in the right. Arrows indicate loss of apical dominance in an infected T. cacao tree (right panel). (Photo courtesy of P.J. Teixeira.)
As an initial step toward developing strategies to combat this devastating tropical disease, Teixeira et al. (2014) sought to characterize the molecular interactions between M. perniciosa and T. cacao during the biotrophic stage of witches’ broom disease. Using dual RNA-seq analysis, the authors simultaneously monitored the transcriptomes of both the host and the pathogen in green brooms. They detected 1967 T. cacao genes that were differentially expressed in green brooms. Whereas genes related to plant defense responses, secondary metabolism, and cell wall modification were upregulated in green brooms, those involved in photosynthesis, starch biosynthesis, and nitrogen assimilation were repressed, indicating that fungal infection causes massive metabolic reprogramming in the diseased tissues. Consistent with the unusual morphology of infected tissues, HORMONOMETER analysis (Volodarsky et al., 2009) suggested that auxin and cytokinin responses were altered in these tissues. Furthermore, this approach revealed 8617 M. perniciosa genes that were expressed in green brooms. Using the WBD Transcriptome Atlas (www.lge.ibi.unicamp.br/wbdatlas), the authors identified 433 fungal transcripts that were particularly abundant in green brooms. Genes that encode secreted proteins and candidate secreted effector proteins were enriched in green broom structures, as were those encoding proteins with high levels of sequence similarity to proteins known to be involved in fungal pathogenesis.
Based on these results, the authors generated a model of the biotrophic interaction between M. perniciosa and T. cacao in which the fungus manipulates the metabolism of the host to increase nutrient availability before ultimately triggering premature senescence and cell death in the host. This study paves the way for developing strategies to combat witches’ broom disease and thus for securing an economically important and beloved crop.
