GmcA Is a Putative Glucose-Methanol-Choline Oxidoreductase Required for the Induction of Asexual Development in Aspergillus nidulans

Etxebeste, Oier; Herrero-García, Erika; Cortese, Marc S.; Garzia, Aitor; Oiartzabal-Arano, Elixabet; Rı́os, Vivian de los; Ugalde, Unai; Espeso, Eduardo A.

doi:10.1371/journal.pone.0040292

Cited by 28 publications

(22 citation statements)

References 61 publications

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“…The same effect was observed in null mutants of UDA genes such as flbE, flbD, and gmcA (Etxebeste et al 2012). Interestingly, the An4394 transcript was overexpressed in the DbrlA background ( Figure 7A, bottom).…”

Section: Global Analysis Of Flbb Activity In the Regulation Of Genes supporting

confidence: 62%

Beyond Asexual Development: Modifications in the Gene Expression Profile Caused by the Absence of the Aspergillus nidulans Transcription Factor FlbB

et al. 2015

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In the model fungus Aspergillus nidulans, asexual development is induced from vegetative hyphae by a set of early regulators including the bZIP-type transcription factor FlbB. To determine the range of genes under the influence of the transcriptional activity of FlbB and to characterize their role in fungal development, we sequenced and compared the transcriptomes of a DflbB mutant and its isogenic wild-type strain at different developmental stages. Results confirmed the activating role of FlbB on downstream regulators of conidiation such as flbD and brlA. However, FlbB has additional functions beyond the induction of asexual development. Among the changes observed, absence of a functional FlbB caused induction of the dba cluster and synthesis of a secondary metabolite with bactericidal properties. In addition, a new transcriptional target of FlbB was unveiled, urdA, that codes for a putative transcription factor that represses premature sexual development. Taken together, our results indicate that the activators of asexual development simultaneously exert a role on other cellular functions, including an inhibitory effect on the sexual cycle, and reinforce the hypothesis that mutually exclusive metabolic and cellular patterns are associated with different morphogenetic programs.KEYWORDS Aspergillus nidulans; mRNA sequencing; transcriptional regulation; development; secondary metabolite cluster C ELLULAR morphogenesis can be defined as programmed gene expression changes that lead to the development of specialized cell types. Basic eukaryotic morphogenetic mechanisms are commonly studied using fungi as models. Aspergillus nidulans is a nonpathogenic fungus that is phylogenetically related to clinically important species (A. fumigatus) as well as species with economical or industrial value such as A. niger and A. oryzae. In addition, A. nidulans is the main reference organism in basic studies of asexual development (Etxebeste et al. 2010a;Park and Yu 2012). The production of asexual spores (conidia) is induced in nonspecialized cells called vegetative hyphae and involves the biogenesis of a succession of cell types that results in the generation of structures called conidiophores (Mims et al. 1988).A significant number of genes involved in asexual development have been identified and characterized (Etxebeste et al. 2010a;Ni et al. 2010;Park and Yu 2012). Some of them are specific to the morphogenetic process and control the later stages leading to conidia production. brlA, the first development-specific transcription factor; abaA; and wetA constitute the backbone of the central developmental pathway (CDP) and regulate the expression of genes involved in the correct spatiotemporal formation of the conidiophore cell types (Park and Yu 2012).The specialization of vegetative hyphae into asexual reproductive structures is induced by exogenous and endogenous stimuli (Fischer and Kües 2006). This requires the existence of an efficient genetic mechanism to guarantee that these cues are correctly transduced into si...

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Section: Global Analysis Of Flbb Activity In the Regulation Of Genes supporting

confidence: 62%

Beyond Asexual Development: Modifications in the Gene Expression Profile Caused by the Absence of the Aspergillus nidulans Transcription Factor FlbB

et al. 2015

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“…These transporters may aid in regulation of ion and membrane potential homeostasis through their transport of nitrate, which is known to regulate the symbiosis (Vincill et al, 2005). These results indicated that GmcA is involved in a variety of metabolic processes, as has been described in A. niger and E. coli (Etxebeste et al, 2012;Liu et al, 2013).…”

Section: Discussionsupporting

confidence: 58%

A GMC Oxidoreductase GmcA Is Required for Symbiotic Nitrogen Fixation in Rhizobium leguminosarum bv. viciae

Zou

Luo

et al. 2020

Front. Microbiol.

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GmcA is a FAD-containing enzyme belonging to the GMC (glucose-methanol-choline oxidase) family of oxidoreductases. A mutation in the Rhizobium leguminosarum gmcA gene was generated by homologous recombination. The mutation in gmcA did not affect the growth of R. leguminosarum, but it displayed decreased antioxidative capacity at H 2 O 2 conditions higher than 5 mM. The gmcA mutant strain displayed no difference of glutathione reductase activity, but significantly lower level of the glutathione peroxidase activity than the wild type. Although the gmcA mutant was able to induce the formation of nodules, the symbiotic ability was severely impaired, which led to an abnormal nodulation phenotype coupled to a 30% reduction in the nitrogen fixation capacity. The observation on ultrastructure of 4-week pea nodules showed that the mutant bacteroids tended to start senescence earlier and accumulate poly-β-hydroxybutyrate (PHB) granules. In addition, the gmcA mutant was severely impaired in rhizosphere colonization. Real-time quantitative PCR showed that the gmcA gene expression was significantly up-regulated in all the detected stages of nodule development, and statistically significant decreases in the expression of the redoxin genes katG, katE, and ohrB were found in gmcA mutant bacteroids. LC-MS/MS analysis quantitative proteomics techniques were employed to compare differential gmcA mutant root bacteroids in response to the wild type infection. Sixty differentially expressed proteins were identified including 33 up-regulated and 27 down-regulated proteins. By sorting the identified proteins according to metabolic function, 15 proteins were transporter protein, 12 proteins were related to stress response and virulence, and 9 proteins were related to transcription factor activity. Moreover, nine proteins related to amino acid metabolism were over-expressed.

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“…The lower conidiation observed in Δ napA mutants might be related to their lower expression of gmcA gene (AN8547), encoding a putative glucose-methanol-choline oxidoreductase required for early stages of conidiophore development (Etxebeste et al, 2012). The fact that GmcA ortholog AFUA_3G01580 is also induced by H 2 O 2 in an AfYap1-dependent manner in A. fumigatus (Lessing et al, 2007) suggests that gmcA regulation by NapA is conserved, at least in the Aspergilli.…”

Section: Discussionmentioning

confidence: 99%

NapA Mediates a Redox Regulation of the Antioxidant Response, Carbon Utilization and Development in Aspergillus nidulans

Mendoza-Martínez¹,

Lara-Rojas²,

Sánchez³

et al. 2017

Front. Microbiol.

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The redox-regulated transcription factors (TFs) of the bZIP AP1 family, such as yeast Yap1 and fission yeast Pap1, are activated by peroxiredoxin proteins (Prxs) to regulate the antioxidant response. Previously, Aspergillus nidulans mutants lacking the Yap1 ortholog NapA have been characterized as sensitive to H2O2 and menadione. Here we study NapA roles in relation to TFs SrrA and AtfA, also involved in oxidant detoxification, showing that these TFs play different roles in oxidative stress resistance, catalase gene regulation and development, during A. nidulans life cycle. We also uncover novel NapA roles in repression of sexual development, normal conidiation, conidial mRNA accumulation, and carbon utilization. The phenotypic characterization of ΔgpxA, ΔtpxA, and ΔtpxB single, double and triple peroxiredoxin mutants in wild type or ΔnapA backgrounds shows that none of these Prxs is required for NapA function in H2O2 and menadione resistance. However, these Prxs participate in a minor NapA-independent H2O2 resistance pathway and NapA and TpxA appear to regulate conidiation along the same route. Using transcriptomic analysis we show that during conidial development NapA-dependent gene expression pattern is different from canonical oxidative stress patterns. In the course of conidiation, NapA is required for regulation of at least 214 genes, including ethanol utilization genes alcR, alcA and aldA, and large sets of genes encoding proteins involved in transcriptional regulation, drug detoxification, carbohydrate utilization and secondary metabolism, comprising multiple oxidoreductases, membrane transporters and hydrolases. In agreement with this, ΔnapA mutants fail to grow or grow very poorly in ethanol, arabinose or fructose as sole carbon sources. Moreover, we show that NapA nuclear localization is induced not only by oxidative stress but also by growth in ethanol and by carbon starvation. Together with our previous work, these results show that SakA-AtfA, SrrA and NapA oxidative stress-sensing pathways regulate essential aspects of spore physiology (i.e., cell cycle arrest, dormancy, drug production and detoxification, and carbohydrate utilization).

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GmcA Is a Putative Glucose-Methanol-Choline Oxidoreductase Required for the Induction of Asexual Development in Aspergillus nidulans

Cited by 28 publications

References 61 publications

Beyond Asexual Development: Modifications in the Gene Expression Profile Caused by the Absence of the Aspergillus nidulans Transcription Factor FlbB

Beyond Asexual Development: Modifications in the Gene Expression Profile Caused by the Absence of the Aspergillus nidulans Transcription Factor FlbB

A GMC Oxidoreductase GmcA Is Required for Symbiotic Nitrogen Fixation in Rhizobium leguminosarum bv. viciae

NapA Mediates a Redox Regulation of the Antioxidant Response, Carbon Utilization and Development in Aspergillus nidulans

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