Genetic Diversity of the Symbiotic Fungus Epichloë festucae in Naturally Occurring Host Grass Populations

Epichloë festucae is a common symbiont of the perennial and widely distributed cool season grass, Festuca rubra. The symbiosis is highly integrated involving systemic growth of the fungus throughout above-ground host parts and vertical transmission from plant to its offspring via host seeds. However...

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Autores principales:	Maria von Cräutlein, Marjo Helander, Helena Korpelainen, Päivi Helena Leinonen, Beatriz R. Vázquez de Aldana, Carolyn Anne Young, Iñigo Zabalgogeazcoa, Kari Saikkonen
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	alkaloid production Epichloë festucae Festuca rubra ergot alkaloid indole-diterpene pyrrolpyrazine Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7a7512cee27146d7a0a1e31a41472bee
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spelling	oai:doaj.org-article:7a7512cee27146d7a0a1e31a41472bee2021-12-03T07:13:33ZGenetic Diversity of the Symbiotic Fungus Epichloë festucae in Naturally Occurring Host Grass Populations1664-302X10.3389/fmicb.2021.756991https://doaj.org/article/7a7512cee27146d7a0a1e31a41472bee2021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.756991/fullhttps://doaj.org/toc/1664-302XEpichloë festucae is a common symbiont of the perennial and widely distributed cool season grass, Festuca rubra. The symbiosis is highly integrated involving systemic growth of the fungus throughout above-ground host parts and vertical transmission from plant to its offspring via host seeds. However, the nature of symbiosis is labile ranging from antagonistic to mutualistic depending on prevailing selection pressures. Both the loss of fungus in the maternal host lineage and horizontal transmission through sexual spores within the host population may partly explain the detected variation in symbiosis in wild grass populations. Epichloë species are commonly considered as pathogens when they produce sexual spores and partly castrate their host plant. This is the pathogenic end of the continuum from antagonistic to mutualistic interactions. Here we examined the population genetic structure of E. festucae to reveal the gene flow, importance of reproduction modes, and alkaloid potential of the symbiotic fungus in Europe. Epichloë-species are highly dependent on the host in survival and reproduction whilst benefits to the host are largely linked to defensive mutualism attributable to fungal-origin bioactive alkaloids that negatively affect vertebrate and/or invertebrate herbivores. We detected decreased genetic diversity in previously glaciated areas compared to non-glaciated regions during the last glacial maximum period and found three major genetic clusters in E. festucae populations: southern, northeastern and northwestern Europe. Sexual reproduction may have a higher role than expected in Spanish E. festucae populations due to the predominance of unique genotypes and presence of both mating types in the region. In contrast, asexual reproduction via host seeds predominates in the Faroe Island and Finland in northern Europe due to the presence of biased mating-type ratios and large dominant genotypes in the E. festucae populations within the region. A substantially larger variation of alkaloid genotypes was observed in the fungal populations than expected, although the variability of the alkaloid genotypes within populations is considerably lower in northern than Spanish populations in southern Europe. E. festucae populations consist of different combinations of alkaloid classes from the gene clusters of ergot alkaloid and indole-terpenes, and from pyrrolopyrazine alkaloid gene. We suggest that the postglacial distribution history of the host grass, prevailing reproduction strategies of E. festucae, and local selection pressures likely explain a large part of the genetic variation observed in fungal populations among geographic regions. The identified alkaloid genotypes can be used by turfgrass breeders to improve resistance against herbivores in red fescue varieties and to develop new sustainable cultivars in Europe.Maria von CräutleinMaria von CräutleinMaria von CräutleinMarjo HelanderHelena KorpelainenPäivi Helena LeinonenPäivi Helena LeinonenBeatriz R. Vázquez de AldanaCarolyn Anne YoungIñigo ZabalgogeazcoaKari SaikkonenKari SaikkonenFrontiers Media S.A.articlealkaloid productionEpichloë festucaeFestuca rubraergot alkaloidindole-diterpenepyrrolpyrazineMicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	alkaloid production Epichloë festucae Festuca rubra ergot alkaloid indole-diterpene pyrrolpyrazine Microbiology QR1-502
spellingShingle	alkaloid production Epichloë festucae Festuca rubra ergot alkaloid indole-diterpene pyrrolpyrazine Microbiology QR1-502 Maria von Cräutlein Maria von Cräutlein Maria von Cräutlein Marjo Helander Helena Korpelainen Päivi Helena Leinonen Päivi Helena Leinonen Beatriz R. Vázquez de Aldana Carolyn Anne Young Iñigo Zabalgogeazcoa Kari Saikkonen Kari Saikkonen Genetic Diversity of the Symbiotic Fungus Epichloë festucae in Naturally Occurring Host Grass Populations
description	Epichloë festucae is a common symbiont of the perennial and widely distributed cool season grass, Festuca rubra. The symbiosis is highly integrated involving systemic growth of the fungus throughout above-ground host parts and vertical transmission from plant to its offspring via host seeds. However, the nature of symbiosis is labile ranging from antagonistic to mutualistic depending on prevailing selection pressures. Both the loss of fungus in the maternal host lineage and horizontal transmission through sexual spores within the host population may partly explain the detected variation in symbiosis in wild grass populations. Epichloë species are commonly considered as pathogens when they produce sexual spores and partly castrate their host plant. This is the pathogenic end of the continuum from antagonistic to mutualistic interactions. Here we examined the population genetic structure of E. festucae to reveal the gene flow, importance of reproduction modes, and alkaloid potential of the symbiotic fungus in Europe. Epichloë-species are highly dependent on the host in survival and reproduction whilst benefits to the host are largely linked to defensive mutualism attributable to fungal-origin bioactive alkaloids that negatively affect vertebrate and/or invertebrate herbivores. We detected decreased genetic diversity in previously glaciated areas compared to non-glaciated regions during the last glacial maximum period and found three major genetic clusters in E. festucae populations: southern, northeastern and northwestern Europe. Sexual reproduction may have a higher role than expected in Spanish E. festucae populations due to the predominance of unique genotypes and presence of both mating types in the region. In contrast, asexual reproduction via host seeds predominates in the Faroe Island and Finland in northern Europe due to the presence of biased mating-type ratios and large dominant genotypes in the E. festucae populations within the region. A substantially larger variation of alkaloid genotypes was observed in the fungal populations than expected, although the variability of the alkaloid genotypes within populations is considerably lower in northern than Spanish populations in southern Europe. E. festucae populations consist of different combinations of alkaloid classes from the gene clusters of ergot alkaloid and indole-terpenes, and from pyrrolopyrazine alkaloid gene. We suggest that the postglacial distribution history of the host grass, prevailing reproduction strategies of E. festucae, and local selection pressures likely explain a large part of the genetic variation observed in fungal populations among geographic regions. The identified alkaloid genotypes can be used by turfgrass breeders to improve resistance against herbivores in red fescue varieties and to develop new sustainable cultivars in Europe.
format	article
author	Maria von Cräutlein Maria von Cräutlein Maria von Cräutlein Marjo Helander Helena Korpelainen Päivi Helena Leinonen Päivi Helena Leinonen Beatriz R. Vázquez de Aldana Carolyn Anne Young Iñigo Zabalgogeazcoa Kari Saikkonen Kari Saikkonen
author_facet	Maria von Cräutlein Maria von Cräutlein Maria von Cräutlein Marjo Helander Helena Korpelainen Päivi Helena Leinonen Päivi Helena Leinonen Beatriz R. Vázquez de Aldana Carolyn Anne Young Iñigo Zabalgogeazcoa Kari Saikkonen Kari Saikkonen
author_sort	Maria von Cräutlein
title	Genetic Diversity of the Symbiotic Fungus Epichloë festucae in Naturally Occurring Host Grass Populations
title_short	Genetic Diversity of the Symbiotic Fungus Epichloë festucae in Naturally Occurring Host Grass Populations
title_full	Genetic Diversity of the Symbiotic Fungus Epichloë festucae in Naturally Occurring Host Grass Populations
title_fullStr	Genetic Diversity of the Symbiotic Fungus Epichloë festucae in Naturally Occurring Host Grass Populations
title_full_unstemmed	Genetic Diversity of the Symbiotic Fungus Epichloë festucae in Naturally Occurring Host Grass Populations
title_sort	genetic diversity of the symbiotic fungus epichloë festucae in naturally occurring host grass populations
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/7a7512cee27146d7a0a1e31a41472bee
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Genetic Diversity of the Symbiotic Fungus Epichloë festucae in Naturally Occurring Host Grass Populations

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