Use of Dual RNA-seq for Systems Biology Analysis of Zea mays and Aspergillus flavus Interaction

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 f...

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Main Authors: Bryan Musungu, Deepak Bhatnagar, Sylvie Quiniou, Robert L. Brown, Gary A. Payne, Greg O’Brian, Ahmad M. Fakhoury, Matt Geisler
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.00853/full
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author Bryan Musungu
Deepak Bhatnagar
Sylvie Quiniou
Robert L. Brown
Gary A. Payne
Greg O’Brian
Ahmad M. Fakhoury
Matt Geisler
author_facet Bryan Musungu
Deepak Bhatnagar
Sylvie Quiniou
Robert L. Brown
Gary A. Payne
Greg O’Brian
Ahmad M. Fakhoury
Matt Geisler
author_sort Bryan Musungu
collection DOAJ
description 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 (0 to 12 h) 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.
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spelling doaj.art-0989a1a986df49ab9eb352088851bbe72022-12-21T23:47:40ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-06-011110.3389/fmicb.2020.00853497237Use of Dual RNA-seq for Systems Biology Analysis of Zea mays and Aspergillus flavus InteractionBryan Musungu0Deepak Bhatnagar1Sylvie Quiniou2Robert L. Brown3Gary A. Payne4Greg O’Brian5Ahmad M. Fakhoury6Matt Geisler7Department of Plant Biology, Southern Illinois University, Carbondale, IL, United StatesSouthern Regional Research Center, USDA-ARS, New Orleans, LA, United StatesWarm Water Aquaculture Research Unit, USDA-ARS, Stoneville, MS, United StatesSouthern Regional Research Center, USDA-ARS, New Orleans, LA, United StatesDepartment of Plant Pathology, North Carolina State University, Raleigh, NC, United StatesDepartment of Plant Pathology, North Carolina State University, Raleigh, NC, United StatesDepartment of Plant Soil and Agriculture Systems, Southern Illinois University, Carbondale, IL, United StatesDepartment of Plant Biology, Southern Illinois University, Carbondale, IL, United StatesThe 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 (0 to 12 h) 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.https://www.frontiersin.org/article/10.3389/fmicb.2020.00853/fullinteractomemaizeAspergillus flavusaflatoxingene regulatory network
spellingShingle Bryan Musungu
Deepak Bhatnagar
Sylvie Quiniou
Robert L. Brown
Gary A. Payne
Greg O’Brian
Ahmad M. Fakhoury
Matt Geisler
Use of Dual RNA-seq for Systems Biology Analysis of Zea mays and Aspergillus flavus Interaction
Frontiers in Microbiology
interactome
maize
Aspergillus flavus
aflatoxin
gene regulatory network
title Use of Dual RNA-seq for Systems Biology Analysis of Zea mays and Aspergillus flavus Interaction
title_full Use of Dual RNA-seq for Systems Biology Analysis of Zea mays and Aspergillus flavus Interaction
title_fullStr Use of Dual RNA-seq for Systems Biology Analysis of Zea mays and Aspergillus flavus Interaction
title_full_unstemmed Use of Dual RNA-seq for Systems Biology Analysis of Zea mays and Aspergillus flavus Interaction
title_short Use of Dual RNA-seq for Systems Biology Analysis of Zea mays and Aspergillus flavus Interaction
title_sort use of dual rna seq for systems biology analysis of zea mays and aspergillus flavus interaction
topic interactome
maize
Aspergillus flavus
aflatoxin
gene regulatory network
url https://www.frontiersin.org/article/10.3389/fmicb.2020.00853/full
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