Paper · 2021 · Molecular Plant-Microbe Interactions

Not Just a Cycle: Three gab Genes Enable the Non-Cyclic Flux Toward Succinate via GABA Shunt in ‘Candidatus Liberibacter asiaticus’–Infected Citrus

Yasser Nehela; Nabil Killiny

10
claims
12
verbatim quotes
22
citations
4
research areas
✓
Open access · cc-by-nc-nd

Abstract

Although the mitochondria retain all required enzymes for an intact tricarboxylic acid (TCA) cycle, plants might shift the cyclic flux from the TCA cycle to an alternative noncyclic pathway via γ-aminobutyric acid (GABA) shunt under specific physiological conditions. We hypothesize that several genes may ease this noncyclic flux and contribute to the citrus response to the phytopathogenic bacterium ‘Candidatus Liberibacter asiaticus’, the causal agent of Huanglongbing in citrus. To test this hypothesis, we used multiomics techniques (metabolomics, fluxomics, and transcriptomics) to investigate the potential roles of putative gab homologies from Valencia sweet orange (Citrus sinensis). Our findings showed that ‘Ca. L. asiaticus’ significantly increased the endogenous GABA and succinate content but decreased ketoglutarate in infected citrus plants. Citrus genome harbors three putative gab genes, including amino-acid permease (also known as GABA permease; CsgabP), GABA transaminase (CsgabT), and succinate-semialdehyde dehydrogenase (also known as GABA dehydrogenase; CsgabD). The transcript levels of CsgabP, CsgabT, and CsgabD were upregulated in citrus leaves upon the infection with ‘Ca. L. asiaticus’ and after the exogenous application of GABA or deuterium-labeled GABA isotope (GABA-D 6 ). Moreover, our finding showed that exogenously applied GABA is quickly converted to succinate and fed into the TCA cycle. Likewise, the fluxomics study showed that GABA-D 6 is rapidly metabolized to succinate-D 4 . Our work proved that GABA shunt and three predicated gab genes from citrus, support the upstream noncyclic flux toward succinate rather than an intact TCA cycle and contribute to citrus defense responses to ‘Ca. L. asiaticus’. [Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

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Claims 10

Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

Infection increased endogenous GABA in citrus.

Taxon
citrus plantsCitruse0
Treatment
‘Ca. L. asiaticus’e0
Interactor
‘Ca. L. asiaticus’e0pathogen
Outcome
endogenous GABAe0
Direction
increasede0

Not reportedComparator

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“‘Ca. L. asiaticus’ significantly increased the endogenous GABA and succinate content but decreased ketoglutarate in infected citrus plants”

✓ located verbatim in the source · abstract, characters 719–857 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

Infection increased succinate in citrus.

Taxon
citrus plantsCitruse0
Treatment
‘Ca. L. asiaticus’e0
Interactor
‘Ca. L. asiaticus’e0pathogen
Outcome
succinate contente0
Direction
increasede0

Not reportedComparator

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“‘Ca. L. asiaticus’ significantly increased the endogenous GABA and succinate content but decreased ketoglutarate in infected citrus plants”

✓ located verbatim in the source · abstract, characters 719–857 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Infection decreased ketoglutarate in citrus.

Taxon
citrus plantsCitruse0
Treatment
‘Ca. L. asiaticus’e0
Interactor
‘Ca. L. asiaticus’e0pathogen
Outcome
ketoglutaratee0
Direction
decreasede0

Not reportedComparator

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“‘Ca. L. asiaticus’ significantly increased the endogenous GABA and succinate content but decreased ketoglutarate in infected citrus plants”

✓ located verbatim in the source · abstract, characters 719–857 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The citrus genome contained three putative gab genes.

Taxon
CitrusCitruse0
Gene
CsgabPe0
Outcome
three putative gab genese0
Value
threee0

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Citrus genome harbors three putative gab genes, including amino-acid permease (also known as GABA permease; CsgabP), GABA transaminase (CsgabT), and succinate-semialdehyde dehydrogenase (also known as GABA dehydrogenase; CsgabD)”

✓ located verbatim in the source · abstract, characters 859–1087 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Infection upregulated CsgabP, CsgabT and CsgabD transcripts in citrus leaves.

Taxon
citrusCitruse0
Organ / stage
leavese0
Treatment
infection with ‘Ca. L. asiaticus’e0
Interactor
‘Ca. L. asiaticus’e0pathogen
Gene
CsgabP, CsgabT, and CsgabDe0
Outcome
transcript levelse0
Direction
upregulatede0

Not reportedComparator

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The transcript levels of CsgabP, CsgabT, and CsgabD were upregulated in citrus leaves upon the infection with ‘Ca. L. asiaticus’”

✓ located verbatim in the source · abstract, characters 1089–1217 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Applied GABA upregulated the three gab transcripts in citrus leaves.

Taxon
citrusCitruse0
Treatment
exogenous application of GABAe0
Gene
CsgabP, CsgabT, and CsgabDe0
Outcome
transcript levelse0
Direction
upregulatede0

Not reportedComparator

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The transcript levels of CsgabP, CsgabT, and CsgabD were upregulated in citrus leaves upon the infection with ‘Ca. L. asiaticus’ and after the exogenous application of GABA or deuterium-labeled GABA isotope (GABA-D 6 )”

✓ located verbatim in the source · abstract, characters 1089–1307 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Applied GABA-D 6 upregulated the three gab transcripts in citrus leaves.

Taxon
citrusCitruse0
Treatment
deuterium-labeled GABA isotope (GABA-D 6 )e0
Gene
CsgabP, CsgabT, and CsgabDe0
Outcome
transcript levelse0
Direction
upregulatede0

Not reportedComparator

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The transcript levels of CsgabP, CsgabT, and CsgabD were upregulated in citrus leaves upon the infection with ‘Ca. L. asiaticus’ and after the exogenous application of GABA or deuterium-labeled GABA isotope (GABA-D 6 )”

✓ located verbatim in the source · abstract, characters 1089–1307 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Applied GABA was rapidly converted to succinate and entered the TCA cycle.

Taxon
citrusCitrust0
Treatment
exogenously applied GABAe0
Outcome
converted to succinate and fed into the TCA cyclee0

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“exogenously applied GABA is quickly converted to succinate and fed into the TCA cycle”

✓ located verbatim in the source · abstract, characters 1343–1428 · show in text ↑
t0

“Citrus”

✓ located verbatim in the source · title, characters 141–147 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

GABA-D 6 was rapidly metabolized to succinate-D 4.

Taxon
citrusCitrust0
Outcome
metabolized to succinate-D 4e0

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“GABA-D 6 is rapidly metabolized to succinate-D 4”

✓ located verbatim in the source · abstract, characters 1472–1520 · show in text ↑
t0

“Citrus”

✓ located verbatim in the source · title, characters 141–147 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors concluded that the GABA shunt and three gab genes support noncyclic succinate flux and citrus defense.

Taxon
citrusCitruse0
Interactor
‘Ca. L. asiaticus’e0pathogen
Gene
three predicated gab genese0
Outcome
upstream noncyclic flux toward succinatee0

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

Citrus
Citrus · Taxon · picture of the genus (one of its species)Ellen Levy Finch ( Elf ) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“GABA shunt and three predicated gab genes from citrus, support the upstream noncyclic flux toward succinate rather than an intact TCA cycle and contribute to citrus defense responses to ‘Ca. L. asiaticus’”

✓ located verbatim in the source · abstract, characters 1544–1748 · show in text ↑

calcium atom · molecular: metabolites · CitrusPositive and negative results

4 papers: 3 positive, 1 negative or no effect

2 papers in the same direction as this paper · 1 in the opposite direction

  1. no effect
  2. positive
  3. positive
See all 4 papers →

calcium atom · molecular: expression · CitrusResults agree

2 papers: 2 positive, 0 negative or no effect

1 paper in the same direction as this paper

  1. positive
See all 2 papers →

infection · molecular: expression · CitrusPositive and negative results

6 papers: 4 positive, 2 negative or no effect

3 papers in the same direction as this paper · 2 in the opposite direction

  1. negative
  2. negative
  3. positive

2 papers more in this group

See all 6 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.