Sorbic acid stress activates the Candida glabrata high osmolarity glycerol MAP kinase pathway
Open accessAbstract
Weak organic acids such as sorbic acid are important food preservatives and powerful fungistatic agents. These compounds accumulate in the cytosol and disturb the cellular pH and energy homeostasis. Candida glabrata is in many aspects similar to Saccharomyces cerevisiae. However, with regard to confrontation to sorbic acid, two of the principal response pathways behave differently in C. glabrata. In yeast, sorbic acid stress causes activation of many genes via the transcription factors Msn2 and Msn4. The C. glabrata homologs CgMsn2 and CgMsn4 are apparently not activated by sorbic acid. In contrast, in C. glabrata the high osmolarity glycerol (HOG) pathway is activated by sorbic acid. Here we show that the MAP kinase of the HOG pathway, CgHog1, becomes phosphorylated and has a function for weak acid stress resistance. Transcript profiling of weak acid treated C. glabrata cells suggests a broad and very similar response pattern of cells lacking CgHog1 compared to wild type which is over lapping with but distinct from S. cerevisiae. The PDR12 gene was the highest induced gene in both species and it required CgHog1 for full expression. Our results support flexibility of the response cues for general stress signaling pathways, even between closely related yeasts, and functional extension of a specific response pathway.
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Written from the paper’s full text.
TL;DR
Sorbic acid stress activates the Candida glabrata HOG MAP kinase pathway, causing CgHog1 phosphorylation and nuclear accumulation, and CgHog1 is required for sorbic acid resistance. Transcript profiling shows a broad sorbate response that is similar between wild type and hog1Δ but distinct from Saccharomyces cerevisiae.
Key findings
- CgHog1 becomes phosphorylated and accumulates in the nucleus upon sorbic acid exposure; the CgHog1-GFP fusion complemented osmotic and sorbic acid growth defects of the BG14hog1Δ strain.
- BG14hog1Δ was sensitive to high osmolarity above 0.5 M NaCl and to sorbic acid: reduced growth at 1 mM and severely reduced growth at 3 mM at pH 4.5, while neutral pH required above 20 mM sorbic acid to inhibit growth.
- Microarray profiling after 20 mM sorbate for 20 min at neutral pH showed similar overall wild-type and mutant responses (Pearson r = 0.84), with CgPDR12 the highest induced gene: >160-fold in wild type and 130-fold in the mutant; qRT-PCR confirmed >10-fold induction and reduced levels in BG14hog1Δ.
- Comparison to S. cerevisiae sorbic acid stress data gave a weak correlation (r = 0.25), though PDR12 was the most highly induced gene in both species.
Methods
- CgHOG1 (CAGL0M11748g) was deleted in the BG14 background by homologous recombination using a SAT1 nourseothricin resistance cassette, deleting ORF base pairs 402–960; correct integration was verified by genomic PCR.
- Stress phenotypes were assayed by serial dilution spot tests on YPD pH 4.5 with NaCl or potassium sorbate, and at neutral pH with sorbic acid; Hog1 phosphorylation was detected with anti-phospho-p38 MAPK antibodies, and CgHog1-GFP localization was followed by live microscopy.
- Expression profiling used custom C. glabrata Agilent arrays with three biological replicates after 20 mM potassium sorbate for 20 min at neutral pH; data were quantile normalized, clustered, GO-analyzed, and PDR12 was measured by qRT-PCR with ACT1 as control.
Limitations
- The authors state that whether the reduced CgPDR12 mRNA level in the hog1Δ mutant accounts for sorbic acid sensitivity “remains to be shown,” and they think failure to express CgPDR12 is not likely the main cause.
- The authors state that the relevance of the constitutive partially active HOG pathway and the observed expression differences to weak acid resistance, virulence, or persistence “requires further investigation.”
- The authors note that part of the difference between C. glabrata and S. cerevisiae expression patterns is “of technical nature”; evident from the text, the microarray analysis used one strain background (BG14), a single 20-min sorbate treatment, and the upstream sensing mechanism for weak acid activation of the C. glabrata HOG pathway remains unknown.
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Claims the paper makes
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- Findingown data
The CgHOG1 deleted strain, BG14hog1Δ, was sensitive to high osmolarity conditions higher than 0.5 M NaCl.
“The CgHOG1 deleted strain, BG14hog1Δ, was sensitive to high osmolarity conditions higher than 0.5 M NaCl (Figure 1B).”
Quote in the paperSubstantial claim - Findingown data
At neutral pH, concentrations above 20 mM sorbic acid were required to inhibit growth.
“At neutral pH, concentrations above 20 mM sorbic acid were required to inhibit growth (Figure 2C).”
Quote in the paperNot a substantial claim - Findingown data
BG14hog1Δ was sensitive to sorbic acid stress.
“In addition to the expected phenotype of high osmolarity sensitivity, BG14hog1Δ, was sensitive to sorbic acid stress (Figure 2A).”
Quote in the paperSubstantial claim - Findingown data
CgHog1 has a function for weak acid stress resistance.
“Here we show that the MAP kinase of the HOG pathway, CgHog1, becomes phosphorylated and has a function for weak acid stress resistance.”
Quote in the paperSubstantial claim - Findingown data
In C. glabrata the HOG pathway is activated by sorbic acid.
“In contrast, in C. glabrata the high osmolarity glycerol (HOG) pathway is activated by sorbic acid.”
Quote in the paperSubstantial claim- Rests on an assumption: Activation of Hog1 by phosphorylation of activation loop residues by MAPKK Pbs2 causes its rapid translocation into the nucleus.
- Findingown data
CgHog1 is required for sorbic acid resistance of C. glabrata.
“Moreover, we show that CgHog1 is required for sorbic acid resistance of C. glabrata.”
Quote in the paperSubstantial claim - Findingown data
PDR12 required CgHog1 for full expression.
“The PDR12 gene was the highest induced gene in both species and it required CgHog1 for full expression.”
Quote in the paperSubstantial claim - Findingown data
CgHog1 becomes phosphorylated under weak acid stress.
“Here we show that the MAP kinase of the HOG pathway, CgHog1, becomes phosphorylated and has a function for weak acid stress resistance.”
Quote in the paperSubstantial claim - Findingnone given
The C. glabrata mutant lacking Hog1 could tolerate higher salt concentration than the corresponding S. cerevisiae mutant strain.
“The C. glabrata mutant lacking Hog1 could tolerate higher salt concentration than the corresponding S. cerevisiae mutant strain.”
Quote in the paperNot a substantial claim - Findingown data
The PDR12 gene was the highest induced gene in both species.
“The PDR12 gene was the highest induced gene in both species and it required CgHog1 for full expression.”
Quote in the paperNot a substantial claim - Findingcitation
The overall sensitivity of the HOG1 deleted strain was similar to the mutant lacking the MAPKK Pbs2.
“The overall sensitivity of the HOG1 deleted strain was similar to the mutant lacking the MAPKK Pbs2 (Gregori et al., 2007b).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Gregori et al., 2007b
Not checked in the free run.
- Findingown data
Transcript profiling of weak acid treated C. glabrata cells suggests a broad and very similar response pattern of cells lacking CgHog1 compared to wild type which is overlapping with but distinct from S. cerevisiae.
“Transcript profiling of weak acid treated C. glabrata cells suggests a broad and very similar response pattern of cells lacking CgHog1 compared to wild type which is over lapping with but distinct from S. cerevisiae.”
Quote in the paperSubstantial claim - Findingown data
Sorbic acid stress at neutral pH increases CgHog1 and CgHog1-GFP phosphorylation to a level comparable to osmotic stress.
“We detected an increase of CgHog1 and of CgHog1-GFP phosphorylation to a comparable level in the osmotic and sorbic acid stressed case (Figure 3D).”
Quote in the paperSubstantial claim - Findingown data
The microarray experiment shows differences between transcript patterns of unstressed hog1Δ mutant and wild type.
“our microarray experiment shows differences between the transcript patterns of unstressed deletion mutant and wild type.”
Quote in the paperNot a substantial claim - Findingown data
The overall response pattern of repressed and induced genes after 20 min treatment with 20 mM sorbate at neutral pH is very similar between BG14hog1Δ mutant and wild type, with a Pearson correlation coefficient r = 0.84.
“The overall response pattern of repressed and induced genes in was very similar between mutant and wild type as seen in a clustered presentation and a scatter plot (pearson correlation coefficient r = 0.84 of genes in Figure 4A).”
Quote in the paperSubstantial claim - Findingown data
We found signals indicating phosphorylation and thus active CgHog1 in unstressed cells.
“Interestingly, and different from S. cerevisiae, we found signals indicating phosphorylation and thus active CgHog1 in unstressed cells (Figures 3C,D).”
Quote in the paperSubstantial claim- Rests on an assumption: Activation of Hog1 by phosphorylation of activation loop residues by MAPKK Pbs2 causes its rapid translocation into the nucleus.
- Findingown data
CgHog1 phosphorylation level increases in cells treated with 5 and 10 mM sorbic acid for 40 min at pH4.5.
“CgHog1 phosphorylation level increases in cells treated with 5 and 10 mM sorbic acid for 40 min at pH4.5 (Figure 3C).”
Quote in the paperSubstantial claim - Findingown data
In both wild type and hog1Δ mutant, the highest induced genes after sorbate treatment were CgPDR12, CgBTN1, CgHSP42, and CgDCS2.
“The highest induced genes in both wild type and mutant were CgPDR12, CgBTN1 (possible role in mediating pH homeostasis), CgHSP42 (a small heat shock protein with chaperone activity), CgDCS2 [m(7)GpppX pyrophosphatase regulator protein].”
Quote in the paperNot a substantial claim - Findingown data
The fluorescence signal of the CgHog1-GFP construct showed a substantial nuclear accumulation in unstressed cells.
“The fluorescence signal of the CgHog1-GFP construct showed a substantial nuclear accumulation in unstressed cells.”
Quote in the paperNot a substantial claim - Findingown data
CgHog1 kinase has a relatively high phosphorylation level in unstressed cells, unlike S. cerevisiae.
“As an additional striking difference to S. cerevisiae, we observe a relatively high phosphorylation level of the CgHog1 kinase in unstressed cells.”
Quote in the paperNot a substantial claim - Findingown data
Exposure to sorbic acid led to an enhanced staining of nuclei by Hog1-GFP within short time.
“Despite an apparent partial activation in unstressed cells, exposure to sorbic acid led to an enhanced staining of nuclei by Hog1-GFP within short time.”
Quote in the paperSubstantial claim - Findingown data
For a small number of genes in cluster one, the fold increase was reduced by a factor of more than 2 in the absence of CgHog1.
“For a small number of genes of this cluster, the fold increase of was reduced by a factor of more than 2 in absence of CgHog1 (Supp DataSheet1/Top_changed; CAGL0L05016g STB6, CAGL0K07205g (unknown), CAGL0C02321g PHM8, CAGL0F01111g OPI10, CAGL0B00858g STE50, CAGL0K07590g, MYO3).”
Quote in the paperNot a substantial claim - Findingown data
Hog1-GFP nuclear accumulation was visible immediately after addition of sorbic acid.
“However, Hog1-GFP nuclear accumulation was visible immediately after addition of sorbic acid.”
Quote in the paperSubstantial claim - Findingown data
CgHog1 partially accumulates in the nucleus in unstressed cells, in contrast to ScHog1.
“In contrast to ScHog1, and possibly connected to its basal phosphorylation, we find a partial accumulation of CgHog1 in the nucleus in unstressed cells.”
Quote in the paperNot a substantial claim - Findingown data
Both endogenous CgHog1 and plasmid encoded CgHog1-GFP fusion protein showed similar changes of phosphorylation levels upon treatment with sorbic acid.
“Both the endogenous CgHog1 and the plasmid encoded CgHog1-GFP fusion protein showed similar changes of phosphorylation levels upon treatment with sorbic acid.”
Quote in the paperNot a substantial claim - Findingown data
Cluster two is enriched in genes with lower expression levels in unstressed hog1Δ mutant cells.
“Furthermore, cluster two is enriched in genes with lower expression levels in unstressed mutant cells.”
Quote in the paperNot a substantial claim - Findingown data
Cluster one of the 466 induced genes is enriched in genes with functions in proteolysis, autophagy, and mainly cytosolic components.
“Cluster one is enriched in genes with functions in proteolysis, autophagy and mainly cytosolic components.”
Quote in the paperNot a substantial claim - Findingown data
CgCOM2 has a 2.6-fold increase in expression.
“whereas CgCOM2 has a robust 2.6-fold increase of expression.”
Quote in the paperNot a substantial claim - Findingown data
Cluster two of the induced genes is enriched in mitochondrial functions and carbon metabolism.
“Cluster two comprises the remaining genes of this set and is strikingly enriched in mitochondrial functions and carbon metabolism (Supplementary GO data in DataSheet1).”
Quote in the paperNot a substantial claim - Findingown data
Basal expression of many genes linked to mitochondrial function and carbon catabolism is reduced in the hog1Δ mutant.
“Basal expression of many genes linked to mitochondrial function and carbon catabolism is reduced in the mutant.”
Quote in the paperNot a substantial claim - Findingown data
Repressed genes after sorbate treatment were enriched in protein synthesis related functions.
“The repressed genes were enriched in protein synthesis related functions.”
Quote in the paperNot a substantial claim - Findingown data
The gene expression dataset shows a large change of CgPDR12 transcript level.
“Our gene expression dataset shows a large change of CgPDR12 transcript level.”
Quote in the paperSubstantial claim - Findingown data
Cells lacking Hog1 had 2/3 of wild type CgPDR12 mRNA level.
“Cells lacking Hog1 had 2/3rd of wild type CgPDR12 mRNA level”
Quote in the paperSubstantial claim - Study design and conductown data
The CgHog1-GFP fusion construct complemented the deleted allele.
“The CgHog1-GFP fusion construct complemented the deleted allele (Figures 2B,C).”
Quote in the paperSubstantial claim - Premisecitation
CgPbs2 mutants display hypersensitivity to weak organic acids.
“In contrast to yeast, however, CgPbs2 (the MAPKK) mutants display hypersensitivity to weak organic acids (Gregori et al., 2007b).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Gregori et al., 2007b
Not checked in the free run.
- Interpretationown data
Our results support flexibility of the response cues for general stress signaling pathways, even between closely related yeasts.
“Our results support flexibility of the response cues for general stress signaling pathways, even between closely related yeasts, and functional extension of a specific response pathway.”
Quote in the paperSubstantial claim - Premisecitation
CgMsn2 does not accumulate in C. glabrata cells exposed to weak acids (sorbate and propionate).
“Strikingly, CgMsn2 did not accumulate in C. glabrata cells exposed to weak acids (sorbate and propionate).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Roetzer et al., 2008
Not checked in the free run.
- Interpretationown data
Our results support functional extension of a specific response pathway.
“Our results support flexibility of the response cues for general stress signaling pathways, even between closely related yeasts, and functional extension of a specific response pathway.”
Quote in the paperSubstantial claim - Interpretationcitation
These results suggest that the CgHOG pathway compared to ScHog1 has acquired or retained other functions.
“These results would suggest that CgHOG pathway compared to ScHog1 has acquired or retained other functions.”
Quote in the paperSubstantial claim - Interpretationown data
The genes with reduced induction in hog1Δ have striking relations to starvation and stress resistance.
“These genes have striking relations to starvation and stress resistance.”
Quote in the paperNot a substantial claim- Rests on an assumption: Phm8 is a lysophosphatidic acid (LPA) phosphatase active in response to phosphate starvation.
- Rests on an assumption: Ste50 is involved in mating, filamentous growth and osmotolerance.
- Interpretationcitation
The sorbic acid stress sensitivity of the CgPbs2 mutant indicates activation of the C. glabrata MAP kinase cascade.
“The sorbic acid stress sensitivity of the CgPbs2 mutant further indicates activation of the C. glabrata MAP kinase cascade but the sensing mechanism upstream is yet unknown (Gregori et al., 2007a).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Gregori et al., 2007a
Not checked in the free run.
- Interpretationown data
The signals obtained suggest that two pools of CgHog1 might exist in C. glabrata which are perhaps not separated at the level of the wild type size protein.
“The signals obtained suggest that two pools of CgHog1 might exist in C. glabrata which are perhaps not separated at the level of the wild type size protein.”
Quote in the paperNot a substantial claim - Premisecitation
The difference in Msn2 behavior is not related to differences in intracellular acidification of sorbate-exposed cells.
“The cause for this difference to S.cerevisiae Msn2 is unclear, however, is not related to difference in intracellular acidification of sorbate exposed cells (Ullah et al., 2013b).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Ullah et al., 2013b
Not checked in the free run.
- Interpretationown data
The HOG pathway does not contribute substantially to transcriptional regulation of the weak acid anion pump.
“and thus the HOG pathway does not contribute substantial to transcriptional regulation of the weak acid anion pump.”
Quote in the paperSubstantial claim
- May combine two claims. 20
- Classified as probably not a substantial claim. 26
May combine two claims.
FindingcitationWe found reduced growth on pH4.5 medium containing 1 mM sorbic acid and severely reduced growth with 3 mM.
“We found reduced growth on pH4.5 medium containing 1 mM sorbic acid and severely reduced growth with 3 mM, as observed earlier (Gregori et al., 2007b).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Gregori et al., 2007b
Not checked in the free run.
May combine two claims.
Findingown dataSorbic acid stress causes a robust high level phosphorylation of CgHog1 coinciding with an enrichment in the nucleus.
“We find that sorbic acid stress causes a robust high level phosphorylation of CgHog1 coinciding with an enrichment in the nucleus.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataCgMSN4 is induced 5-fold in sorbate-treated cells and higher in the hog1Δ mutant.
“Interestingly, CgMSN4 is induced 5-fold (and higher in the mutant)”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataWeak acids activate the C. glabrata HOG pathway, leading to MAP kinase activation and nuclear accumulation.
“We report an initial characterization of the C. glabrata Hog1 MAP kinase and show activation of the HOG pathway by weak acids in this yeast.”
- Also stated in: § Discussion · boosted
“Taken together, we show that weak acids trigger the C. glabrata HOG response pathway leading to MAP kinase activation and nuclear accumulation.”
Quote in the paperSubstantial claim- Also stated in: § Discussion · boosted
May combine two claims.
Findingown dataThe GFP fusion protein splits into two species of which the slower migrating form shows more dynamic changes of phosphorylation.
“Interestingly, the GFP fusion protein splits into two species of which the slower migrating form shows more dynamic changes of phosphorylation.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataIn array data, PDR12 changes more than 160-fold in wild type and 130-fold in the hog1Δ mutant.
“In our array data the PDR12 gene changes more than 160-fold in the wild type and 130-fold in the mutant.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataComparison of C. glabrata sorbate stress data to S. cerevisiae sorbic acid stress data yields a weak correlation coefficient r = 0.25, but some similarities such as PDR12 as the most highly induced gene exist.
“Comparison to S. cerevisiae sorbic acid stress data (Schüller et al., 2004; SuppTable1: SCvsCG_Sorbat) results in a mixed picture of a surprisingly weak correlation coefficient (r = 0.25), however, some characteristic similarities such as PDR12 as the most highly induced gene exist.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Schüller et al., 2004
Not checked in the free run.
May combine two claims.
Findingown dataWeak acid treatment causes a rapid increase of dually phosphorylated CgHog1 and thus signaling through this pathway.
“We show here that weak acid treatment causes a rapid increase of dually phosphorylated CgHog1 and thus signaling through this pathway.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataRT-qPCR in two independent biological replicates confirmed PDR12 induction with >10-fold change and a similarly reduced level in the BG14hog1Δ strain.
“We confirmed this by RT-qPCR in two independent biological replicas and found a fold change of >10-fold (due to higher unstressed background signal) and a similarly reduced level in the BG14hog1Δ strain (Figure 4D).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationStress activated protein kinase networks are well conserved across kingdoms and orthologs of Hog1 are present in other fungi.
“Stress activated protein kinase networks are well conserved across kingdoms and orthologs of Hog1 are present in other fungi (Nikolaou et al., 2009).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Nikolaou et al., 2009
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Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationActivation of PDR12 transcription is sufficient for weak acid resistance.
“Strikingly, activation of PDR12 transcription is sufficient for weak acid resistance (Schüller et al., 2004).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Schüller et al., 2004
Not checked in the free run.
Classified as probably not a substantial claim.
Study design and conductown dataCorrect integration of the cassette was verified by genomic PCR.
“The correct integration of the cassette was verified by genomic PCR (Figure 1A).”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
PremisecitationThe well-characterized HOG pathway is essential for yeast survival under high osmolarity conditions.
“The well-characterized high-osmolarity glycerol (HOG) pathway is essential for yeast survival under-high osmolarity conditions, since it triggers adaptation through intracellular accumulation of glycerol as the adaptive osmolytes to reestablish the balance of water and ion concentration (De Nadal and Posas, 2010).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites De Nadal and Posas, 2010
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationIn yeast and C. glabrata, the HOG signaling pathway is required for osmotic stress response and oxidative stress.
“In yeast and C. glabrata, the HOG signaling pathway is required for osmotic stress response and oxidative stress (Kaloriti et al., 2012).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Kaloriti et al., 2012
Not checked in the free run.
Classified as probably not a substantial claim. May combine two claims.
PremisecitationS. cerevisiae cells treated with weak organic acids accumulate Msn2 and Msn4 rapidly in the nucleus and activate a relatively large regulon of generic stress responsive genes.
“S. cerevisiae cells treated with weak organic acids accumulate the transcription factors Msn2 and Msn4 rapidly in the nucleus and activate a relative large regulon of generic stress responsive genes (Schüller et al., 2004).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Schüller et al., 2004
Not checked in the free run.
Classified as probably not a substantial claim. May combine two claims.
InterpretationreasoningThus, C. glabrata either lacks a pathway which is operative in S. cerevisiae or responds differently to weak acids.
“Thus, C. glabrata either lacks a pathway which is operative in S. cerevisiae or responds differently to weak acids.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationCompared to C. albicans, C. glabrata is more similar to Saccharomyces cerevisiae.
“Compared to C. albicans, C. glabrata is more similar to Saccharomyces cerevisiae (Dujon, 2010)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Dujon, 2010
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PremisecitationCgMsn2 expressed in yeast cells showed similar nuclear accumulation as ScMsn2.
“However, CgMsn2 expressed in yeast cells showed similar nuclear accumulation as ScMsn2 (Roetzer et al., 2008).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Roetzer et al., 2008
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Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationWeak acids induce expression of the C. glabrata adhesin Epa6 via an Msn2/4 and War1 independent mechanism leading to enhanced adherence.
“Weak acids induce expression of the C glabrata adhesin Epa6 via an Msn2/4 and War1 independent mechanism leading to enhance adherence.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Mundy and Cormack, 2009
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PremisecitationIn S. cerevisiae this factor triggers expression of a small regulon consisting of PDR12 and FUN34.
“In S. cerevisiae this factor triggers expression of a small regulon consisting of an ABC (ATP binding cassette) transporter gene PDR12 which is required for weak acid ion efflux as well as an ammonia transporter FUN34 (Kren et al., 2003; Schüller et al., 2004; Gregori et al., 2007a).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Kren et al., 2003
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- cites Schüller et al., 2004
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- cites Gregori et al., 2007a
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PremisecitationWeak acid response at the transcriptional level is mediated by the zinc cluster transcription factor War1 in S. cerevisiae, C. albicans, and C. glabrata.
“Weak acid response at the transcriptional level is mediated by the zinc cluster transcription factor War1 (weak acid response 1) in S.cerevisiae, C. albicans, and C. glabrata (Kren et al., 2003; Lebel et al., 2006; Mundy and Cormack, 2009).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Kren et al., 2003
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- cites Lebel et al., 2006
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- cites Mundy and Cormack, 2009
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PremisecitationAdaptation to weak acids also requires Haa1, a further weak acid inducible transcription factor in S. cerevisiae.
“In addition, adaptation to weak acids also requires Haa1, a further weak acid inducible transcription factor S. cerevisiae (Fernandes et al., 2005).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Fernandes et al., 2005
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InterpretationreasoningYer130C/Com2 might be connected to weak acid stress in both organisms.
“Therefore, Yer130C/Com2 might be connected to weak acid stress in both organisms.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
PremisecitationWeak acids like sorbic or benzoic acid traverse the plasma membrane in the protonated form and dissociate in the cytosol.
“Weak acids like sorbic or benzoic acid traverse the plasma membrane in the protonated form and dissociate in the cytosol (Piper, 2011).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Piper, 2011
Not checked in the free run.
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PremisecitationThe C. glabrata HOG pathway is involved in weak acid and acetate resistance.
“Previously, the C. glabrata HOG pathway has been shown to be involved in weak acid and acetate resistance (Gregori et al., 2007a).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Gregori et al., 2007a
Not checked in the free run.
May combine two claims.
Interpretationown dataOne pool is apparently constitutively phosphorylated and the other shows dynamic changes.
“One is apparently constitutively phosphorylated and the other shows dynamic changes.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationS. cerevisiae Hog1 has a role in re-entry into the cell cycle after starvation-induced resting.
“A role for S. cerevisiae Hog1 for the re-entry into the cell cycle after starvation induced resting has been reported (Escote et al., 2011).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Escote et al., 2011
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Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationIn C. albicans and S. cerevisiae, Hog1 activation causes nuclear translocation and a dramatic change of gene expression mediated by transcription factors, in addition to changes in cytosolic targets.
“The consequence of Hog1 activation in C. albicans and S. cerevisiae is, apart from changes of the activity of cytosolic targets (Thorsen et al., 2006; Mollapour and Piper, 2007), nuclear translocation and a dramatic change of gene expression mediated by a set of transcription factors.”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Thorsen et al., 2006
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- cites Mollapour and Piper, 2007
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Study design and conductown dataWe repeated the experiment with an antibody recognizing the double phosphorylated form to confirm that the observations are not due to a mono-phosphorylated TEY, and thus likely inactive CgHog1.
“We repeated the experiment with an antibody recognizing the double phosphorylated form to confirm that the observations are not due to a mono-phosphorylated TEY, and thus likely inactive CgHog1.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown dataThe RT-qPCR confirmation was performed in two independent biological replicates.
“We confirmed this by RT-qPCR in two independent biological replicas”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Study design and conductown dataThe signal originating from CgHog1 is identified by testing a BG14hog1Δ strain without GFP plasmid.
“The signal originating from CgHog1 is identified by testing a BG14hog1Δ strain without GFP plasmid (Figure 3D).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationYer130C/Com2 is a Zn-finger protein similar to ScMsn2/4 and C. albicans Mnl1, and its expression is induced by acetic acid stress.
“Yer130C (designated COM2 for Cousin Of Msn2) is a Zn-finger protein similar to ScMsn2/4 and C. albicans Mnl1 and interestingly its expression is induced by acetic acid stress (Mira et al., 2011).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Mira et al., 2011
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Interpretationown dataThe pattern of genes induced in both organisms suggests less pronounced increase of S. cerevisiae Msn2/4 orthologous target genes in C. glabrata.
“Inspection of the pattern of genes induced in both organisms raises a suspicion of less pronounced increase of S. cerevisiae Msn2/4 orthologous target genes in C. glabrata.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationIn S. cerevisiae, PDR12 confers most of weak acid resistance.
“The S. cerevisiae PDR12 gene confers most of weak acid resistance (Schüller et al., 2004).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Schüller et al., 2004
Not checked in the free run.
May combine two claims.
PremisecitationCgMsn2 and CgMsn4 do not translocate into the nucleus in weak acid stressed C. glabrata cells, suggesting they are not involved.
“CgMsn2 and CgMsn4 do not translocate into the nucleus in weak acid stressed C. glabrata cells, suggesting that they are presumably not involved (Roetzer et al., 2008).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Roetzer et al., 2008
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
InterpretationcitationThe similar response of p38 might represent a conserved SAPK-dependent response for cells leaving a resting state.
“Since p38 shows similar response, this might represent a conserved SAPK-dependent response for cells leaving a resting state (Escote et al., 2011).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Escote et al., 2011
Not checked in the free run.
May combine two claims.
InterpretationreasoningIn C. glabrata, a similar large number of genes change expression upon sorbate treatment, suggesting other factors substitute for Msn2/4 function.
“Nevertheless, in C. glabrata a similar large number of genes change expression upon Sorbate treatment suggesting other factors substitute for their function.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationHog1 rapidly enters the nucleus at the time of resumption of growth in absence of osmotic stress.
“Strikingly, Hog1 rapidly enters the nucleus at the time of resumption of growth in absence of osmotic stress.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Escote et al., 2011
Not checked in the free run.
The paper relies on this without support.
Activation of Hog1 by phosphorylation of activation loop residues by MAPKK Pbs2 causes its rapid translocation into the nucleus.
“Activation of Hog1 by phosphorylation of the activation loop residues by the MAPKK Pbs2 causes its rapid translocation into the nucleus.”
The paper relies on this without support.
The detailed action of Hog1 in C. glabrata and its downstream targets have not been investigated in depth so far.
“However, the detailed action of Hog1 in C. glabrata and its downstream targets have not been investigated in depth so far.”
The paper relies on this without support.
S. cerevisiae strains lacking Hog1 are not sensitive to sorbic acid.
“Notably, S. cerevisiae strains lacking Hog1 are not sensitive to sorbic acid.”
The paper relies on this without support.
Phm8 is a lysophosphatidic acid (LPA) phosphatase active in response to phosphate starvation.
“Phm8 is a Lysophosphatidic acid (LPA) phosphatase active in response to phosphate starvation.”
The paper relies on this without support.
Ste50 is involved in mating, filamentous growth and osmotolerance.
“Ste50 is involved in mating, filamentous growth and osmotolerance.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The high osmolarity glycerol pathway is activated by sorbic acid, and its terminal MAPK CgHog1 is required for survival of weak acid and osmotic stress.
“However, the high osmolarity glycerol pathway [HOG] is known to be activated by sorbic acid, and its terminal MAPK CgHog1 is required for survival of weak acid and osmotic stress [95,96].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [95]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Conflicting treatment time for the Figure 3C phosphorylation experiment
MinorThe results describe the 5 and 10 mM sorbic acid samples in Figure 3C as treated for 40 minutes, while the Figure 3C caption says they were harvested after 20 minutes.
“CgHog1 phosphorylation level increases in cells treated with 5 and 10 mM sorbic acid for 40 min at pH4.5 (Figure 3C).”
“(C) CgHog1 and CgHog1-GFP phosphorylation increases in sorbate treated cells. Cultures of BG14, BG14hog1Δ, and BG14 carrying pHog1-GFP were grown in YPD (pH 4.5) to the early-exponential-growth phase before 5 or 10 mM Sorbic acid was added. Samples were harvested after 20 min.”
Fluorescence ratio is defined in opposite directions
MinorThe microscopy methods say the quantified ratio is cytosol to nucleus, whereas the Figure 3B caption calls it nucleus to cytosol. These are reciprocal ratios.
“The background subtracted signal ratio of cytosol to nucleus was determined comparing the fluorescence signals obtained from both compartments during 10 min 10 mM of sorbic acid stress, and non-stress conditions.”
“(B) Nuclear accumulation of Hog1 upon stress induction results in a higher fluorescence signal and increases the nucleus to cytosol signal ratio. Fluorescence intensity ratio, nucleus to cytosol, in unstressed (n = 20) and stressed (n = 26) cells.”
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- Authors
- Jandric, Z., Gregori, C., Klopf, E., Radolf, M., & Schüller, C.
- Affiliations
- BOKU University (AT)
- Max Perutz Labs (AT)
- Research Institute of Molecular Pathology (AT)
- Corresponding author
- Schüller, Christoph
- ORCID
- Schüller, Christoph
- Venue
- Frontiers in Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2013
- Volume
- 4
- Pages
- 350-350
- ISSN
- 1664-302X (ISSN-L)
- PMC
- PMC3840799
- OpenAlex
- W2008156634
- Semantic Scholar
- 99a212d65dcc76ffb16b20386eaae341d6fbdc3a
- Cited by
- 28
- References
- 49
- Citations by year
- 2024: 3 · 2023: 1 · 2022: 1 · 2021: 2 · 2020: 2 · 2019: 2 · 2018: 3 · 2017: 4 · 2016: 4 · 2015: 4 · 2014: 1 · 2013: 1
- FWCI
- 1.49
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Microbiology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Austrian Science Fund (P 23355)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Keywords
- Candida glabrata, high-osmolarity glycerol pathway, Hog1 MAP kinase, Msn2, Msn4, gene expression profiling, Saccharomyces cerevisiae comparison, stress signaling pathways, food preservatives
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.
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