The SLAC1 Anion Channel

Abstract

The balance between CO2 uptake for photosynthesis and water loss through transpiration determines plant growth and productivity. Guard cells form stomatal pores in plant epidermis that adjust this balance via volume changes that control stomatal aperture. Guard cell volume is regulated by fluxes of ions and water across the membrane via various ion channels. The slow anion channel 1 (SLAC1) is essential for efficient stomatal regulation, as it is the major mediator of the efflux of anions from guard cells during stomatal closure. The activation of SLAC1 requires phosphorylation and is the end point of signalling pathways initiated by abiotic and biotic triggers that cause stomata to close, such as the phytohormone abscisic acid, elevated CO2 levels, darkness, low air humidity, ozone; and pathogen and damage‐associated molecular patterns and hormones. SLAC1 is conserved in evolution, but SLACs in different plant groups have different mechanisms of regulation.

Key Concepts

  • SLAC1 is the major guard cell slow‐type anion channel that needs to be activated by phosphorylation in the N‐ and C‐terminal regions for stomatal closure in response to endogenous and environmental stimuli.
  • The plant hormone abscisic acid (ABA) triggers SLAC1 activation through a signalling pathway that involves ABA receptors and PP2C phosphatases, which regulate the Ca2+‐independent kinase OST1 and several Ca2+‐dependent protein kinases that phosphorylate SLAC1. The same pathway is involved in SLAC1 activation in response to darkness, CO2, ozone and low air humidity.
  • Elevated CO2 activates SLAC1 via bicarbonate, which directly enhances ion channel activity. The Raf‐type kinase HT1 and mitogen‐activated protein kinases MPK12 and MPK4 regulate SLAC1 activation in response to CO2, but not ABA, contributing to a CO2‐specific branch of SLAC1 activation.
  • Pathogen‐associated molecules trigger the activation of SLAC1 and its homologue SLAH3 that contributes to guard cell anion currents. SLAH3 is the key anion channel in stomatal response to fungal chitin, whereas SLAC1, SLAH3 and OST1 contribute to bacterial flagellin‐induced stomatal closure.
  • SLAC1 and OST1 are conserved in early land plants, such as mosses, lycophytes and ferns, but their role in these plants needs further study. The regulation of SLAC1 anion channel differs among plant groups – for example, the monocot SLACs, unlike Arabidopsis SLAC1, require external nitrate for activation.

Keywords: ion channel regulation; guard cell signalling; stomatal closure; ABA signalling; CO2 signalling; pathogen responses; ion channel evolution

Figure 1. The structure of the SLAC1 anion channel. (a) SLAC1 channel is a trimer, where the pore of each protomer is gated by a phenylalanine residue (Phe 450). The channel conducts nitrate and chloride ions. (b) SLAC1 protomer has 10 transmembrane helical domains (TM1‐10) and cytoplasmic N‐ and C‐ terminal domains, which contain phosphorylation sites indicated in pink. Amino acids involved in CO2‐induced activation of the channel are indicated in blue and the gating residue in orange.
Figure 2. SLAC1 activation in response to abiotic stimuli. ABA is the key regulator of SLAC1 activation. ABA is perceived by its receptors, which, together with ABA, form a complex with the PP2C phosphatases, suppressing their activity. Thereafter, downstream calcium‐dependent (CPKs and CIPK/CBL complexes) and calcium‐independent (OST1) SLAC1‐activating kinases can phosphorylate SLAC1, leading to channel activation, anion efflux and stomatal closure. Various triggers, such as low air humidity (high VPD), darkness, elevated CO2 and ozone also feed into the ABA signalling pathway. CO2 signalling is mediated by bicarbonate formed with the help of carbonic β‐anhydrases βCA1 and βCA4. Elevated CO2 levels lead to the activation of the mitogen‐activated protein kinases MPK12 and MPK4, which inhibit the activity of the HT1 kinase. This enables the activation of SLAC1 by OST1 and through GHR1, which is suppressed by HT1 at ambient CO2 levels. Dashed lines indicate unclear mechanisms, which may involve multiple steps, black lines indicate known interactions and grey lines indicate interactions that are suppressed upon stimulus‐activated signalling.
Figure 3. SLAC1 and SLAH3 activation in response to biotic stimuli. The guard cell anion channels SLAC1 and SLAH3 are activated in response to damage‐ and pathogen‐associated molecules (DAMPs and PAMPs). The DAMP Pep1 is perceived by the PEPR1‐BAK1 receptor complex that trasmits the signal to the BIK1 kinase which leads to downstream activation of SLAC1 and SLAH3. The fungal PAMP chitin is perceived by the CERK1‐LYK5 receptor complex, which leads to the activation of the kinase PBL27 that activates SLAH3 by phosphorylation. The bacterial PAMP flg22 is perceived by the FLS2‐BAK1 receptor complex, which leads to SLAC1 activation through the OST1 kinase. Calcium‐dependent kinases CPK3 and CPK6 are involved in SLAC1 and SLAH3 activation in response to hormones that mediate responses to biotic stress, salicylic acid (SA) and jasmonic acid (JA). Dashed lines indicate unclear mechanisms, which may involve multiple steps, black lines indicate known interactions.
Figure 4. SLAC1 in green plant evolution. SLAC1 arose early in green plant evolution before the origin of stomata and is present in all land plants from charophyte green algae to angiosperms. SLAC1 regulation differs between plant groups, with the notable trait of nitrate‐dependent gating evolved in monocots.
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Further Reading

Assmann SM and Jegla T (2016) Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2. Current Opinion in Plant Biology 33: 157–167.

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Jezek M and Blatt MR (2017) The membrane transport system of the guard cell and its integration for stomatal dynamics. Plant Physiology 174: 487–519.

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Saito S and Uozumi N (2019) Guard cell membrane anion transport systems and their regulatory components: an elaborate mechanism controlling stress‐induced stomatal closure. Plants 8: 9.

Sussmilch FC, Schultz J, Hedrich R and Roelfsema MRG (2019) Acquiring control: the evolution of stomatal signalling pathways. Trends in Plant Science 24: 342–351.

Zhang J, De‐oliveira‐Ceciliato P, Takahashi Y, et al. (2018) Insights into the molecular mechanisms of CO2‐mediated regulation of stomatal movements. Current Biology 28: R1356–R1363.

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How to Cite close
Hõrak, Hanna(Mar 2020) The SLAC1 Anion Channel. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0027951]