High-Resolution Transcript Profiling of the Atypical Biotrophic Interaction betweenTheobroma cacaoand the Fungal PathogenMoniliophthora 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.

Plant pathogenesis–related proteins of the cacao fungal pathogen Moniliophthora perniciosa differ in their lipid-binding specificities

“…Furthermore, gene expression analyses revealed that some of M. perniciosa CAP genes, termed MpPR-1 genes, are highly and specifically expressed during the green broom stage of WBD, and in germinating basidiospores (4,26). These results suggest that some MpPR-1 proteins function during the M. perniciosa infective process.…”

“…These chlorotic and swollen shoots are formed as a consequence of a hormonal imbalance and intense reprogramming of the plant metabolism induced by the fungal infection (4,5). The necrotrophic phase of the disease begins upon death of plant tissues, which are invaded by the proliferative mycelia.…”

“…A genome draft of M. perniciosa (6), a comprehensive transcriptomic analysis of the biotrophic stage of the interaction (4), and a series of functional analyses of M. perniciosa proteins provided insights into this intriguing disease (7)(8)(9)(10).…”

Dual RNA-Sequencing to Elucidate the Plant-Pathogen Duel

“…This tactic, known as dual RNAseq, in planta RNA-seq, simultaneous RNA-seq, or comparative RNA-seq, is a relatively new technique both in the plant and medical fields. In plants, it allows for the study of plant-pathogen interactions in herbaceous crops Kunjeti et al, 2012;Lowe et al, 2014) as well as trees (Hayden et al, 2014;Liang et al, 2014;Teixeira et al, 2014). This review outlines technical considerations for dual RNA-seq experiments, summarizes recent insights drawn from such approaches in plant-pathogen interactions, and provides an overview of the next generation of dual approaches.…”

“…In dual RNA-seq experiments, reads are mapped to the host reference sequence and the unaligned sequences are retained and mapped to the pathogen reference sequence (Teixeira et al, 2014). A common program used for read alignment to a reference is the short read aligner Bowtie, which is part of the Tophat package of the Tuxedo pipeline (Trapnell et al, 2012).…”