Paper · 2022 · Frontiers in Microbiology

Modulation of extracellular Penicillium expansum-driven acidification by Papiliotrema terrestris affects biosynthesis of patulin and has a possible role in biocontrol activity

Davide Palmieri; Cecilia Miccoli; Ivan Notardonato; et al.

13
claims
32
verbatim quotes
15
citations
1
research areas
✓
Open access · cc-by

Abstract

The active regulation of extracellular pH is critical for the virulence of fungal pathogens. Penicillium expansum is the causal agent of green-blue mold on stored pome fruits and during its infection process acidifies the host tissues by secreting organic acids. P. expansum is also the main producer of patulin (PAT), a mycotoxin found in pome fruit-based products and that represents a serious health hazard for its potential carcinogenicity. While it is known that PAT biosynthesis in P. expansum is regulated by nutritional factors such as carbon and nitrogen and by the pH, the mechanistic effects of biocontrol on PAT production by P. expansum are not known. In this work, we assessed how optimal and suboptimal concentrations of the biocontrol agent (BCA) Papiliotrema terrestris LS28 affect both extracellular pH and PAT biosynthesis in P. expansum . In wounded apples, the optimal and suboptimal concentrations of the BCA provided almost complete and partial protection from P. expansum infection, respectively, and reduced PAT contamination in both cases. However, the suboptimal concentration of the BCA increased the specific mycotoxigenic activity by P. expansum . In vitro , the rate of PAT biosynthesis was strictly related to the extracellular pH, with the highest amount of PAT detected in the pH range 4–7, whereas only traces were detectable at pH 3. Moreover, both in vitro and in apple wounds the BCA counteracted the extracellular P. expansum -driven acidification maintaining extracellular pH around 4, which is within the pH range that is optimal for PAT biosynthesis. Conversely, in the absence of LS28 the pathogen-driven acidification led to rapidly achieving acidic pH values (<3) that lie outside of the optimal pH range for PAT biosynthesis. Taken together, these results suggest that pH modulation by LS28 is important to counteract the host tissue acidification and, therefore, the virulence of P. expansum . On the other hand, the buffering of P. expansum -driven acidification provided by the BCA increases the specific rate of PAT biosynthesis through the extension of the time interval at which the pH value lies within the optimal range for PAT biosynthesis. Nevertheless, the antagonistic effect provided by the BCA greatly reduced the total amount of PAT.

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Claims 13

Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Optimal BCA concentration gave almost complete protection of wounded apples from P. expansum infection.

Treatment
optimale2
Interactor
P. expansumPenicillium expansume2pathogen
Second interactor
Papiliotrema terrestris LS28Papiliotrema terrestrise3biocontrol_agent
Outcome
protection from P. expansum infectione2
Direction
almost completee2

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗
Penicillium expansum
Penicillium expansum · InteractorH.J. Larsen, Bugwood.org · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e2

“the optimal and suboptimal concentrations of the BCA provided almost complete and partial protection from P. expansum infection, respectively, and reduced PAT contamination in both cases”

✓ located verbatim in the source · abstract, characters 878–1064 · show in text ↑
e3

“biocontrol agent (BCA) Papiliotrema terrestris LS28”

✓ located verbatim in the source · abstract, characters 740–791 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Suboptimal BCA concentration gave partial protection of wounded apples from P. expansum infection.

Treatment
suboptimale2
Interactor
P. expansumPenicillium expansume2pathogen
Second interactor
Papiliotrema terrestris LS28Papiliotrema terrestrise3biocontrol_agent
Outcome
protection from P. expansum infectione2
Direction
partiale2

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗
Penicillium expansum
Penicillium expansum · InteractorH.J. Larsen, Bugwood.org · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e2

“the optimal and suboptimal concentrations of the BCA provided almost complete and partial protection from P. expansum infection, respectively, and reduced PAT contamination in both cases”

✓ located verbatim in the source · abstract, characters 878–1064 · show in text ↑
e3

“biocontrol agent (BCA) Papiliotrema terrestris LS28”

✓ located verbatim in the source · abstract, characters 740–791 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Optimal BCA concentration reduced PAT contamination in wounded apples.

Treatment
optimale2
Interactor
P. expansumPenicillium expansume2pathogen
Second interactor
Papiliotrema terrestris LS28Papiliotrema terrestrise3biocontrol_agent
Outcome
PAT contaminatione2
Direction
reducede2

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗
Penicillium expansum
Penicillium expansum · InteractorH.J. Larsen, Bugwood.org · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e2

“the optimal and suboptimal concentrations of the BCA provided almost complete and partial protection from P. expansum infection, respectively, and reduced PAT contamination in both cases”

✓ located verbatim in the source · abstract, characters 878–1064 · show in text ↑
e3

“biocontrol agent (BCA) Papiliotrema terrestris LS28”

✓ located verbatim in the source · abstract, characters 740–791 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Suboptimal BCA concentration reduced PAT contamination in wounded apples.

Treatment
suboptimale2
Interactor
P. expansumPenicillium expansume2pathogen
Second interactor
Papiliotrema terrestris LS28Papiliotrema terrestrise3biocontrol_agent
Outcome
PAT contaminatione2
Direction
reducede2

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗
Penicillium expansum
Penicillium expansum · InteractorH.J. Larsen, Bugwood.org · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e2

“the optimal and suboptimal concentrations of the BCA provided almost complete and partial protection from P. expansum infection, respectively, and reduced PAT contamination in both cases”

✓ located verbatim in the source · abstract, characters 878–1064 · show in text ↑
e3

“biocontrol agent (BCA) Papiliotrema terrestris LS28”

✓ located verbatim in the source · abstract, characters 740–791 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Suboptimal BCA concentration increased the specific mycotoxigenic activity of P. expansum.

Treatment
suboptimale4
Interactor
P. expansumPenicillium expansume4pathogen
Second interactor
Papiliotrema terrestris LS28Papiliotrema terrestrise3biocontrol_agent
Outcome
specific mycotoxigenic activitye4
Direction
increasede4

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗
Penicillium expansum
Penicillium expansum · InteractorH.J. Larsen, Bugwood.org · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e4

“the suboptimal concentration of the BCA increased the specific mycotoxigenic activity by P. expansum”

✓ located verbatim in the source · abstract, characters 1075–1175 · show in text ↑
e3

“biocontrol agent (BCA) Papiliotrema terrestris LS28”

✓ located verbatim in the source · abstract, characters 740–791 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

In vitro, the rate of PAT biosynthesis was strictly related to extracellular pH.

Treatment
extracellular pHe5
Outcome
rate of PAT biosynthesise5
Setting
In vitroe5

Not reportedDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e5

“In vitro , the rate of PAT biosynthesis was strictly related to the extracellular pH”

✓ located verbatim in the source · abstract, characters 1178–1262 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

The highest amount of PAT was detected at extracellular pH in the range 4–7.

Treatment
pH range 4–7e6
Outcome
amount of PAT detectede6
Direction
higheste6

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e6

“the highest amount of PAT detected in the pH range 4–7”

✓ located verbatim in the source · abstract, characters 1269–1323 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Only traces of PAT were detectable at pH 3.

Outcome
only traces were detectablee7
Qualifier
at pH 3e7

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e7

“only traces were detectable at pH 3”

✓ located verbatim in the source · abstract, characters 1333–1368 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

The BCA maintained extracellular pH around 4 against P. expansum-driven acidification in vitro and in apple wounds.

Treatment
the BCAe4
Interactor
P. expansumPenicillium expansume4pathogen
Second interactor
Papiliotrema terrestris LS28Papiliotrema terrestrise3biocontrol_agent
Outcome
extracellular pHe4
Direction
maintaininge4
Value
around 4e4
Setting
in vitroe4

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗
Penicillium expansum
Penicillium expansum · InteractorH.J. Larsen, Bugwood.org · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e4

“both in vitro and in apple wounds the BCA counteracted the extracellular P. expansum -driven acidification maintaining extracellular pH around 4”

✓ located verbatim in the source · abstract, characters 1380–1524 · show in text ↑
e3

“biocontrol agent (BCA) Papiliotrema terrestris LS28”

✓ located verbatim in the source · abstract, characters 740–791 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

In the absence of LS28, pathogen-driven acidification rapidly led to acidic pH values below 3.

Outcome
rapidly achieving acidic pH valuese4
Value
<3e4
Qualifier
in the absence of LS28e4

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e4

“in the absence of LS28 the pathogen-driven acidification led to rapidly achieving acidic pH values (<3)”

✓ located verbatim in the source · abstract, characters 1605–1708 · show in text ↑
Mechanismauthor interpretationoriginal resultpositivemeasured

Claim · model-written summary

pH modulation by LS28 appears important to counteract host tissue acidification and the virulence of P. expansum.

Treatment
pH modulation by LS28e4
Interactor
P. expansumPenicillium expansume4pathogen
Second interactor
LS28e4biocontrol_agent
Outcome
virulence of P. expansume4

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗
Penicillium expansum
Penicillium expansum · InteractorH.J. Larsen, Bugwood.org · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e4

“pH modulation by LS28 is important to counteract the host tissue acidification and, therefore, the virulence of P. expansum”

✓ located verbatim in the source · abstract, characters 1815–1938 · show in text ↑
Associationobservedoriginal resultnegativemeasured

Claim · model-written summary

The buffering of P. expansum-driven acidification by the BCA increased the specific rate of PAT biosynthesis.

Treatment
buffering of P. expansum -driven acidification provided by the BCAe4
Interactor
P. expansumPenicillium expansume4pathogen
Outcome
specific rate of PAT biosynthesise4
Direction
increasese4

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗
Penicillium expansum
Penicillium expansum · InteractorH.J. Larsen, Bugwood.org · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e4

“the buffering of P. expansum -driven acidification provided by the BCA increases the specific rate of PAT biosynthesis”

✓ located verbatim in the source · abstract, characters 1960–2078 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

The antagonistic effect of the BCA greatly reduced the total amount of PAT in apples.

Treatment
the antagonistic effect provided by the BCAe4
Outcome
total amount of PATe4
Direction
greatly reducede4

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Malus domestica
Malus domestica · TaxonW.carter · CC0 · Wikimedia Commons ↗

Verbatim

e1

“In wounded apples”

✓ located verbatim in the source · abstract, characters 859–876 · show in text ↑
e4

“the antagonistic effect provided by the BCA greatly reduced the total amount of PAT”

✓ located verbatim in the source · abstract, characters 2210–2293 · show in text ↑

biocontrol · Penicillium expansum · Malus domestica (apple)Results agree

7 papers: 7 positive, 0 negative or no effect

6 papers in the same direction as this paper

  1. positive
  2. positive
  3. positive

3 papers more in this group

See all 7 papers →

biocontrol · disease · Malus domestica (apple)Results agree

16 papers: 16 positive, 0 negative or no effect

15 papers in the same direction as this paper

  1. positive
  2. positive
  3. positive

12 papers more in this group

See all 16 papers →

Claims are grouped by organism, treatment and what was measured or targeted. A paper counts as positive when any of its claims in the group is positive.