Possible Involvement of Pleiomorphic Vacuolar Networks in Nutrient Recycling in Filamentous Fungi

Shoji, Jun‐ya; Arioka, Manabu; Kitamoto, Katsuhiko

doi:10.4161/auto.2695

Cited by 39 publications

(31 citation statements)

References 21 publications

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“…Besides growth, the facility in metabolizing different carbon sources also seems to affect M. perniciosa morphology. Growth in the absence of a carbon source, with non-fermentable carbon sources or with galactose, all representing nutritional limitations in comparison to the addition of GLU, induced the development of branched and thinner mycelia; it also showed the translocation of components between hyphae (Figures 2, 3, and 4), a characteristic already reported for other fungi grown under nutritional limitation (Shoji et al, 2006). This phenotype correlates with a smaller biomass production and, with the exception of galactose, is related to a slower radial growth of mycelia ( Figures 1A,B and 2).…”

Section: Discussionmentioning

confidence: 60%

Carbon source-induced changes in the physiology of the cacao pathogen Moniliophthora perniciosa (Basidiomycetes) affect mycelial morphology and secretion of necrosis-inducing proteins

Alvim¹,

Mattos²,

Pirovani³

et al. 2009

Genet. Mol. Res.

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ABSTRACT. Quantitative and qualitative relationships were found between secreted proteins and their activity, and the hyphal morphology of Moniliophthora perniciosa, the causal agent of witches' broom disease in Theobroma cacao. This fungus was grown on fermentable and non-fermentable carbon sources; significant differences in mycelial morphology were observed and correlated with the carbon source. A biological assay performed with Nicotiana tabacum leaves revealed that the necrosis-related activity of extracellular fungal proteins also differed with carbon source. There were clear differences in the type and quantity of the secreted proteins. In addition, the expression of the cacao molecular chaperone BiP increased after treatment with secreted proteins, suggesting a physiological response to the fungus secretome. We suggest that the carbon source-dependent energy metabolism of M. perniciosa results in physiological alterations in protein expression and secretion; these may affect not only M. perniciosa growth, but also its ability to express pathogenicity proteins.

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Section: Discussionmentioning

confidence: 60%

Carbon source-induced changes in the physiology of the cacao pathogen Moniliophthora perniciosa (Basidiomycetes) affect mycelial morphology and secretion of necrosis-inducing proteins

Alvim¹,

Mattos²,

Pirovani³

et al. 2009

Genet. Mol. Res.

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“…Besides tubular and vesicular vacuoles, filamentous fungi also possess large spherical vacuoles that are mostly static and commonly positioned adjacent to, and on the distal side of, septa (5,8,56). PRO22-GFP was found to be absent from these spherical vacuolar compartments (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Our finding that PRO22 does not localize to the entire vacuolar system of S. macrospora, but specifically to the dynamic tubular and vesicular vacuolar components near growing hyphal tips in the peripheral region of the colony and to vacuoles in ascogonia strongly suggests that the protein has a unique function in these organelles. It has been previously proposed that the different types of vacuoles may play different roles in different regions of the mycelium (56,57).…”

Section: Discussionmentioning

confidence: 99%

A Mutant Defective in Sexual Development Produces Aseptate Ascogonia

et al. 2010

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The transition from the vegetative to the sexual cycle in filamentous ascomycetes is initiated with the formation of ascogonia. Here, we describe a novel type of sterile mutant from Sordaria macrospora with a defect in ascogonial septum formation. This mutant, named pro22, produces only small, defective protoperithecia and carries a point mutation in a gene encoding a protein that is highly conserved throughout eukaryotes. Sequence analyses revealed three putative transmembrane domains and a C-terminal domain of unknown function. Live-cell imaging showed that PRO22 is predominantly localized in the dynamic tubular and vesicular vacuolar network of the peripheral colony region close to growing hyphal tips and in ascogonia; it is absent from the large spherical vacuoles in the vegetative hyphae of the subperipheral region of the colony. This points to a specific role of PRO22 in the tubular and vesicular vacuolar network, and the loss of intercalary septation in ascogonia suggests that PRO22 functions during the initiation of sexual development.The formation of fruiting bodies in filamentous ascomycetes is a process of multicellular differentiation controlled by many developmentally regulated genes. The self-fertile ascomycete Sordaria macrospora represents an excellent model for studying cell differentiation during fungal fruiting body development (reviewed in references 9 and 24).During the life cycle of S. macrospora, a mature haploid ascospore germinates and produces a mycelium composed of multinucleate hyphal compartments. After 2 to 3 days, coiled female reproductive hyphae, called ascogonia, are formed. Each ascogonium develops further into a more-or-less spherical protoperithecium composed of pseudoparenchymatous tissue surrounding the original ascogonium (24, 47). Ascogenous hyphae emerge from the ascogonium inside the protoperithecium. Within the ascogenous hyphae, the nuclei pair up to form the dikaryotic state, even though S. macrospora is selffertile and does not require fertilization with an opposite mating type (11,49). The transition from the spherical protoperithecial to the flask-shaped perithecial stage, is believed to be stimulated by the formation of the dikaryon, although this has not been experimentally verified (24). The dikaryotic state in individual hyphal compartments of the growing ascogenous hyphae is maintained by precisely orchestrated crozier formation from the tip of an ascogenous hypha, fusion of the crozier tip with the penultimate cell of the ascogenous hypha, conjugate mitotic divisions, and highly regulated septation (50, 69). Karyogamy of two nuclei in the penultimate cell results in the formation of a diploid ascus mother cell. The diploid state is very short-lived because the diploid nuclei which are formed immediately undergo meiosis, followed by an extra mitotic division resulting in an ascus containing eight haploid ascospores (11,49). An identical process has been observed in the heterothallic fungus Neurospora crassa, with the exception that cell fusion between opposit...

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“…This foraging-like response is facilitated by the fact that fungal hyphae are divided by perforated septa into multinucleated compartments that permit sharing of nutrients throughout the mycelium (13,47). It has been suggested that vacuole-mediated recycling in the older portions of the mycelium supports the growth of the hyphal tips when exogenous nutrients are scarce (51), but the contribution of autophagy to this process has not been tested directly. Here we demonstrate that Afatg1-dependent autophagy is dispensable for normal radial growth rates on rich or minimal medium but is essential for the hyphal growth that permits colonial expansion under starvation conditions.…”

Section: Discussionmentioning

confidence: 99%

Unexpected Link between Metal Ion Deficiency and Autophagy in Aspergillus fumigatus

et al. 2007

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Autophagy is the major cellular pathway for bulk degradation of cytosolic material and is required to maintain viability under starvation conditions. To determine the contribution of autophagy to starvation stress responses in the filamentous fungus Aspergillus fumigatus, we disrupted the A. fumigatus atg1 gene, encoding a serine/threonine kinase required for autophagy. The ⌬Afatg1 mutant showed abnormal conidiophore development and reduced conidiation, but the defect could be bypassed by increasing the nitrogen content of the medium. When transferred to starvation medium, wild-type hyphae were able to undergo a limited amount of growth, resulting in radial expansion of the colony. In contrast, the ⌬Afatg1 mutant was unable to grow under these conditions. However, supplementation of the medium with metal ions rescued the ability of the ⌬Afatg1 mutant to grow in the absence of a carbon or nitrogen source. Depleting the medium of cations by using EDTA was sufficient to induce autophagy in wild-type A. fumigatus, even in the presence of abundant carbon and nitrogen, and the ⌬Afatg1 mutant was severely growth impaired under these conditions. These findings establish a role for autophagy in the recycling of internal nitrogen sources to support conidiophore development and suggest that autophagy also contributes to the recycling of essential metal ions to sustain hyphal growth when exogenous nutrients are scarce.Nutrient limitation is one of the most significant stresses encountered by microorganisms in nature. Autophagy is a catabolic membrane trafficking system that counters such nutrient stress by initiating a process of limited intracellular digestion to support the organism during periods of reduced nutrient availability (26,32,37,60). The process begins with the formation of isolation membranes within the cytoplasm, whose origin is not entirely clear. These membranes progressively expand, nonselectively encapsulating cytosolic material into a doublemembrane vesicle called the autophagosome. The autophagosome fuses its outer membrane with a vacuole, releasing the autophagic body and its contents into the vacuolar lumen for degradation by resident hydrolases. Autophagy is upregulated in response to starvation stress, resulting in the generation of a pool of recycled molecules that provide the building blocks for continued synthesis of essential components until nutrient conditions improve (26,37,39,60). However, some autophagy remains constitutively active at low levels, even under nutrientreplete conditions, where it serves as a mechanism to remove old or damaged proteins and organelles (17,25,28,46,54). This provides an important form of quality control that combats the toxic accumulation of abnormal cytoplasmic components.The degradative functions of autophagy contribute to several important aspects of cell physiology, including autophagydependent programmed cell death (2, 14), cellular remodeling during development and differentiation (21,36,40,49,57), maintenance of endoplasmic reticulum homeostasis (4, 30, 6...

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Possible Involvement of Pleiomorphic Vacuolar Networks in Nutrient Recycling in Filamentous Fungi

Cited by 39 publications

References 21 publications

Carbon source-induced changes in the physiology of the cacao pathogen Moniliophthora perniciosa (Basidiomycetes) affect mycelial morphology and secretion of necrosis-inducing proteins

Carbon source-induced changes in the physiology of the cacao pathogen Moniliophthora perniciosa (Basidiomycetes) affect mycelial morphology and secretion of necrosis-inducing proteins

A Mutant Defective in Sexual Development Produces Aseptate Ascogonia

Unexpected Link between Metal Ion Deficiency and Autophagy in Aspergillus fumigatus

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