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

Eaton, Carla J.; Cox, Murray P.; Ambrose, Barbara A.; Becker, Matthias; Hesse, Uljana; Schardl, Christopher L.; Scott, Barry

doi:10.1104/pp.110.158451

Cited by 118 publications

(125 citation statements)

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“…While infection of L. perenne with the E. festucae ⌬sakA mutant results in a defective symbiotic interaction phenotype (42), yapA mutants are able to infect and colonize L. perenne seedlings as effectively as the wild type and give rise to mature plants with a phenotype similar to that with the wild type. These results contrast with the reduced virulence observed for AP-1 mutants of the biotrophic fungal pathogens U. maydis and M. oryzae, because of their sensitivity to the host oxidative burst (7,8).…”

Section: Discussionmentioning

confidence: 99%

“…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%

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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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Section: Discussionmentioning

confidence: 99%

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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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“…Samples of fresh tissue were fixed using formaldehyde/glacial acetic acid/ethanol/distilled water (FAA 2:1:10:7 by volume) overnight at 4 8C, and dehydrated using a graded ethanol series (Eaton et al 2010). Tissues were then prepared for wax infiltration through a graded series of ethanol/ Histoclear TM (National Diagnostics, Atlanta, GA, USA).…”

Section: Anatomy and Macroscopic Observationsmentioning

confidence: 99%

Anatomical investigations determining the origin of crown buds on the transition zone of gentians

Samarakoon

Funnell

Woolley

et al. 2013

New Zealand Journal of Botany

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Gentians are herbaceous perennials of ornamental and medicinal value, which utilize preformed crown buds as part of the perennating structure. Understanding the morphology and associated development of these crown buds is required if manipulation of bud initiation, emergence and development are to be achieved. The point of origin of crown buds, or whether crown buds originate from axillary or adventitious meristems, has not previously been published. In the current study, therefore, anatomical features of the shoot/stem, storage root, transition zone between shoot and root, axillary buds and crown bud clusters, were examined using light microscopy. In seedlings of Gentiana lutea, G. straminea, G. triflora and G. scabra, the transition zone was determined to be the area of initiation of crown buds, which differed morphologically in vascular arrangement from both the true shoot/stem and storage root. Crown buds that first developed on the transition zone were considered to be adventitious in origin.

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“…17 Deletion of E. festucae sakA induces a switch from a mutualistic to an antagonistic interaction with the host; infected plants exhibit dramatic changes in development, stunted growth and premature senescence. To determine the molecular basis of these changes, we undertook a high throughput RNA sequencing survey of gene expression in both the fungus and its plant host.…”

Section: Dissecting Symbiosismentioning

confidence: 99%

Exploring molecular signaling in plant-fungal symbioses using high throughput RNA sequencing

Cox

Eaton

Scott

2010

Plant Signaling & Behavior

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Plant-fungal associations play an important role in terrestrial ecosystems. These interactions range from detrimental (i.e., antagonistic) associations to mutualistic (i.e., beneficial) associations. Plant-fungal signaling plays an important role across this interaction continuum. In antagonistic associations, fungi attempt to circumvent host defense responses, whereas in mutualistic states, both host and fungus must constantly communicate to maintain the tightly balanced symbiosis. Although this inter-species signaling is a vital function in many ecosystems, little is known about how it is controlled at the molecular level.Studying cross-species signaling has traditionally proven difficult. The communication process is both spatially and temporally dynamic, and involves interactions between two very different and very complex biological systems. A wide range of approaches has been applied to understanding this signaling. One such technique is suppression subtractive hybridization (SSH), Plant-fungal symbioses are a common feature in nature. They vary from pathogenic interactions, where fungi subvert plant resources for their own use, to mutualistic associations, where both fungus and host benefit from the interaction. Although the ecological importance of plant-fungal symbioses has long been recognized and the biology of several key associations are now well studied, new technologies have the potential to allow fresh insight into the molecular basis of plant-fungal interactions. One such technique, high throughput RNA sequencing, has recently been used to explore the molecular basis of cross-species communications. Here, we give a brief overview of this emerging technology, and present a general guide for employing the methodology to dissect plant-fungal symbiosis.

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

Cited by 118 publications

References 55 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

Anatomical investigations determining the origin of crown buds on the transition zone of gentians

Exploring molecular signaling in plant-fungal symbioses using high throughput RNA sequencing

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