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Research article - Peer-reviewed, 2020

A Comparative Transcriptome Analysis, Conserved Regulatory Elements and Associated Transcription Factors Related to Accumulation of Fusariotoxins in Grain of Rye (Secale cereale L.) Hybrids

Mahmood, Khalid; Orabi, Jihad; Kristensen, Peter Skov; Sarup, Pernille; Jorgensen, Lise Nistrup; Jahoor, Ahmed

Abstract

Detoxification of fusariotoxin is a type V Fusarium head blight (FHB) resistance and is considered a component of type II resistance, which is related to the spread of infection within spikes. Understanding this type of resistance is vital for FHB resistance, but to date, nothing is known about candidate genes that confer this resistance in rye due to scarce genomic resources. In this study, we generated a transcriptomic resource. The molecular response was mined through a comprehensive transcriptomic analysis of two rye hybrids differing in the build-up of fusariotoxin contents in grain upon pathogen infection. Gene mining identified candidate genes and pathways contributing to the detoxification of fusariotoxins in rye. Moreover, we found cis regulatory elements in the promoters of identified genes and linked them to transcription factors. In the fusariotoxin analysis, we found that grain from the Nordic seed rye hybrid "Helltop" accumulated 4 times higher concentrations of deoxynivalenol (DON), 9 times higher nivalenol (NIV), and 28 times higher of zearalenone (ZEN) than that of the hybrid "DH372" after artificial inoculation under field conditions. In the transcriptome analysis, we identified 6675 and 5151 differentially expressed genes (DEGs) in DH372 and Helltop, respectively, compared to non-inoculated control plants. A Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that DEGs were associated with glycolysis and the mechanistic target of rapamycin (mTOR) signaling pathway in Helltop, whereas carbon fixation in photosynthesis organisms were represented in DH372. The gene ontology (GO) enrichment and gene set enrichment analysis (GSEA) of DEGs lead to identification of the metabolic and biosynthetic processes of peptides and amides in DH372, whereas photosynthesis, negative regulation of catalytic activity, and protein-chromophore linkage were the significant pathways in Helltop. In the process of gene mining, we found four genes that were known to be involved in FHB resistance in wheat and that were differentially expressed after infection only in DH372 but not in Helltop. Based on our results, we assume that DH372 employed a specific response to pathogen infection that led to detoxification of fusariotoxin and prevented their accumulation in grain. Our results indicate that DH372 might resist the accumulation of fusariotoxin through activation of the glycolysis and drug metabolism via cytochrome P450. The identified genes in DH372 might be regulated by the WRKY family transcription factors as associated cis regulatory elements found in the in silico analysis. The results of this study will help rye breeders to develop strategies against type V FHB.

Keywords

cis-regulatory elements; disease resistance; Fusarium head blight; GO enrichment; hybrids; transcriptome; rye

Published in

International Journal of Molecular Sciences
2020, volume: 21, number: 19, article number: 7418
Publisher: MDPI

Authors' information

Mahmood, Khalid
Aarhus University
Orabi, Jihad
Nordic Seed A/S
Kristensen, Peter Skov
Nordic Seed AS
Sarup, Pernille
Nordic Seed AS
Jorgensen, Lise Nistrup
Aarhus University
Nordic Seed A/S
Swedish University of Agricultural Sciences, Department of Plant Breeding

Associated SLU-program

SLU Network Plant Protection

UKÄ Subject classification

Agricultural Science
Biochemistry and Molecular Biology

Publication Identifiers

DOI: https://doi.org/10.3390/ijms21197418

URI (permanent link to this page)

https://res.slu.se/id/publ/109314