Epigenetic control of Fusarium head blight resistance in durum wheat

Authors: KUMAR, JITENDRA - University Of Minnesota; RAI, KRISHAN - University Of Minnesota; PIRSEYEDI, SEYED - North Dakota State University; ELIAS, ELIAS - North Dakota State University; Xu, Steven; DILL-MACKY, RUTH - University Of Minnesota; Kianian, Shahryar

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/14/2020
Publication Date: 10/19/2020
Citation: Kumar, J., Rai, K.M., Pirseyedi, S.M., Elias, E.M., Xu, S.S., Dill-Macky, R., Kianian, S.F. 2020. Epigenetic control of Fusarium head blight resistance in durum wheat. Frontiers in Plant Science. 10. Article: 17610. https://doi.org/10.1038/s41598-020-73521-2.
DOI: https://doi.org/10.1038/s41598-020-73521-2

Interpretive Summary: Fusarium head blight (FHB) is a major disease of bread wheat, durum wheat and barley affecting yield and quality in majority of the U.S. growing regions. Durum lines that are genetically resistant to FHB are critical to continued production of this important crop in the United States. Despite effort of researchers and advances in recent years, there is a need to develop even more resistant durum cultivars. Various studies suggest that either the cultivated durum genome carries a suppressor of FHB resistance or is missing enhancers of resistance on D-genome chromosomes. To test these hypotheses, we treated several popular durum cultivars with a chemical mutagen that removes CG methylation. These lines were advanced and tested for FHB resistance. Our repeated tests over several years in field nurseries (various locations in ND and MN) and greenhouse screening have identified 5 lines that are significantly more resistant than parental lines and durum checks. These lines also have significantly lower damaged kernels and Fusarium toxin in their grain. We have crossed these lines to popular durum cultivars aimed at testing the stability and inheritance of resistance. Additionally, we have obtained RNA sequence data from various tissues with and without Fusarium infection from one of these lines along with controls, to determine changes that are responsible for the enhanced resistance. Additionally, these lines are being utilized in breeding more resistant germplasm as well as being characterized for the genetic basis of resistance.

Technical Abstract: DNA methylation plays an important role in plant responses to various stress factors; however, there is little or no information on its role in immunity against Fusarium graminearum. In the present study, eight advanced durum-breeding lines were treated with 5-methyl-azacytidine to remove cytosine DNA methylation to test the feasibility of generating source of Fusarium head blight (FHB) resistance in durum wheat. A total of 415 progeny of the treated plants were advanced up to four (M4) generations. Thirty-two of the 415 M4 lines were selected following preliminary FHB testing. The 32 promising lines and eight parental checks were further tested for FHB resistance for multiple years (3 years), locations (2 locations), and settings (greenhouse vs field conditions). Five of the 32 M4 lines consistently showed less than 30% FHB severity, as compared with the parental lines and FHB-susceptible lines, which ranged above 30%. Fusarium-damaged kernels (FDK) and deoxynivalenol (DON) analyses on grain harvested from inoculated plants further supported the greenhouse and field disease assessments. To test the stability and inheritance of the epigenetic resistance, two of the most resistant M4 lines were crossed to a susceptible parent and advanced for two generations without selection. The backcross-derived families were tested for FHB resistance in third generation (BC1:F3) and a number of lines showed FHB resistance similar to or better than the resistant M4 parent indicating stable inheritance of modified status. The overall methylation level (%) between M4 and parental lines were compared using FASTmC method indicating no significant difference. However, transcriptome analysis of a selected M4 line revealed a number of differentially expressed genes (=2 folds; log2 value) as compared to the susceptible parent. The differentially expressed genes belonged to PR-proteins, oxidative stress, transcription factors, secondary metabolite, signaling, cell wall, proteolysis and metabolic pathways and have been reported to play crucial roles in FHB resistance. Significantly up-regulated genes related to biosynthesis of secondary metabolites, photosynthesis, starch and sucrose metabolism, plant hormone signal transduction and plant-pathogen interaction pathways that may have equipped the M4 line to fight Fusarium infection.