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Title: Use of dual RNA-seq for systems biology analysis of zea mays and Aspergillus flavus interaction

Author
item Musungu, Bryan
item Bhatnagar, Deepak
item PAYNE, GARY - North Carolina State University
item O'BRIAN, GREG - North Carolina State University
item Quiniou, Sylvie
item GEISLER, MATT - Southern Illinois University
item FAKHOURY, AHMAD - Southern Illinois University

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/9/2020
Publication Date: 6/3/2020
Citation: Musungu, B.M., Bhatnagar, D., Payne, G.A., O'Brian, G., Quiniou, S., Geisler, M., Fakhoury, A. 2020. Use of dual RNA-seq for systems biology analysis of zea mays and Aspergillus flavus interaction. Frontiers in Microbiology. 11:853.

Interpretive Summary: The purpose of the study was to utilize a novel genomic approach to gain information to improve resistance of Zea mays (maize) to the mycotoxin producing pathogen Aspergillus flavus. Using genes expressed during the interaction between maize and A. flavus, pathways were identified in both organisms that seem to be synchronously modulated upon infection. hese pathways included pathways involved in secondary metabolism in fungi as well as plant defense pathways. This study can serve as a model that could be applied to study interactions in other pathosystems. The generated information also serves as a resource for the agronomy and plant pathology communities to improve breeding for resistance to aflatoxin accumulation and ear rots in corn.

Technical Abstract: The interaction between Aspergillus flavus and Zea mays is complex, and the identification of plant genes and pathways conferring resistance to the fungus has been challenging. Therefore, the authors undertook a systems biology approach involving dual RNA-seq to determine the simultaneous response from the host and the pathogen. What was dramatically highlighted in the analysis is the uniformity in the development patterns of gene expression of the host and the pathogen during infection. This led to the development of a “stage of infection index” that was subsequently used to categorize the samples before down-stream system biology analysis. Additionally, we were able to ascertain that key maize genes in pathways such as the jasmonate, ethylene and ROS pathways, were up-regulated in the study. The stage of infection index used for the transcriptomic analysis revealed that A. flavus produces a relatively limited number of transcripts during the early stages of infection. At later stages, in A. flavus, transcripts and pathways involved in endosomal transport, aflatoxin production, and carbohydrate metabolism were up-regulated. Multiple WRKY genes targeting the activation of the resistance pathways (i.e. jasmonate, phenylpropanoid and ethylene) were detected using causal inference analysis. This analysis also revealed, for the first time, the activation of Z. mays resistance genes influencing the expression of specific A. flavus genes. Our results show that A. flavus seems to be reacting to a hostile environment resulting from the activation of resistance pathways in Z. mays. This study revealed the dynamic nature of the interaction between the two organisms.