Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves

Christensen, Michael J.; Bennett, Raymond J.; Ansari, H. A.; Koga, Hironori; Johnson, Richard D.; Bryan, Gregory T.; Simpson, Wayne R.; Koolaard, J.; Nickless, Elizabeth; Voisey, Christine R.

doi:10.1016/j.fgb.2007.07.013

Cited by 228 publications

(165 citation statements)

References 34 publications

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“…The growth of this fungus within the leaves is tightly regulated, with usually just a single hypha found between adjacent columns of plant cells. Hyphae that colonize the leaves are firmly attached to the plant cells and extend by intercalary division and extension, a mechanism of growth that synchronizes hyphal growth with plant leaf growth (38). Using both forward and reverse genetic strategies, we previously identified genes crucial for establishment and maintenance of this symbiosis, including genes encoding components of the NADPH oxidase and mitogen-activated protein kinase (MAPK) signaling complexes (15,(39)(40)(41)(42).…”

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confidence: 99%

Redox Regulation of an AP-1-Like Transcription Factor, YapA, in the Fungal Symbiont Epichloë festucae

Cartwright

Scott

2013

Eukaryot Cell

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One of the central regulators of oxidative stress in Saccharomyces cerevisiae is Yap1, a bZIP transcription factor of the AP-1 family. In unstressed cells, Yap1 is reduced and cytoplasmic, but in response to oxidative stress, it becomes oxidized and accumulates in the nucleus. To date, there have been no reports on the role of AP-1-like transcription factors in symbiotic fungi. An ortholog of Yap1, named YapA, was identified in the genome of the grass symbiont Epichloë festucae and shown to complement an S. cerevisiae ⌬yap1 mutant. Hyphae of the E. festucae ⌬yapA strain were sensitive to menadione and diamide but resistant to H 2 O 2 , KO 2 , and tert-butyl hydroperoxide (t-BOOH). In contrast, conidia of the ⌬yapA strain were very sensitive to H 2 O 2 and failed to germinate. Using a PcatA-eGFP degron-tagged reporter, YapA was shown to be required for expression of a spore-specific catalase gene, catA. Although YapA-EGFP localized to the nucleus in response to host reactive oxygen species during seedling infection, there was no difference in whole-plant and cellular phenotypes of plants infected with the ⌬yapA strain compared to the wild-type strain. Homologs of the S. cerevisiae and Schizosaccharomyces pombe redox-sensing proteins (Gpx3 and Tpx1, respectively) did not act as redox sensors for YapA in E. festucae. In response to oxidative stress, YapA-EGFP localized to the nuclei of E. festucae ⌬gpxC, ⌬tpxA, and ⌬gpxC ⌬tpxA cells to the same degree as that in wild-type cells. These results show that E. festucae has a robust system for countering oxidative stress in culture and in planta but that Gpx3-or Tpx1-like thiol peroxidases are dispensable for activation of YapA.

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confidence: 99%

Redox Regulation of an AP-1-Like Transcription Factor, YapA, in the Fungal Symbiont Epichloë festucae

Cartwright

Scott

2013

Eukaryot Cell

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“…In epichloë endophyte-grass associations, hyphae display a highly restricted growth pattern, systemically colonizing all aerial host tissues but remaining within host intercellular spaces, aligned parallel to the leaf axis and seldom branching (Christensen et al, 2002(Christensen et al, , 2008. Hyphal growth is closely coordinated with host growth, such that hyphae only grow during periods of host leaf growth but remain metabolically active throughout the life of the host (Tan et al, 1997;Christensen et al, 2002Christensen et al, , 2008.…”

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confidence: 99%

“…Hyphal growth is closely coordinated with host growth, such that hyphae only grow during periods of host leaf growth but remain metabolically active throughout the life of the host (Tan et al, 1997;Christensen et al, 2002Christensen et al, , 2008. This highly regulated control of endophyte growth within the grass is indicative of signaling between host and symbiont.…”

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Disruption of Signaling in a Fungal-Grass Symbiosis Leads to Pathogenesis

et al. 2010

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Symbiotic associations between plants and fungi are a dominant feature of many terrestrial ecosystems, yet relatively little is known about the signaling, and associated transcriptome profiles, that define the symbiotic metabolic state. Using the Epichloë festucae-perennial ryegrass (Lolium perenne) association as a model symbiotic experimental system, we show an essential role for the fungal stress-activated mitogen-activated protein kinase (sakA) in the establishment and maintenance of this mutualistic interaction. Deletion of sakA switches the fungal interaction with the host from mutualistic to pathogenic. Infected plants exhibit loss of apical dominance, premature senescence, and dramatic changes in development, including the formation of bulb-like structures at the base of tillers that lack anthocyanin pigmentation. A comparison of the transcriptome of wild-type and sakA associations using high-throughput mRNA sequencing reveals dramatic changes in fungal gene expression consistent with the transition from restricted to proliferative growth, including a down-regulation of several clusters of secondary metabolite genes and up-regulation of a large set of genes that encode hydrolytic enzymes and transporters. Analysis of the plant transcriptome reveals up-regulation of host genes involved in pathogen defense and transposon activation as well as dramatic changes in anthocyanin and hormone biosynthetic/responsive gene expression. These results highlight the fine balance between mutualism and antagonism in a plant-fungal interaction and the power of deep mRNA sequencing to identify candidate sets of genes underlying the symbiosis.

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“…Recently, associations of grass plants with fungal endophytes belonging to the Clavicipitaceae family and residing in aboveground plant parts, have become the subject of detailed ecological studies (Clay et al, 2005;Rudgers et al, 2005;Finkes et al, 2006;Meister et al, 2006). These fungi occur in 20% to 30% of all grass species (Leuchtmann, 1993) with their hyphae growing in the apoplastic space without penetrating into plant cells and generally causing no visible symptoms of infection (Christensen et al, 2008). The most commonly studied associations are Neotyphodium lolii-Lolium perenne in Australasia and Neotyphodium coenophialum-Lolium arundinaceum in North America (Christensen et al, 1993) because these are of particular importance to agricultural pastoral systems.…”

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Metabolic Profiles ofLolium perenneAre Differentially Affected by Nitrogen Supply, Carbohydrate Content, and Fungal Endophyte Infection

et al. 2008

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Lolium perenne cultivars differing in their capacity to accumulate water soluble carbohydrates (WSCs) were infected with three strains of fungal Neotyphodium lolii endophytes or left uninfected. The endophyte strains differed in their alkaloid profiles. Plants were grown at two different levels of nitrogen (N) supply in a controlled environment. Metabolic profiles of blades were analyzed using a variety of analytical methods. A total of 66 response variables were subjected to a principle components analysis and factor rotation. The first three rotated factors (46% of the total variance) were subsequently analyzed by analysis of variance. At high N supply nitrogenous compounds, organic acids and lipids were increased; WSCs, chlorogenic acid (CGA), and fibers were decreased. The high-sugar cultivar 'AberDove' had reduced levels of nitrate, most minor amino acids, sulfur, and fibers compared to the control cultivar 'Fennema', whereas WSCs, CGA, and methionine were increased. In plants infected with endophytes, nitrate, several amino acids, and, magnesium were decreased; WSCs, lipids, some organic acids, and CGA were increased. Regrowth of blades was stimulated at high N, and there was a significant endophyte 3 cultivar interaction on regrowth. Mannitol, a fungal specific sugar alcohol, was significantly correlated with fungal biomass. Our findings suggest that effects of endophytes on metabolic profiles of L. perenne can be considerable, depending on host plant characteristics and nutrient supply, and we propose that a shift in carbon/N ratios and in secondary metabolite production as seen in our study is likely to have impacts on herbivore responses.

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Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves

Cited by 228 publications

References 34 publications

Redox Regulation of an AP-1-Like Transcription Factor, YapA, in the Fungal Symbiont Epichloë festucae

Redox Regulation of an AP-1-Like Transcription Factor, YapA, in the Fungal Symbiont Epichloë festucae

Disruption of Signaling in a Fungal-Grass Symbiosis Leads to Pathogenesis

Metabolic Profiles ofLolium perenneAre Differentially Affected by Nitrogen Supply, Carbohydrate Content, and Fungal Endophyte Infection

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