Transcriptome analysis of Epichloë strains in tall fescue in response to drought stress

Authors: NAGABHYRU, PADMAJA - University Of Kentucky; Dinkins, Randy; SCHARDL, CHRISTOPHER - University Of Kentucky

Submitted to: Mycologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/28/2022
Publication Date: 6/7/2022
Citation: Nagabhyru, P., Dinkins, R.D., Schardl, C.L. 2022. Transcriptome analysis of Epichloë strains in tall fescue in response to drought stress. Mycologia. 114(4):697-712. https://doi.org/10.1080/00275514.2022.2060008.
DOI: https://doi.org/10.1080/00275514.2022.2060008

Interpretive Summary: Epichloë coenophiala, is a seed-borne fungal symbiont (endophyte) of tall fescue and has been documented to confer better persistence to tall fescue plants than plants lacking the endophyte, especially under stress conditions. How the endophyte senses and responds to stress when the host plant is subjected to stress has not been previously characterized. Thus, this work was done to investigate the effects on gene expression of E. coenophiala, and closely related non-toxic producing endophytes, when tall fescue plants were subjected to acute water-deficit stress. Plants harboring different endophyte strains were grown in the greenhouse, then half were deprived of water for 48 hours and the other half remained under the regular watering regime. RNA was isolated from different plant tissues and whole transcriptome sequencing (mRNA-seq) was conducted to identify genes that were differentially expressed under the stress treatment. Our results showed that the fungal response to drought involved gene-expression changes in similar pathways that have been documented for plants under stress. Increased expression of genes involved in oxidative stress response, oxygen radical detoxification, heat shock, cellular transport and carbohydrate metabolism pathways were observed. The magnitude of fungal gene responses during stress depended and varied with the host plant and endophyte strain. Our results suggest that Epichloë fungi, along with their host plants, cooperate to regulate stress responses or to separately activate stress response mechanisms, that when combined together for mutual protection, results in better plant persistence.

Technical Abstract: Epichloë coenophiala, a systemic fungal symbiont (endophyte) of tall fescue (Lolium arundinaceum) has been documented to confer to this grass better persistence than plants lacking the endophyte, especially under stress conditions such as drought. The response, if any, of the endophyte to imposition of stress on the host plant has not been characterized previously. Therefore, we investigated effects on gene expression by E. coenophiala and a related endophyte when plant-endophyte symbiota were subjected to acute water-deficit stress. Plants harboring different endophyte strains were grown in sand in the greenhouse, then half were deprived of water for 48 hours and the other half were watered controls. RNA was isolated from different plant tissues and mRNA sequencing (RNA-seq) was conducted to identify genes that were differentially expressed comparing stress treatment with control. We compared two different plants harboring the common toxic E. coenophiala strain (CTE) and two non-ergot-alkaloid producing Epichloë strains in tall fescue pseudostems, and in a second experiment we compared responses of the two CTE strains in plant pseudostem and crown tissues. The endophytes responded to the stress with increased expression of genes involved in oxidative stress response, oxygen radical detoxification, C-compound carbohydrate metabolism, heat shock and cellular transport pathways. The magnitude of fungal gene responses during stress depended and varied on the host plant and endophyte strain. Responses in pseudostem and crown involved some common pathways as well as some tissue-specific pathways. The fungal response to water deficit stress involved gene-expression changes in similar pathways that have been documented for plant stress responses indicating that Epichloë spp. and their host plants either coordinate stress responses or separately activate similar stress response mechanisms that work together for mutual protection.