cAMP signalling regulates synchronised growth of symbiotic Epichloë fungi with the host grass Lolium perenne
The seed-transmitted fungal symbiont, Epichloë festucae, colonizes grasses by infecting host tissues as they form on the shoot apical meristem (SAM) of the seedling. How this fungus accommodates the complexities of plant development to successfully colonize the leaves and inflorescences is unclear....
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2016-10-01
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| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01546/full |
| _version_ | 1818517019708882944 |
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| author | Christine Rosalie Voisey Michael Christensen Michael Christensen Linda Joy Johnson Natasha Forester Milan Gagic Gregory T Bryan Wayne Roydon Simpson Damien Fleetwood Stuart Douglas Card John Koolaard Paul Maclean Richard David Johnson |
| author_facet | Christine Rosalie Voisey Michael Christensen Michael Christensen Linda Joy Johnson Natasha Forester Milan Gagic Gregory T Bryan Wayne Roydon Simpson Damien Fleetwood Stuart Douglas Card John Koolaard Paul Maclean Richard David Johnson |
| author_sort | Christine Rosalie Voisey |
| collection | DOAJ |
| description | The seed-transmitted fungal symbiont, Epichloë festucae, colonizes grasses by infecting host tissues as they form on the shoot apical meristem (SAM) of the seedling. How this fungus accommodates the complexities of plant development to successfully colonize the leaves and inflorescences is unclear. Since adenosine 3′, 5′-cyclic monophosphate (cAMP)-dependent signaling is often essential for host colonization by fungal pathogens, we disrupted the cAMP cascade by insertional mutagenesis of the E. festucae adenylate cyclase gene (acyA). Consistent with deletions of this gene in other fungi, acyA mutants had a slow radial growth rate in culture, and hyphae were convoluted and hyper-branched suggesting that fungal apical dominance had been disrupted. Nitro blue tetrazolium (NBT) staining of hyphae showed that cAMP disruption mutants were impaired in their ability to synthesize superoxide, indicating that cAMP signaling regulates accumulation of reactive oxygen species (ROS). Despite significant defects in hyphal growth and ROS production, E. festucae ΔacyA mutants were infectious and capable of forming symbiotic associations with grasses. Plants infected with E. festucae ΔacyA were marginally less robust than the wild-type (WT), however hyphae were hyper-branched, and leaf tissues heavily colonized, indicating that the tight regulation of hyphal growth normally observed in maturing leaves requires functional cAMP signaling. |
| first_indexed | 2024-12-11T00:50:20Z |
| format | Article |
| id | doaj.art-b6ed6dd767984c88951c995206aec768 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-11T00:50:20Z |
| publishDate | 2016-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-b6ed6dd767984c88951c995206aec7682022-12-22T01:26:39ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2016-10-01710.3389/fpls.2016.01546206901cAMP signalling regulates synchronised growth of symbiotic Epichloë fungi with the host grass Lolium perenneChristine Rosalie Voisey0Michael Christensen1Michael Christensen2Linda Joy Johnson3Natasha Forester4Milan Gagic5Gregory T Bryan6Wayne Roydon Simpson7Damien Fleetwood8Stuart Douglas Card9John Koolaard10Paul Maclean11Richard David Johnson12AgResearchAgResearchAgResearchAgResearchAgResearchAgResearchAgResearchAgResearchBiotelliga LtdAgResearchAgResearchAgResearchAgResearchThe seed-transmitted fungal symbiont, Epichloë festucae, colonizes grasses by infecting host tissues as they form on the shoot apical meristem (SAM) of the seedling. How this fungus accommodates the complexities of plant development to successfully colonize the leaves and inflorescences is unclear. Since adenosine 3′, 5′-cyclic monophosphate (cAMP)-dependent signaling is often essential for host colonization by fungal pathogens, we disrupted the cAMP cascade by insertional mutagenesis of the E. festucae adenylate cyclase gene (acyA). Consistent with deletions of this gene in other fungi, acyA mutants had a slow radial growth rate in culture, and hyphae were convoluted and hyper-branched suggesting that fungal apical dominance had been disrupted. Nitro blue tetrazolium (NBT) staining of hyphae showed that cAMP disruption mutants were impaired in their ability to synthesize superoxide, indicating that cAMP signaling regulates accumulation of reactive oxygen species (ROS). Despite significant defects in hyphal growth and ROS production, E. festucae ΔacyA mutants were infectious and capable of forming symbiotic associations with grasses. Plants infected with E. festucae ΔacyA were marginally less robust than the wild-type (WT), however hyphae were hyper-branched, and leaf tissues heavily colonized, indicating that the tight regulation of hyphal growth normally observed in maturing leaves requires functional cAMP signaling.http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01546/fullReactive Oxygen SpeciesSymbiosisLolium perennecAMP signallingHyphal branchingEpichloë festucae |
| spellingShingle | Christine Rosalie Voisey Michael Christensen Michael Christensen Linda Joy Johnson Natasha Forester Milan Gagic Gregory T Bryan Wayne Roydon Simpson Damien Fleetwood Stuart Douglas Card John Koolaard Paul Maclean Richard David Johnson cAMP signalling regulates synchronised growth of symbiotic Epichloë fungi with the host grass Lolium perenne Frontiers in Plant Science Reactive Oxygen Species Symbiosis Lolium perenne cAMP signalling Hyphal branching Epichloë festucae |
| title | cAMP signalling regulates synchronised growth of symbiotic Epichloë fungi with the host grass Lolium perenne |
| title_full | cAMP signalling regulates synchronised growth of symbiotic Epichloë fungi with the host grass Lolium perenne |
| title_fullStr | cAMP signalling regulates synchronised growth of symbiotic Epichloë fungi with the host grass Lolium perenne |
| title_full_unstemmed | cAMP signalling regulates synchronised growth of symbiotic Epichloë fungi with the host grass Lolium perenne |
| title_short | cAMP signalling regulates synchronised growth of symbiotic Epichloë fungi with the host grass Lolium perenne |
| title_sort | camp signalling regulates synchronised growth of symbiotic epichlo 235 fungi with the host grass lolium perenne |
| topic | Reactive Oxygen Species Symbiosis Lolium perenne cAMP signalling Hyphal branching Epichloë festucae |
| url | http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01546/full |
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