Paper · 2025 · Nature Plants

Apoplastic metabolomics reveals sugars as mesophyll messengers regulating guard cell ion transport under red light

Yotam Zait; Mengmeng Zhu; Eigo Ando; et al.

9
claims
17
verbatim quotes
12
citations
1
research areas
✓
Open access · cc-by-nc-nd

Abstract

Guard cell pairs in the leaf epidermis enclose stomata, microscopic pores mediating CO2 uptake and water loss. Historical data suggest that signals from interior mesophyll tissue may modulate guard-cell regulation of stomatal apertures, but the molecular identity of any metabolite-based signals has remained elusive. We discovered that extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening. Our extensive metabolomics analyses identified 448 apoplastic metabolites; among these, both sugars (photosynthetic products) and maleic acid increased under red light and caused enhanced stomatal opening. Immunohistochemical assays demonstrated sucrose upregulation of H+-ATPase phosphorylation, indicating increased ATPase activity. Patch clamp assays revealed that sucrose inhibits slow anion currents, thus opposing anion efflux. These impacts occurred at sucrose concentrations matching those present endogenously under red light. These regulatory influences promote guard-cell solute import and retention, which drive stomatal opening. Our research thus addresses the decades-long question concerning the existence, identity and mechanistic impact of mesophyll messengers that coordinate photosynthesis with stomatal response. Guard cells define microscopic stomatal pores for CO2 uptake and water loss. Characterization of the extracellular metabolome revealed sugars as ‘mesophyll messengers’ from the leaf interior that enhance stomatal opening via regulation of the guard-cell H+-ATPase and anion channels.

Abstract from the paper’s OpenAlex record; open copy licensed cc-by-nc-nd. Read at the source ↗

The text the model read, with the source record’s inline markup (italics, sub- and superscripts) rendered and its character entities decoded; quote offsets refer to the raw text.

Claims 9

Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Apoplastic fluid from Arabidopsis thaliana enhances red-light-induced stomatal opening.

Taxon
Arabidopsis thalianaArabidopsis thalianae0
Treatment
extracellular (apoplastic) fluide0
Outcome
stomatal openinge0
Direction
enhancese0

Not reportedComparator

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”

✓ located verbatim in the source · abstract, characters 337–454 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Apoplastic fluid from Vicia faba enhances red-light-induced stomatal opening.

Taxon
Vicia fabaVicia fabae0
Treatment
extracellular (apoplastic) fluide0
Outcome
stomatal openinge0
Direction
enhancese0

Not reportedComparator

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

Vicia faba
Vicia faba · TaxonRahmaziz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”

✓ located verbatim in the source · abstract, characters 337–454 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Sugars and maleic acid increased in the apoplast under red light.

Taxon
Arabidopsis thalianaArabidopsis thalianae0
Treatment
red lighte1
Outcome
sugars (photosynthetic products) and maleic acide1
Direction
increasede1

Not reportedComparator

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e1

“among these, both sugars (photosynthetic products) and maleic acid increased under red light and caused enhanced stomatal opening”

✓ located verbatim in the source · abstract, characters 531–660 · show in text ↑
e0

“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”

✓ located verbatim in the source · abstract, characters 337–454 · show in text ↑
Mechanismobservedoriginal resultpositivemeasured

Claim · model-written summary

Sugars enhance stomatal opening.

Taxon
Arabidopsis thalianaArabidopsis thalianae0
Compound
sugarse1
Outcome
enhanced stomatal openinge1

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e1

“among these, both sugars (photosynthetic products) and maleic acid increased under red light and caused enhanced stomatal opening”

✓ located verbatim in the source · abstract, characters 531–660 · show in text ↑
e0

“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”

✓ located verbatim in the source · abstract, characters 337–454 · show in text ↑
Mechanismobservedoriginal resultpositivemeasured

Claim · model-written summary

Maleic acid enhances stomatal opening.

Taxon
Arabidopsis thalianaArabidopsis thalianae0
Compound
maleic acide1
Outcome
enhanced stomatal openinge1

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e1

“among these, both sugars (photosynthetic products) and maleic acid increased under red light and caused enhanced stomatal opening”

✓ located verbatim in the source · abstract, characters 531–660 · show in text ↑
e0

“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”

✓ located verbatim in the source · abstract, characters 337–454 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Sucrose upregulates H+-ATPase phosphorylation.

Taxon
Arabidopsis thalianaArabidopsis thalianae0
Treatment
sucrosee2
Gene
H+-ATPasee2
Outcome
H+-ATPase phosphorylatione2
Direction
upregulatione2

Not reportedComparator

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e2

“Immunohistochemical assays demonstrated sucrose upregulation of H+-ATPase phosphorylation”

✓ located verbatim in the source · abstract, characters 662–751 · show in text ↑
e0

“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”

✓ located verbatim in the source · abstract, characters 337–454 · show in text ↑
Intervention effectauthor interpretationoriginal resultpositivemeasured

Claim · model-written summary

Sucrose increases ATPase activity.

Taxon
Arabidopsis thalianaArabidopsis thalianae0
Treatment
sucrosee2
Outcome
ATPase activitye2
Direction
increasede2

Not reportedComparator

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e2

“Immunohistochemical assays demonstrated sucrose upregulation of H+-ATPase phosphorylation, indicating increased ATPase activity”

✓ located verbatim in the source · abstract, characters 662–789 · show in text ↑
e0

“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”

✓ located verbatim in the source · abstract, characters 337–454 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Sucrose inhibits slow anion currents at concentrations matching endogenous levels under red light.

Taxon
Arabidopsis thalianaArabidopsis thalianae0
Treatment
sucrosee3
Outcome
slow anion currentse3
Direction
inhibitse3
Qualifier
at sucrose concentrations matching those present endogenously under red lighte4

Not reportedComparator

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e3

“Patch clamp assays revealed that sucrose inhibits slow anion currents, thus opposing anion efflux”

✓ located verbatim in the source · abstract, characters 791–888 · show in text ↑
e4

“These impacts occurred at sucrose concentrations matching those present endogenously under red light”

✓ located verbatim in the source · abstract, characters 890–990 · show in text ↑
e0

“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”

✓ located verbatim in the source · abstract, characters 337–454 · show in text ↑
Mechanismauthor interpretationoriginal resultpositivebasis n/a

Claim · model-written summary

Sucrose-mediated regulation promotes guard-cell solute import and retention that drive stomatal opening.

Taxon
Arabidopsis thalianaArabidopsis thalianae0
Outcome
stomatal openinge5
Qualifier
guard-cell solute import and retentione5

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e5

“These regulatory influences promote guard-cell solute import and retention, which drive stomatal opening”

✓ located verbatim in the source · abstract, characters 992–1096 · show in text ↑
e0

“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”

✓ located verbatim in the source · abstract, characters 337–454 · show in text ↑

sucrose · molecular: metabolites · Arabidopsis thaliana (thale cress)Positive and negative results

5 papers: 2 positive, 3 negative or no effect

1 paper in the same direction as this paper · 3 in the opposite direction

  1. negative
  2. negative
  3. negative

1 paper more in this group

See all 5 papers →

sucrose · molecular: expression · Arabidopsis thaliana (thale cress)Positive and negative results

14 papers: 9 positive, 5 negative or no effect

8 papers in the same direction as this paper · 5 in the opposite direction

  1. negative
  2. negative
  3. negative

10 papers more in this group

See all 14 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.