Three α-Subunits of Heterotrimeric G Proteins and an Adenylyl Cyclase Have Distinct Roles in Fruiting Body Development in the Homothallic Fungus <i>Sordaria macrospora</i>

Kamerewerd, Jens; Jansson, Malin; Nowrousian, Minou; Pöggeler, Stefanie; Kück, Ulrich

doi:10.1534/genetics.108.091603

Cited by 38 publications

(29 citation statements)

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“…Cultivation for ascospore germination assays and DNA extraction were performed as described previously (Nowrousian and Cebula 2005;Kamerewerd et al 2008;Teichert et al 2012). For rescue of fertility, strains were inoculated on filter paper covering solid BMM medium.…”

Section: Methodsmentioning

confidence: 99%

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New Insights Into the Roles of NADPH Oxidases in Sexual Development and Ascospore Germination in Sordaria macrospora

et al. 2014

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NADPH oxidase (NOX)-derived reactive oxygen species (ROS) act as signaling determinants that induce different cellular processes. To characterize NOX function during fungal development, we utilized the genetically tractable ascomycete Sordaria macrospora. Genome sequencing of a sterile mutant led us to identify the NADPH oxidase encoding nox1 as a gene required for fruiting body formation, regular hyphal growth, and hyphal fusion. These phenotypes are shared by Δnor1, lacking the NOX regulator NOR1. Further phenotypic analyses revealed a high correlation between increased ROS production and hyphal fusion deficiencies in Δnox1 and other sterile mutants. A genome-wide transcriptional profiling analysis of mycelia and isolated protoperithecia from wild type and Δnox1 revealed that nox1 inactivation affects the expression of genes related to cytoskeleton remodeling, hyphal fusion, metabolism, and mitochondrial respiration. Genetic analysis of Δnox2, lacking the NADPH oxidase 2 gene, Δnor1, and transcription factor deletion mutant Δste12, revealed a strict melanin-dependent ascospore germination defect, indicating a common genetic pathway for these three genes. We report that gsa3, encoding a G-protein a-subunit, and sac1, encoding cAMP-generating adenylate cyclase, act in a separate pathway during the germination process. The finding that cAMP inhibits ascospore germination in a melanin-dependent manner supports a model in which cAMP inhibits NOX2 activity, thus suggesting a link between both pathways. Our results expand the current knowledge on the role of NOX enzymes in fungal development and provide a frame to define upstream and downstream components of the NOX signaling pathways in fungi. D URING sexual reproduction, filamentous fungi generate complex fruiting bodies that contain and protect meiosporangia. We used the ascomycetous model fungus Sordaria macrospora to identify genes directly involved in fruiting body development (Kück et al. 2009;Engh et al. 2010;Kück et al. 2009). Due to its homothallic life style, S. macrospora is able to complete the sexual life cycle without the mating of strains with opposite sex, and therefore, fruiting body-deficient mutants can be recognized directly without the need for crossing experiments. In earlier work, we generated sterile mutants showing a developmental block after formation of young fruiting bodies (protoperithecia), but being unable to generate mature perithecia, and referred to these mutants as pro. Recently, we have applied next-generation genome re-sequencing to identify the genes affected in some of these mutants . Based on this approach, we now have characterized mutant pro32 and show that it carries a mutation in the nox1 gene encoding NAPDH oxidase 1 (NOX1).NADPH oxidase (NOX) enzymes are transmembrane proteins that are highly conserved among eukaryotes and produce reactive oxygen species (ROS) through the oxidation of NADPH (Lambeth 2004;Kawahara and Lambeth 2007). ROS have long been recognized as damaging agents due to uncontrolled oxidizing re...

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Section: Methodsmentioning

confidence: 99%

“…None of the 4000 ascospores analyzed showed germination. Thus, the germination-related phenotypes of Δnox2 and Δgsa3 (Kamerewerd et al 2008) are exacerbated in the Δgsa3Δnox2/fus mutant. This result clearly shows that NOX2 and GSA3 have a different impact on ascospore germination.…”

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New Insights Into the Roles of NADPH Oxidases in Sexual Development and Ascospore Germination in Sordaria macrospora

et al. 2014

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“…Indeed, two main upstream signalling regulators of adenylyl cyclase, guanine nucleotide-binding protein (G proteins) beta subunit-like protein and GTP-binding protein Ran, increased in the fruiting body of C. sinensis (Table 2). G proteins can interact with adenylyl cyclases and catalyse the formation of cAMP (D’Souza and Heitman, 2001; Kamerewerd et al 2008). GTP-binding protein Ran belongs to the superfamily of Ras proteins and is crucial regulator of adenylyl cyclase (Schlenstedt et al 1997; Seewald et al 2003).…”

Section: Resultsmentioning

confidence: 99%

Potential molecular mechanisms for fruiting body formation of Cordyceps illustrated in the case ofCordyceps sinensis

et al. 2017

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The fruiting body formation mechanisms of Cordyceps sinensis are still unclear. To explore the mechanisms, proteins potentially related to the fruiting body formation, proteins from fruiting bodies, and mycelia of Cordyceps species were assessed by using two-dimensional fluorescence difference gel electrophoresis, and the differential expression proteins were identified by matrix-assisted laser desorption/ionisation tandem time of flight mass spectrometry. The results showed that 198 differential expression proteins (252 protein spots) were identified during the fruiting body formation of Cordyceps species, and 24 of them involved in fruiting body development in both C. sinensis and other microorganisms. Especially, enolase and malate dehydrogenase were first found to play an important role in fruiting body development in macro-fungus. The results implied that cAMP signal pathway involved in fruiting body development of C. sinensis, meanwhile glycometabolism, protein metabolism, energy metabolism, and cell reconstruction were more active during fruiting body development. It has become evident that fruiting body formation of C. sinensis is a highly complex differentiation process and requires precise integration of a number of fundamental biological processes. Although the fruiting body formation mechanisms for all these activities remain to be further elucidated, the possible mechanism provides insights into the culture of C. sinensis.

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“…This mutant displays an even more obvious delay in fruiting body development than the Dcas2 single mutant and is completely impaired in the production of mature ascospores (Elleuche & Pöggeler, 2009b). Interestingly, deletion of the S. macrospora adenylyl cyclase gene sac1 causes a phenotype comparable to the Dcas2 mutant (Kamerewerd et al, 2008). The Dsac1 deletion strain is impaired in vegetative growth and ascospore germination as well as in the production of fruiting bodies.…”

Section: Cas1 and Cas2 Are Involved In Sordaria Macrospora Fruiting Bmentioning

confidence: 99%

“…While growth defects and fruiting body development are restored by the addition of cAMP to the medium, the germination defect cannot be complemented by the supply of cAMP. Furthermore, SAC1 was shown to be genetically linked to G-protein signalling (Kamerewerd et al, 2008).…”

Section: Cas1 and Cas2 Are Involved In Sordaria Macrospora Fruiting Bmentioning

confidence: 99%

Carbonic anhydrases in fungi

2010

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Carbonic anhydrases (CAs) are metalloenzymes that catalyse the interconversion of carbon dioxide and bicarbonate with high efficiency. This reaction is fundamental to biological processes such as respiration, photosynthesis, pH homeostasis, CO2 transport and electrolyte secretion. CAs are distributed among all three domains of life, and are currently divided into five evolutionarily unrelated classes (α, β, γ, δ and ζ). Fungal CAs have only recently been identified and characterized in detail. While Saccharomyces cerevisiae and Candida albicans each have only one β-CA, multiple copies of β-CA- and α-CA-encoding genes are found in other fungi. Recent work demonstrates that CAs play an important role in the CO2-sensing system of fungal pathogens and in the regulation of sexual development. This review focuses on CA functions in S. cerevisiae, the fungal pathogens C. albicans and Cryptococcus neoformans, and the filamentous ascomycete Sordaria macrospora.

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Three α-Subunits of Heterotrimeric G Proteins and an Adenylyl Cyclase Have Distinct Roles in Fruiting Body Development in the Homothallic Fungus Sordaria macrospora

Cited by 38 publications

References 71 publications

New Insights Into the Roles of NADPH Oxidases in Sexual Development and Ascospore Germination in Sordaria macrospora

New Insights Into the Roles of NADPH Oxidases in Sexual Development and Ascospore Germination in Sordaria macrospora

Potential molecular mechanisms for fruiting body formation of Cordyceps illustrated in the case ofCordyceps sinensis

Carbonic anhydrases in fungi

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