Molecular and cellular analysis of the pH response transcription factor PacC in the fungal symbiont Epichloë festucae

Lukito, Yonathan; Chujo, Takeshi; Scott, Barry

doi:10.1016/j.fgb.2015.10.008

Cited by 17 publications

(19 citation statements)

References 75 publications

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“…The role of PacC in mutualistic interactions with plants has only been previously studied during symbiosis of the endophyte Epichloë festucae with Lolium perenne (Lukito et al, ). In this case, deletion of pacC resulted in an increased sensitivity of the mutant to salt‐stress but, surprisingly, did not affect the ability of the mutant to grow under alkaline pH conditions.…”

Section: Discussionmentioning

confidence: 99%

The endophyte Serendipita indica reduces the sodium content of Arabidopsis plants exposed to salt stress: fungal ENA ATPases are expressed and regulated at high pH and during plant co‐cultivation in salinity

Lanza

Haro

Conchillo

et al. 2019

Environmental Microbiology

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Summary Serendipita indica (formerly Piriformospora indica) is an endophytic fungus that colonizes plant roots producing a beneficial effect on plant growth and development under optimal and suboptimal conditions provoked by any biotic or abiotic stress, such as salt stress. Salinity induces osmotic and ionic imbalances in plants, mainly by altering the Na+ and K+ contents. However, the mechanism by which Serendipita improves plant growth has yet to be elucidated. Previous works suggest that this fungus improves the plant osmotic state but not much is known about whether it participates in readjustment of the ionic imbalance in plants. Here, we report that co‐cultivation with Serendipita reduces the Na+ content of Arabidopsis plants under saline conditions. Additionally, we describe the functional characterization of the two Serendipita ENA ATPases, which are homologous to the main proteins involved in the salt tolerance of other fungi. Their heterologous expression in salt‐sensitive yeast mutants shows that SiENA1 is involved in Na+ and K+ efflux, while SiENA5 seems to only be involved in Na+ detoxification. Both are induced and might have a relevant function at alkaline pH, condition in which there are few chlamydospores in the mycelium, as well as during co‐cultivation with plants exposed to saline conditions.

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Section: Discussionmentioning

confidence: 99%

The endophyte Serendipita indica reduces the sodium content of Arabidopsis plants exposed to salt stress: fungal ENA ATPases are expressed and regulated at high pH and during plant co‐cultivation in salinity

Lanza

Haro

Conchillo

et al. 2019

Environmental Microbiology

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“…How Epichloë colonization processes are synchronized with host development is likely mediated through hyphal sensing of changes in host development that induce corresponding changes in fungal development. E. festucae genes in the stress-activated mitogen-activated protein kinase ( sakA ) (Eaton et al, 2010), pH-sensing ( pacC ) (Lukito et al, 2015) and striatin-interacting phosphatase and kinase complex ( mobC ) (Green et al, 2016) are required for regulation of hyphal growth in L. perenne , and their deletion induces aberrant hyphal distribution in plants and alters host growth and development. Production of reactive oxygen species (ROS) by E. festucae in culture and in planta is also vital for establishment of normal symbiotic associations between these organisms.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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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.

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“…The remaining plants, which did not test positive for eGFP presence in the immunoblot, showed a range of host interaction phenotypes from severe stunting to normal growth (S7A and S7C Fig). To test the hypothesis that the stunted plants contained more mutant hyphae compared to the non-stunted plants, we isolated gDNA from these plants and performed qPCR analysis to measure the relative abundance of eGFP (marker) to pacC (control), a single-copy gene in E. festucae [31] In the ΔsetB/eGFP co-inoculated plants, we detected the eGFP gene in four out of five stunted plants (80%), and in one of the six non-stunted plants (17%) (S7B Fig). In the ΔclrD/eGFP co-inoculated plants, we detected the eGFP gene in 11 out of the 14 stunted plants (79%), and in two of the seven non-stunted plants (29%) (S7D Fig).…”

Section: δClrd and δSetb Are Able To Infect L Perenne If Co-inoculatmentioning

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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Molecular and cellular analysis of the pH response transcription factor PacC in the fungal symbiont Epichloë festucae

Cited by 17 publications

References 75 publications

The endophyte Serendipita indica reduces the sodium content of Arabidopsis plants exposed to salt stress: fungal ENA ATPases are expressed and regulated at high pH and during plant co‐cultivation in salinity

The endophyte Serendipita indica reduces the sodium content of Arabidopsis plants exposed to salt stress: fungal ENA ATPases are expressed and regulated at high pH and during plant co‐cultivation in salinity

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

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

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