cAMP Signaling Regulates Synchronised Growth of Symbiotic Epichloë Fungi with the Host Grass Lolium perenne

Voisey, Christine R.; Christensen, Merrill J.; Johnson, Linda J.; Forester, Natasha T.; Gagic, Milan; Bryan, Gregory T.; Simpson, Wayne R.; Fleetwood, Damien J.; Card, Stuart D.; Koolaard, J.; Maclean, Paul; Johnson, Richard D.

doi:10.3389/fpls.2016.01546

Cited by 19 publications

(13 citation statements)

References 85 publications

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“…Indeed, all fusion‐negative E. festucae strains obtained to date have a stunted host phenotype (Scott, Green, & Berry, ). However, given E. festucae mutants in cAMP/PKA signaling (Voisey et al, ), apoplastic iron homestasis (Johnson et al, ), and chromatin regulation (Chujo et al, ), exhibit a proliferative growth phenotype in planta but are not defective in cell fusion, an alternative more general hypothesis is needed to explain these results. One possibility is alkalinization of the apoplast (Scott et al, ); a change that activates signaling through the PacC‐mediated pH responsive and MAP kinase pathways, triggering invasive growth (Fernandes, Segorbe, Prusky, & Pietro, ).…”

Section: Discussionmentioning

confidence: 99%

Phosphatidic acid produced by phospholipase D is required for hyphal cell‐cell fusion and fungal‐plant symbiosis

Hassing

Eaton

Winter

et al. 2020

Molecular Microbiology

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Although lipid signaling has been shown to serve crucial roles in mammals and plants, little is known about this process in filamentous fungi. Here we analyze the contribution of phospholipase D (PLD) and its product phosphatidic acid (PA) in hyphal morphogenesis and growth of Epichloë festucae and Neurospora crassa, and in the establishment of a symbiotic interaction between E. festucae and Lolium perenne. Growth of E. festucae and N. crassa PLD deletion strains in axenic culture, and for E. festucae in association with L. perenne, were analyzed by light‐, confocal‐ and electron microscopy. Changes in PA distribution were analyzed in E. festucae using a PA biosensor and the impact of these changes on the endocytic recycling and superoxide production investigated. We found that E. festucae PldB, and the N. crassa ortholog, PLA‐7, are required for polarized growth and cell fusion and contribute to ascospore development, whereas PldA/PLA‐8 are dispensable for these functions. Exogenous addition of PA rescues the cell‐fusion phenotype in E. festucae. PldB is also crucial for E. festucae to establish a symbiotic association with L. perenne. This study identifies a new component of the cell‐cell communication and cell fusion signaling network for hyphal morphogenesis and growth of filamentous fungi.

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Section: Discussionmentioning

confidence: 99%

Phosphatidic acid produced by phospholipase D is required for hyphal cell‐cell fusion and fungal‐plant symbiosis

Hassing

Eaton

Winter

et al. 2020

Molecular Microbiology

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“…The combination of both forward and reverse genetics studies in Epichloë festucae have identified key signaling pathways for the symbiotic interaction with the grass host, Lolium perenne. These include fungal cell wall integrity [36,37], pheromone response/invasive growth [38], and stress-activated [39] mitogen-activated protein kinase (MAPK) pathways, cAMP [40], calcineurin [29], pH [31], light [41,42], reactive oxygen species (ROS) [43][44][45] and lipid [46] signalling pathways. These genetic analyses uncovered host interaction phenotypes ranging from a mild alteration in the host tiller morphology to severe stunting of tiller growth.…”

Section: Discussionmentioning

confidence: 99%

Host infection by the grass-symbiotic fungusEpichloë festucaerequires catalytically active H3K9 and H3K36 methyltransferases

Lukito

Lee²,

Noorifar³

et al. 2020

Preprint

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Recent studies have identified key genes in Epichloë festucae that control the symbiotic interaction of this filamentous fungus with its grass host. Here we report on the identification of specific fungal genes that determine its ability to infect and colonize the host. Deletion of setB, which encodes a homolog of the H3K36 histone methyltransferase Set2/KMT3, specifically reduced histone H3K36 trimethylation and led to severe defects in colony growth and hyphal development. The E. festucae ΔclrD mutant, which lacks the gene encoding the homolog of the H3K9 methyltransferase KMT1, displays similar developmental defects. Both mutants are completely defective in their ability to infect the host grass, and mutational studies of key residues in the catalytic SET domains from these proteins show that these phenotypes are dependent on the methyltransferase activities of SetB and ClrD. A comparison of the differences in the host transcriptome between seedlings inoculated with wild-type versus mutants suggests that the inability of these mutants to infect the host was not due to an aberrant host defense response. Co-inoculation of either ΔsetB or ΔclrD with the wild-type strain enables these mutants to colonize the host. However, successful colonization by the mutants resulted in death or stunting of the host plant. Transcriptome analysis at the early infection stage identified four fungal candidate genes, three of which encode small-secreted proteins, that are differentially regulated in these mutants compared to wild-type. Deletion of crbA, which encodes a putative carbohydrate binding protein, resulted in significantly reduced host infection rates by E. festucae.Author SummaryThe filamentous fungus Epichloë festucae is an endophyte that forms highly regulated symbiotic interactions with the perennial ryegrass. Proper maintenance of such interactions is known to involve several signalling pathways, but much less is understood about the infection capability of this fungus in the host. In this study, we uncovered two epigenetic marks and their respective histone methyltransferases that are required for E. festucae to infect perennial ryegrass. Null mutants of the histone H3 lysine 9 and lysine 36 methyltransferases are completely defective in colonizing the host intercellular space, and these defects are dependent on the methyltransferase activities of these enzymes. Importantly, we observed no evidence for increased host defense response to these mutants that can account for their non-infection. Rather, these infection defects can be rescued by the wild-type strain in co-inoculation experiments, suggesting that failure of the mutants to infect is due to altered expression of genes encoding infection factors that are under the control of the above epigenetic marks that can be supplied by the wild-type strain. Among genes differentially expressed in the mutants at the early infection stage is a putative small-secreted protein with a carbohydrate binding function, which deletion in E. festucae severely reduced infection efficiency.

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“…Although ROS play a major role in regulating E. festucae growth in planta , the NoxA and NoxB complexes are not the only signalling pathways required for controlling the establishment and maintenance of a mutualistic symbiotic association (Scott et al , ). A siderophore for maintaining iron homeostasis (Johnson et al , ), the transcription factor ProA (Green et al , ; Tanaka et al , ), the stress‐activated and cell wall integrity mitogen‐activated protein kinase (MAPK) signalling pathways (Becker et al , ; Eaton et al , ), the STRIPAK complex (Green et al , ), cAMP/PKA (Voisey et al , ) and calcineurin (Mitic et al , ) are all required for maintaining the symbiosis and cause similar host‐association defects when disrupted. Given the similarities between mutant phenotypes, the molecular mechanisms which facilitate gene regulation and cross talk between the Nox complex components and the different signalling pathways in E. festucae –host associations are of considerable interest and still relatively poorly described.…”

Section: Discussionmentioning

confidence: 99%

A homologue of the fungal tetraspanin Pls1 is required for Epichloë festucae expressorium formation and establishment of a mutualistic interaction with Lolium perenne

Green

Eaton

Savoian

et al. 2019

Molecular Plant Pathology

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Summary Epichloë festucae is an endophytic fungus that forms a mutualistic symbiotic association with the grass host Lolium perenne . Endophytic hyphae exit the host by an appressorium‐like structure known as an expressorium. In plant‐pathogenic fungi, the tetraspanin Pls1 and the NADPH oxidase component Nox2 are required for appressorium development. Previously we showed that the homologue of Nox2, NoxB, is required for E. festucae expressorium development and establishment of a mutualistic symbiotic interaction with the grass host. Here we used a reverse genetics approach to functionally characterize the role of the E. festucae homologue of Pls1, PlsA. The morphology and growth of Δ plsA in axenic culture was comparable to wild‐type. The tiller length of plants infected with Δ plsA was significantly reduced. Hyphae of Δ plsA had a proliferative pattern of growth within the leaves of L. perenne with increased colonization of the intercellular spaces and the vascular bundles. The Δ plsA mutant was also defective in expressorium development although the phenotype was not as severe as for Δ noxB , highlighting potentially distinct roles for PlsA and NoxB in signalling through the NoxB complex. Hyphae of Δ plsA proliferate below the cuticle surface but still occasionally form an expressorium‐like structure that enables the mutant hyphae to exit the leaf to grow on the surface. These expressoria still form a septin ring‐like structure at the point of cuticle exit as found in the wild‐type strain. These results establish that E. festucae PlsA has an important, but distinct, role to NoxB in expressorium development and plant symbiosis.

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cAMP Signaling Regulates Synchronised Growth of Symbiotic Epichloë Fungi with the Host Grass Lolium perenne

Cited by 19 publications

References 85 publications

Phosphatidic acid produced by phospholipase D is required for hyphal cell‐cell fusion and fungal‐plant symbiosis

Phosphatidic acid produced by phospholipase D is required for hyphal cell‐cell fusion and fungal‐plant symbiosis

Host infection by the grass-symbiotic fungusEpichloë festucaerequires catalytically active H3K9 and H3K36 methyltransferases

A homologue of the fungal tetraspanin Pls1 is required for Epichloë festucae expressorium formation and establishment of a mutualistic interaction with Lolium perenne

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