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.
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Claims 9
Claim · model-written summary
Apoplastic fluid from Arabidopsis thaliana enhances red-light-induced stomatal opening.
- Taxon
- Arabidopsis thaliana
Arabidopsis 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.

Verbatim
e0“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”
Claim · model-written summary
Apoplastic fluid from Vicia faba enhances red-light-induced stomatal opening.
- Taxon
- Vicia faba
Vicia 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.

Verbatim
e0“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”
Claim · model-written summary
Sugars and maleic acid increased in the apoplast under red light.
- Taxon
- Arabidopsis thaliana
Arabidopsis 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.

Verbatim
e1“among these, both sugars (photosynthetic products) and maleic acid increased under red light and caused enhanced stomatal opening”
e0“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”
Claim · model-written summary
Sugars enhance stomatal opening.
- Taxon
- Arabidopsis thaliana
Arabidopsis thalianae0 - Compound
- sugarse1
- Outcome
- enhanced stomatal openinge1
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e1“among these, both sugars (photosynthetic products) and maleic acid increased under red light and caused enhanced stomatal opening”
e0“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”
Claim · model-written summary
Maleic acid enhances stomatal opening.
- Taxon
- Arabidopsis thaliana
Arabidopsis thalianae0 - Compound
- maleic acide1
- Outcome
- enhanced stomatal openinge1
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e1“among these, both sugars (photosynthetic products) and maleic acid increased under red light and caused enhanced stomatal opening”
e0“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”
Claim · model-written summary
Sucrose upregulates H+-ATPase phosphorylation.
- Taxon
- Arabidopsis thaliana
Arabidopsis 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.

Verbatim
e2“Immunohistochemical assays demonstrated sucrose upregulation of H+-ATPase phosphorylation”
e0“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”
Claim · model-written summary
Sucrose increases ATPase activity.
- Taxon
- Arabidopsis thaliana
Arabidopsis thalianae0 - Treatment
- sucrosee2
- Outcome
- ATPase activitye2
- Direction
- increasede2
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e2“Immunohistochemical assays demonstrated sucrose upregulation of H+-ATPase phosphorylation, indicating increased ATPase activity”
e0“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”
Claim · model-written summary
Sucrose inhibits slow anion currents at concentrations matching endogenous levels under red light.
- Taxon
- Arabidopsis thaliana
Arabidopsis 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.

Verbatim
e3“Patch clamp assays revealed that sucrose inhibits slow anion currents, thus opposing anion efflux”
e4“These impacts occurred at sucrose concentrations matching those present endogenously under red light”
e0“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”
Claim · model-written summary
Sucrose-mediated regulation promotes guard-cell solute import and retention that drive stomatal opening.
- Taxon
- Arabidopsis thaliana
Arabidopsis thalianae0 - Outcome
- stomatal openinge5
- Qualifier
- guard-cell solute import and retentione5
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e5“These regulatory influences promote guard-cell solute import and retention, which drive stomatal opening”
e0“extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening”
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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.