Under salt stress guard cells rewire ion transport and abscisic acid signaling

Abstract

Plant productivity depends on optimal water-use efficiency and photosynthetic capacity balanced by stomatal conductance. Whether and how stomatal behavior contributes to salt sensitivity or tolerance is currently unknown. This work identifies guard cell-specific signaling networks exerted by a salt-sensitive and salt-tolerant plant under ionic and osmotic stress conditions accompanied with increasing NaCl loads.  We challenged soil grown Arabidopsis thaliana and Thellungiella salsuginea plants with shortand long-term salinity stress and monitored genome-wide gene expression and signals of guard cells that determine their function.  Arabidopsis plants suffered from both salt regimes and showed reduced stomatal conductance while Thellungiella displayed no obvious stress symptoms. The salt-dependent gene expression changes of guard cells supported the ability of the halophyte to maintain high potassium to sodium ratios and to attenuate the ABA signaling pathway which the glycophyte kept activated despite fading ABA levels.  Our study shows that salinity stress and even the different tolerance levels are manifested on a single cell level. Halophytic guard cells react less sensitive than glycophytic guard cells providing opportunities to manipulate stomatal behavior and improve plant productivity.

Tobacco leaf tissue rapidly detoxifies direct salt loads without activation of calcium and SOS signaling

“…Subsequent extraction and chromatographic separation of plant material was carried out as described (Stingl et al ., 2013), using 5 ng of (D6)‐ABA as internal standard. Abscisic acid content was analyzed by ultrahigh‐performance liquid chromatography electrospray ionization tandem mass spectrometry (UHPLC‐ESI–MS/MS) using a Waters Acquity I‐Class UHPLC system (Milford, MA, USA) coupled to an AB Sciex 6500+ QTRAP ® tandem mass spectrometer (AB Sciex, Framingham, MA, USA), operated in the negative ionization mode as previously described (Karimi et al ., 2021).…”

Abscisic acid facilitates phosphate acquisition through the transcription factor ABA INSENSITIVE5 in Arabidopsis

“…Abscisic acid (ABA) is a major stress phytohormone that modulates plant responses to various adverse environmental stimuli (Karimi et al., 2021; Wang et al., 2020; Zhu, 2016; Zhu et al., 2020). When perceived by PYRABACTIN RESISTANCE1/PYR1‐LIKE/REGULATORY COMPONENTS OF ABA RECEPTOR (PYR/PYL/RCAR), increased ABA accumulation can relieve protein phosphatase 2C‐mediated inhibition of downstream protein kinases, such as the Snf1‐related kinases 2 (SnRK2s), leading to the phosphorylation of transcription factors and altered expression of stress‐responsive genes (Raghavendra et al., 2010; Wang et al., 2018; Zhao et al., 2020).…”

Functional Crypto-Adenylate Cyclases Operate in Complex Plant Proteins

“…Meanwhile, in the guard cell, cAMP has long been shown to be involved in ABA-mediated K + efflux through outward-rectifying channels, such as AtGORK ( Jin and Wu, 1999 ; Lemtiri-Chlieh and Berkowitz, 2004 ). Salt stress increases cellular ABA but reduces K + levels through the combined downregulation of guard cell-specific K + influx channel AtKAT2 and upregulation of guard cell-specific K + efflux channel AtGORK genes, thus leading to stomatal closure ( Ache et al, 2000 ; Karimi et al, 2021 ). Since AtNCED3 is annotated as “response to osmotic stress” and “hyperosmotic salinity response” and “response to water deprivation” ( Sato et al, 2018 ; Kalladan et al, 2019 ), it is conceivable that during salt stress, this gene is upregulated resulting in increased ABA and cAMP levels; the latter could then mediate ABA signaling through, e.g., the activation of ion channels.…”

“…Indeed, CNGC12 is strongly induced by salt stress in guard cells and the resulting Ca 2+ influx activated S-type anion channels to cause stomatal closure ( Dietrich et al, 2020 ). Additionally, the intracellular ABA signaling cascades of Arabidopsis thaliana beginning from the intracellular ABA receptors PYL5 and PYL6, type 2C protein phosphatases PP2C ( Zhang et al, 2014 ), to the Ca 2+ -independent and Ca 2+ -dependent protein kinases SnRK2.9 and SnRK3/CIPK, were all upregulated in guard cells during salt stress ( Karimi et al, 2021 ).…”