Location: Sustainable Perennial Crops LaboratoryTitle: Differential gene expression by Moniliophthora roreri while overcoming cacao tolerance in the field) Author
Submitted to: Molecular Plant Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/25/2014
Publication Date: 2/25/2014
Citation: Bailey, B.A., Melnick, R.L., Strem, M.D., Crozier, J., Shao, J.Y., Sicher, Jr., R.C., Ali, S.S., Zhang, D., Philips-Mora, W., Meinhardt, L.W. 2014. Differential gene expression by Moniliophthora roreri while overcoming cacao tolerance in the field. Molecular Plant Pathology. DOI:10.1111/mpp.12134. Interpretive Summary: The fungus Monilophthora roreri causes frosty pod rot, a devastating disease on Theobroma cacao (cacao), the source of chocolate. Cacao clones showing tolerance against frosty pod rot are being planted throughout Central America. A significant concern associated with the planting of tolerant clones is that the fungus may mutate and overcome the tolerance making them highly susceptible to frosty pod rot. We characterized fungal gene expression associated with infections of tolerant clones. The fungus alters its gene expression patterns when infecting tolerant clones, increasing expression of stress response genes. The genes identified likely contribute to the fungus overcoming cacao defense mechanisms in tolerant clones. By understanding how the fungus causes disease on tolerant cacao clones, we can optimize breeding programs that are selecting tolerance to frosty pod rot, influence farming practices associated with the use of tolerant clones, and extend the usefulness of tolerant clones in the field. Chocolate is combined with United States agricultural products providing direct benefit to the American farmer. The extended use of tolerant clones should help stabilize and increase cacao supplies resulting to increased benefits to the cacao farmer, the cacao industry, and the American farmer.
Technical Abstract: Frosty pod rot (FPR), caused by the hemibiotrophic fungus Moniliophthora roreri (Mr), can destroy 100% of pods in susceptible Theoborma cacao (cacao) fields under favorable conditions. Cacao clones with high levels of tolerance to FPR are being deployed throughout Central America. To determine whether Mr had a differential molecular response during successful infections of tolerant clones, we collected field infected pods at all stages of symptomology for five cacao clones. Two clones were highly susceptible (Pound-7 and CATIE-1000) and three clones were tolerant (UF-273, CATIE-R7, and CATIE-R4). RNA-Seq analysis of RNA samples from infected pods of Pound-7, CATIE-1000, CATIE-R4 and CATIE-R7 identified a set of 872 Mr genes that were differentially expressed between clones with the primary difference being whether the clone was susceptible or tolerant to FPR. Metabolite analysis was also carried out. As FPR progressed, the concentrations of sugars in pods of Pound-7, CATIE-1000, CATIE-R7, and CATIE-R4 dropped while levels of trehalose and mannitol increased. Associations between disease parameters (symptoms and infection level) and some organic and amino acids concentrations varied depending on the clone considered. The differential Mr gene expression between clones of a subset of forty two Mr genes was validated by RT-qPCR. Expression of Mr genes in the majority of infected pods from tolerant clones resembled that observed in the necrotrophic phase of the disease cycle. Mr transcription factors, small heat proteins, transporters, enzymes modifying fungal or plant membranes or cell walls, and several metabolic processes including the glyoxylate cycle and alternative oxidase were differentially expressed between tolerant and susceptible clones. Successful Mr infection of tolerant clones, although uncommon, altered expression of Mr genes which may benefit the fungus in overcoming cacao defense mechanisms.