The role of gasotransmitters in movement of stomata: mechanisms of action and importance for plant immunity

Abstract

Stomatal guard cells are specialized epidermal cells regulating gas exchange. The ability to open or close in response to external and internal cues makes stomata a dynamic and fascinating system. Stomatal closure upon infection ensures restriction of pathogen entry into the plant and forms an essential component of innate immunity. The opening or closure of stomata is dependent on the turgidity or flaccidity of guard cells, respectively, facilitated by several signaling components, including reactive oxygen species, nitric oxide (NO) and Ca 2+ . Among these, NO is the most extensively studied gasotransmitter. Its pivotal role in stomatal closure by modulating various downstream components as well as regulation of crucial proteins by post-translational modifications makes NO an essential factor. Two more gasotransmitters, carbon monoxide and hydrogen sulfide, also trigger stomatal closure. Other gaseous molecules, like ethylene, methane, sulfur dioxide, ozone, and CO2, can modulate stomatal closure, but they are not considered strictly as gasotransmitters due to specific criteria. We review the signaling events in guard cells triggered by these gasotransmitters leading to stomatal closure. We point out the dual role of NO to promote stomatal closure and stomatal opening. Both NO and H2S help in reinforcing the innate immunity against pathogen attack. Although there is extensive information on the mechanism of NO action on stomata, the enzymatic source of NO or CO is still ambiguous. Similarly, research is warranted to establish the relative importance of and interactions among the three main gasotransmitters. Further studies on gasotransmitters would answer the ambiguity about their functions and confirm if they can act independently.

Abscisic Acid-Induced Stomatal Closure: An Important Component of Plant Defense Against Abiotic and Biotic Stress

“…In addition to NO, two more gaseous signaling molecules (gasotransmitters), hydrogen sulfide (H 2 S), and carbon monoxide (CO) produced within plant cells are an integral part of ABA-dependent stomatal closure as well as other stress conditions. These three gasotransmitters interacted with ABA-signaling during drought ( García-Mata and Lamattina, 2013 ; Yao et al, 2019 ; Gahir et al, 2020 ). Under abiotic stress, ABA could elevate the levels of NO as well as CO or H 2 S. For e.g., ABA activated heme oxygenase (HO), thereby increased CO levels and caused stomatal closure ( Cao et al, 2007 ; Wang and Liao, 2016 ).…”

“…Under abiotic stress, ABA could elevate the levels of NO as well as CO or H 2 S. For e.g., ABA activated heme oxygenase (HO), thereby increased CO levels and caused stomatal closure ( Cao et al, 2007 ; Wang and Liao, 2016 ). In turn, NO elevated the levels of H 2 S by regulating H 2 S producing enzymes (L/D-cysteine desulfhydrases) ( Kolupaev et al, 2019 ; Gahir et al, 2020 ). Similarly, CO promoted both NO and ROS synthesis, facilitating stomatal closure during abiotic stress ( Song et al, 2008 ; He and He, 2014 ).…”

“…NO produced in response to lipopolysaccharide contributed towards resistance against Pst DC3000 ( Melotto et al, 2006 ). The upregulation of H 2 S production suggested a strong association between H 2 S and plant defense ( Shi et al, 2015 ; Gahir et al, 2020 ). Further studies on these protective abilities of gasotransmitters to improve pathogen resistance could help achieve plants’ resilience.…”

“…Gasotransmitters exert their actions by mediating post-translational modifications (PTMs) such as S-nitrosylation, nitridation, and persulfidation of target proteins ( Scuffi et al, 2016 ; Kolupaev et al, 2019 ; Gahir et al, 2020 ). These PTMs seem to exert different effects.…”

“…Other compounds involved in ABA signaling, like phospholipase D and phosphatidic acid, were also associated with plants’ defense against pathogens ( Li and Wang, 2019 ; Moeder et al, 2019 ). The ability of H 2 S, a gasotransmitter, to impart resistance against typical plant pathogen ( Pseudomonas syringae ) suggests a link between stomatal closure and adaptation to plant pathogens ( Shi et al, 2015 ; Gahir et al, 2020 ). The promotion or inhibition of ROS and NO production by gasotransmitters can be a significant factor during plant defense.…”