Stomatal Immunity

Abstract

Stomata have long been assumed as passive portals of entry for pathogenic microorganisms, which may cause severe crop loss and food poisoning; however, accumulating evidence suggests that stomata have an important immune function. Plants actively close their stomata upon recognition of invading pathogens to stave off pathogenesis. Stomatal immunity starts from the perception of pathogen‐associated molecular patterns by surface‐localised pattern recognition receptors and activating a signalling cascade that requires plant hormones, reactive oxygen species (ROS) production, ion flux and gene expression to trigger stomatal closure. However, the arms race between plants and pathogens has driven the pathogenic microbes to constantly evolve new strategies and effector combinations as a countermeasure to manipulate stomatal movement for their own benefit. Changes in the guard cell metabolome, circadian clock regulating genes and climate‐related factors can impact plant defence through stomatal regulation. Understanding stomatal immunity has broad applications in combating pathogens, enhancing agricultural capacity and food safety.

Key Concepts

  • Active stomatal movement is tightly regulated by plants as a general mechanism of defence against biotic and abiotic stresses.
  • Guard cells recognise pathogen‐associated molecular patterns and trigger a signalling cascade rendering stomatal closure and a reduction of pathogen entry into the plant.
  • Different types of pathogens can subvert or take control of the plant immune responses and re‐open stomata for enhancing pathogenicity via toxins and/or effectors.
  • Changes in the guard cell metabolome, redox homeostasis, circadian clock regulating genes and climate‐related factors can impact plant defence through stomatal regulation.
  • Elucidating how stomata prioritise their responses to multiple biotic and abiotic signal inputs and the epistatic relationships between various signalling pathways in the guard cells will be a next important step in understanding the regulatory mechanism of stomatal immunity.

Keywords: climate change; microbial pathogens; PAMP recognition; signal transduction; stomatal immunity; food security and safety

Figure 1. Schematic diagram representing stomatal regulation. External or internal signals transduce via signal recognition by receptors. Signal perception triggers downstream signal transduction leading to stomatal movement including ROS and NO bursts, cytosolic Ca2+ increasement, signal transduction through mitogen‐activated protein kinases (MAPKs) and transcription factors (TFs) activation, and channel activation to manipulate turgor pressure. Gradient black arrows in the triangle indicate the signalling direction, and the curved arrow on the right side indicates positive feedback to amplify signals.
Figure 2. PAMPs‐induced stomatal closure and ‐induced downstream events in guard cells. (a) Bacterial PAMPs recognition and bacterial‐induced stomatal closure. After pattern‐associated molecular pattern (PAMP) recognition by pattern recognition receptor (PRR) in guard cell, stomatal pores are reduced actively. Hemibiotrophic pathogen, Pseudomonas syringae pv. tomato DC3000 (Pst); nonpathogenic strain Pseudomonas fluorescens A506 (Pfo); necrotrophic bacteria Pectobacterium carotovorum ssp. carotovorum (Pectobacterium); human pathogen, Escherichia coli O157:H7 (E. coli). (b) Downstream events after PAMPs recognition. A PAMP flg22 is perceived by FLS2. FLS2 interacts with BAK1 in flg22‐dependent manner. BIK1, a kind of receptor‐like cytoplasmic kinase (RLCK) associates with FLS and BAK1, respectively. As flg22 recognition, phosphorylated (p) BIK1 is released from PRR complex and phosphorylate RbohD leading to apoplastic H2O2 burst via superoxide dismutase (SOD). SA‐regulated cell wall peroxidases (PRXs) can also produce H2O2 from O2. Cytosolic increased H2O2 inhibits a proton pump H+‐ATPase (AHA1). PAMPs perception induces nitric oxide (NO) and Ca2+ influx. Cytosolic Ca2+ increasement with NO burst activates K+ efflux channel GORK, Cl efflux channel SLAC1, and inhibits AHA1 pump. (c) Hormonal signalling including ABA, SA and CK in stomatal immunity. ABA induces NO burst, CNGC2 activation for inward Ca2+ current, SLAC1 and RbohF phosphorylation by OST1. SA also induces NO burst, and together with CK, triggers H2O2 production by PRX33 and PRX34 via transcription factor ARR2 activation.
Figure 3. Circadian and flowering components involved in stomatal immunity. Mis‐regulation of CCA1 and LHY compromises PAMP‐triggered immunity (PTI) and effector‐triggered immunity (ETI) responses through circadian control of stomatal aperture. Flowering components are involved in stomatal opening. Increased FT level activates AHA1 activity resulting in stomatal opening.
Figure 4. Virulence factors overcoming stomatal immunity to re‐open stomata from closed stomata. Coronatine (COR) secreted from Pst, which is mimic bioactive jasmonate (JA), hijacks JA receptor COI1 to activate NAC TFs preventing SA biosynthesis. COR–COI1 complex is thought to inhibit ABA signalling (dotted line). Secreted effectors from Pst (T3S effectors) can inhibit PAMP‐induced H2O2, activate AHA1 through RIN4 phosphorylation. Fungal secreted cytokinin (CK) enhances ethylene accumulation leading to compromised ABA signalling. Fungal secreted oxalate inhibits ABA signalling and fusicoccin directly activates AHA1 leading to stomatal opening.
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Further Reading

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Kim, Dae Sung, and Liang, Yun‐Kuan(Dec 2019) Stomatal Immunity. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028342]