H 2 O 2 , Ca 2+ , and K + in subsidiary cells of maize leaves are involved in regulatory signaling of stomatal movement

Mapping Intimacies ◽

10.21203/rs.2.15366/v1 ◽

2019 ◽

Author(s):

Li Zhang ◽

Yaqin Yao ◽

Suiqi Zhang

Keyword(s):

Zea Mays ◽

Stomatal Closure ◽

Guard Cells ◽

Stomatal Movement ◽

Diphenylene Iodonium ◽

Maize Leaves ◽

Subsidiary Cells

Abstract Background : The stomata of maize ( Zea mays ) contain a pair of guard cells and a pair of subsidiary cells. To determine whether H 2 O 2 , Ca 2+ , and K + in subsidiary cells were involved in stomatal movement, we treated four-week-old maize (Zhengdan 958) leaves with H 2 O 2 , diphenylene iodonium (DPI), CaCl 2 , and LaCl 3 . Changes in content and distribution of H 2 O 2 , Ca 2+ , and K + during stomatal movement were observed. Results : When exogenous H 2 O 2 was applied, Ca 2+ increased and K + decreased in guard cells, while both ions increased in subsidiary cells, leading to stomatal closure. After DPI treatment, Ca 2+ decreased and K + increased in guard cells, but both Ca 2+ and K + decreased in subsidiary cells, resulting in open stomata. Exogenous CaCl 2 increased H 2 O 2 and reduced K + in guard cells, while significantly increasing them in subsidiary cells and causing stomatal closure. After LaCl 3 treatment, decreased and K + increased in guard cells, whereas both H 2 O 2 and K + decreased in subsidiary cells and stomata became open. Conclusions : These results indicated that H 2 O 2 and Ca 2+ were correlated positively with each other and with K + in subsidiary cells during stomatal movement. Both H 2 O 2 and Ca 2+ in subsidiary cells promote an inflow of K + , indirectly regulating stomatal closure.

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Stomatal movement in Zea mays: Shuttle of potassium and chloride between guard cells and subsidiary cells

Planta ◽

10.1007/bf00398116 ◽

1971 ◽

Vol 101 (4) ◽

pp. 296-316 ◽

Cited By ~ 141

Author(s):

Klaus Raschke ◽

Margaret Pierce Fellows

Keyword(s):

Zea Mays ◽

Guard Cells ◽

Stomatal Movement ◽

Subsidiary Cells

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Hydrogen sulfide induced by hydrogen peroxide mediates darkness-induced stomatal closure in Arabidopsis thaliana

10.21203/rs.2.14712/v2 ◽

2019 ◽

Author(s):

Yinli Ma ◽

Luhan Shao ◽

Jiao Niu

Keyword(s):

Hydrogen Peroxide ◽

Arabidopsis Thaliana ◽

Hydrogen Sulfide ◽

Stomatal Closure ◽

Guard Cells ◽

Stomatal Movement ◽

Wild Type ◽

Salicylhydroxamic Acid ◽

Diphenylene Iodonium ◽

Cysteine Desulfhydrase

Abstract Background Whether stomatal movement by darkness in Arabidopsis thaliana is mediated by hydrogen sulfide (H2S) is undiscovered yet, so the interaction between hydrogen peroxide (H2O2) and H2S in the process needs to be elucidated. Results Our results indicated that H2S modulators aminooxy acetic acid (AOA), potassium pyruvate (N3H3KO3) + ammonia (NH3), hydroxylamine (NH2OH), and hypotaurine (HT) inhibited darkness-induced stomatal closure, H2S generation and L-/D-cysteine desulfhydrase (L-/D-CDes) activity increased in wild-type A. thaliana leaves. Darkness induced stomatal closure in wild-type plants, but failed in Atl-cdes and Atd-cdes mutants. Additionally, both L-/D-CDes activity and H2S content were significantly decreased after applying H2O2 modulators salicylhydroxamic acid (SHAM), ascorbic acid (ASA), diphenylene iodonium (DPI), and catalase (CAT) in darkness, but there was almost no effects on H2O2 levels in the presence of AOA, C3H3KO3+NH3, NH2OH, and HT of wild-type plants in darkness. Moreover, darkness couldn't increase H2S content and L-/D-CDes activity of AtrbohF and AtrbohD/F mutants leaves, but increased H2O2 levels in Atl-cdes and Atd-cdes guard cells. Conclusions We observed that L-/D-CDes-generated H2S mediates stomatal closure by darkness, and functions downstream of H2O2 in A. thaliana.

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Downregulating VAC14 in Guard Cells Causes Drought Hypersensitivity by Inhibiting Stomatal Closure

Frontiers in Plant Science ◽

10.3389/fpls.2020.602701 ◽

2020 ◽

Vol 11 ◽

Author(s):

Zong-Qi Wang ◽

Qi Liu ◽

Ju-Hua Wu ◽

Juan Li ◽

Jun-Min He ◽

...

Keyword(s):

Stomatal Closure ◽

Guard Cells ◽

Land Plant ◽

Scaffolding Protein ◽

Stomatal Movement ◽

Wild Type ◽

Physiological Factors ◽

Surrounding Environment ◽

Intracellular Activities

Stomata are a key land plant innovation that permit the regulation of gaseous exchanges between the plant interior and the surrounding environment. By opening or closing, stomata regulate transpiration of water though the plant; and these actions are coordinated with acquisition of CO2 for photosynthesis. Stomatal movement is controlled by various environmental and physiological factors and associates with multiple intracellular activities, among which the dynamic remodeling of vacuoles plays a crucial role. Phosphatidylinositol 3,5-bisphosphate [PI(3,5)P2] is critical for dynamic remodeling of vacuoles. Its production requires a PI(3,5)P2-metabolizing complex consisting of FAB1/PIKfyve kinases, SAC phosphatases, and the scaffolding protein VAC14. Although genetic or pharmacological downregulation of PI(3,5)P2 causes hyposensitivity to ABA-induced stomatal closure, whether the effect of PI(3,5)P2 on stomatal movement is cell-autonomous and the physiological consequences of its reduction were unclear. We report that downregulating Arabidopsis VAC14 specifically in guard cells by artificial microRNAs (amiR-VAC14) results in enlarged guard cells and hyposensitivity to ABA- and dark-induced stomatal closure. Vacuolar fission during stomatal closure is compromised by downregulating VAC14 in guard cells. Exogenous application of PI(3,5)P2 rescued the amiR-VAC14 phenotype whereas PI(3,5)P2 inhibitor YM201636 caused wild-type plants to have inhibited stomatal closure. We further show that downregulating VAC14 specifically in guard cells impairs drought tolerance, suggestive of a key role of guard cell-produced PI(3,5)P2 in plant fitness.

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Hydrogen sulfide may function downstream of hydrogen peroxide in salt stress-induced stomatal closure in Vicia faba

Functional Plant Biology ◽

10.1071/fp18096 ◽

2019 ◽

Vol 46 (2) ◽

pp. 136 ◽

Cited By ~ 7

Author(s):

Yinli Ma ◽

Wei Zhang ◽

Jiao Niu ◽

Yu Ren ◽

Fan Zhang

Keyword(s):

Hydrogen Peroxide ◽

Hydrogen Sulfide ◽

Salt Stress ◽

Vicia Faba ◽

Laser Scanning ◽

Stomatal Closure ◽

Guard Cells ◽

H2o2 Production ◽

Diphenylene Iodonium ◽

Cysteine Desulfhydrase

The roles of hydrogen sulfide (H2S) and hydrogen peroxide (H2O2) in signalling transduction of stomatal closure induced by salt stress were examined by using pharmacological, spectrophotographic and laser scanning confocal microscopic (LSCM) approaches in Vicia faba L. Salt stress resulted in stomatal closure, and this effect was blocked by H2S modulators hypotaurine (HT), aminooxy acetic acid (AOA), hydroxylamine (NH2OH), potassium pyruvate (C3H3KO3) and ammonia (NH3) and H2O2 modulators ascorbic acid (ASA), catalase (CAT), diphenylene iodonium (DPI). Additionally, salt stress induced H2S generation and increased L-/D-cysteine desulfhydrase (L-/D-CDes, pyridoxalphosphate-dependent enzyme) activity in leaves, and caused H2O2 production in guard cells, and these effects were significantly suppressed by H2S modulators and H2O2 modulators respectively. Moreover, H2O2 modulators suppressed salt stress-induced increase of H2S levels and L-/D-CDes activity in leaves as well as stomatal closure of V. faba. However, H2S modulators had no effects on salt stress-induced H2O2 production in guard cells. Altogether, our data suggested that H2S and H2O2 probably are involved in salt stress-induced stomatal closure, and H2S may function downstream of H2O2 in salt stress-induced stomatal movement in V. faba.

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Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum

Functional Plant Biology ◽

10.1071/fp04035 ◽

2004 ◽

Vol 31 (9) ◽

pp. 913 ◽

Cited By ~ 84

Author(s):

Radhika Desikan ◽

Man-Kim Cheung ◽

Andrew Clarke ◽

Sarah Golding ◽

Moshe Sagi ◽

...

Keyword(s):

Hydrogen Peroxide ◽

Pisum Sativum ◽

Nadph Oxidase ◽

Stomatal Closure ◽

Guard Cells ◽

Dependent Manner ◽

Degenerate Oligonucleotide ◽

Diphenylene Iodonium ◽

Common Signal ◽

Respiratory Burst Oxidase

The requirement for hydrogen peroxide (H2O2) generation and action during stomatal closure induced by darkness and abscisic acid (ABA) was investigated in pea (Pisum sativum L.). Stomatal closure induced by darkness or ABA was inhibited by the H2O2-scavenging enzyme catalase or the antioxidant N-acetyl cysteine (NAC), or by diphenylene iodonium (DPI), an inhibitor of the H2O2-generating enzyme NADPH oxidase. Exogenous H2O2 induced stomatal closure in a dose- and time-dependent manner, and H2O2 was also required for ABA-inhibition of stomatal opening in the light. H2O2 accumulation in guard cells was increased by darkness or ABA, as assessed with the fluorescent dye dichlorodihydrofluorescein diacetate (H2-DCFDA) and confocal microscopy. Such increases were inhibited by catalase, NAC or DPI, consistent with the effects of these compounds on stomatal apertures. Employing polymerase chain reaction (PCR) with degenerate oligonucleotide primers, several NADPH oxidase homologues were identified from pea genomic DNA that had substantial identity to the Arabidopsis thaliana (L.) Heynh. rboh (respiratory burst oxidase homologue) genes. Furthermore, an antibody raised against the tomato rboh identified immunoreactive proteins in epidermal, mesophyll and guard cells.

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Regulation of stomatal movement and photosynthetic activity in guard cells of tomato abaxial epidermal peels by salicylic acid

Functional Plant Biology ◽

10.1071/fp12187 ◽

2012 ◽

Vol 39 (12) ◽

pp. 1028 ◽

Cited By ~ 16

Author(s):

Péter Poór ◽

Irma Tari

Keyword(s):

Salicylic Acid ◽

Stomatal Closure ◽

Control Level ◽

Guard Cells ◽

Quantum Yields ◽

Photochemical Quenching ◽

Stomatal Movement ◽

Signalling Molecule ◽

Psii Photochemistry ◽

Plant Pathogen Interactions

Salicylic acid (SA), a signalling molecule in plant–pathogen interactions induces stomatal closure in intact leaves and it has a direct control over stomatal movement by increasing the levels of reactive oxygen species (ROS) and nitric oxide (NO) in guard cells (GC). Stomatal closure on the abaxial epidermal peels of tomato leaves was induced at 10−7 and 10−3 M SA but stomata remained open at 10−4 M. At concentrations that reduced stomatal aperture, the ROS and NO levels were raised. The accumulation of ROS and NO could be prevented by specific scavengers, which were effective inhibitors of the SA-induced stomatal closure. In contrast with other plant species, the guard cells (GCs) of tomato did not show a long-lasting accumulation of ROS in the presence of 10−4 M SA and their NO content decreased to below the control level, leading to stomatal opening. Increasing SA concentrations resulted in a significant decrease in the maximum and effective quantum yields of PSII photochemistry and in the photochemical quenching parameter of GCs. In the presence of 10−7 and 10−4 M SA, the chloroplasts of GCs sustained a higher electron transport rate than in the presence of 10−3 M, suggesting that the SA-induced inhibition of GC photosynthesis may affect stomatal closure at high SA concentrations.

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Inhibition of abscisic acid-induced stomatal closure by ethylene is related to the change of hydrogen peroxide levels in guard cells in broad bean

Australian Journal of Botany ◽

10.1071/bt11144 ◽

2011 ◽

Vol 59 (8) ◽

pp. 781 ◽

Cited By ~ 3

Author(s):

XiGui Song ◽

XiaoPing She ◽

Juan Wang

Keyword(s):

Hydrogen Peroxide ◽

Ascorbic Acid ◽

Abscisic Acid ◽

Nadph Oxidase ◽

Broad Bean ◽

Stomatal Closure ◽

Guard Cells ◽

Diphenylene Iodonium ◽

Scavenging Enzymes ◽

Exogenous H2o2

We analysed the role and relationship between hydrogen peroxide (H2O2) reduction and the inhibition of abscisic acid (ABA)-induced stomatal closure by ethylene. Like ascorbic acid (ASA), the most important reducing substrate for H2O2 removal, catalase, one of the H2O2 scavenging enzymes and diphenylene iodonium, an inhibitor of the H2O2-generating enzyme NADPH oxidase, both ethylene-releasing compound 2-chloroethylene phosphonic acid (ethephon, ETH) and 1-aminocyclopropane-1-carboxylic acid (ACC), the immediate precursor of ethylene, were found to inhibit stomatal closure by ABA and to reduce H2O2 levels by ABA in guard cells, indicating that ethylene-caused inhibition of ABA-induced stomatal closure involves reduction of H2O2 levels in guard cells. Additionally, similar to ASA and catalase, ACC/ETH not only suppressed H2O2-induced stomatal closure and H2O2 levels in guard cells treated with exogenous H2O2 in light, but also reopened the stomata which had been closed by ABA and reduced H2O2 levels that had been generated by ABA. The abovementioned effects of ACC and ETH were dissimilar to that of diphenylene iodonium, an inhibitor of the H2O2-generating enzyme NADPH oxidase, which not only had incapability to reduce H2O2 levels by exogenous H2O2 but also could not abolish H2O2 that had been generated by ABA. So we suggest that ethylene probably induces H2O2 removal and reduces H2O2 levels in Vicia faba guard cells, and finally inhibits stomatal closure induced by ABA.

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Role and interrelationship of PTPases and H2O2 in light/dark-regulated stomatal movement in Vicia faba

Australian Journal of Botany ◽

10.1071/bt09017 ◽

2009 ◽

Vol 57 (6) ◽

pp. 486 ◽

Cited By ~ 1

Author(s):

Yuanhua Zhang ◽

Xiaoping She ◽

Guangbin Zhang

Keyword(s):

Vicia Faba ◽

Laser Scanning ◽

Stomatal Closure ◽

Specific Inhibitor ◽

Guard Cells ◽

Stomatal Aperture ◽

Stomatal Movement ◽

Obvious Effect ◽

Exogenous H2o2 ◽

Ptpase Activity

Role and interrelationship of protein tyrosine phosphatases (PTPases) and H2O2 in light/dark-regulated stomatal movement in Vicia faba were investigated by epidermal strip bioassay, laser-scanning confocal microscopy and assays of PTPase activity. Our results indicate that phenylarsine oxide (PAO), a specific inhibitor of PTPases, ascorbic acid (ASA), an important reducing substrate for H2O2 removal, and catalase (CAT), one of the H2O2 scavenging enzymes, did not cause any change of stomatal aperture in light, but remarkably prevented dark-induced stomatal closure. Exogenous H2O2 had no obvious effect on stomatal aperture in the dark, but significantly induced stomatal closure in light. Both PTPase activity in epidermal strips and endogenous H2O2 level in guard cells in the dark were higher than those in light. The results showed that both PTPases and H2O2 mediate light/dark-regulated stomatal movement, that dark-induced stomatal closure requires the activation of PTPases and the enhancement of H2O2 levels in guard cells, and stomatal opening caused by light is associated with the inactivation of PTPases and the reduction of H2O2 levels in guard cells. Additionally, like ASA and CAT, PAO abolished dark-, exogenous H2O2-induced stomatal closure and dichlorofluorescein fluorescence in guard cells, indicating that activation of PTPases can enhance H2O2 levels probably via suppressing the decrease of H2O2 levels in guard cells. On the other hand, similar to PAO, ASA and CAT evidently prevented dark-, exogenous H2O2-induced stomatal closure and obviously inactivated PTPases in the dark. However, exogenous H2O2 significantly activated PTPases in light. The results show that H2O2 can induce activation of PTPases. Taken together, the present results provide evidence that both H2O2 and PTPases are involved in light/dark-regulated stomatal movement, and the interaction between H2O2 and PTPases plays a pivotal role in light/dark signal transduction process in guard cells.

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AP3M harbors actin filament binding activity that is crucial for vacuole morphology and stomatal closure in Arabidopsis

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1901431116 ◽

2019 ◽

Vol 116 (36) ◽

pp. 18132-18141 ◽

Cited By ~ 2

Author(s):

Wenna Zheng ◽

Yuxiang Jiang ◽

Xiangfeng Wang ◽

Shanjin Huang ◽

Ming Yuan ◽

...

Keyword(s):

Stomatal Closure ◽

Adaptor Protein ◽

Guard Cells ◽

Binding Activity ◽

Binding Domain ◽

Actin Dynamics ◽

Actin Binding ◽

Stomatal Movement ◽

Actin Binding Domain

Stomatal movement is essential for plant growth. This process is precisely regulated by various cellular activities in guard cells. F-actin dynamics and vacuole morphology are both involved in stomatal movement. The sorting of cargoes by clathrin adaptor protein (AP) complexes from the Golgi to the vacuole is critical for establishing a normal vacuole morphology. In this study, we demonstrate that the medium subunit of the AP3 complex (AP3M) binds to and severs actin filaments in vitro and that it participates in the sorting of cargoes (such as the sucrose exporter SUC4) to the tonoplast, and thereby regulates stomatal closure in Arabidopsis thaliana. Defects in AP3 or SUC4 led to more rapid water loss and delayed stomatal closure, as well as hypersensitivity to drought stress. In ap3m mutants, the F-actin status was altered compared to the wild type, and the sorted cargoes failed to localize to the tonoplast. AP3M contains a previously unidentified F-actin binding domain that is conserved in AP3M homologs in both plants and animals. Mutations in the F-actin binding domain of AP3M abolished its F-actin binding activity in vitro, leading to an aberrant vacuole morphology and reduced levels of SUC4 on the tonoplast in guard cells. Our findings indicate that the F-actin binding activity of AP3M is required for the precise localization of AP3-dependent cargoes to the tonoplast and for the regulation of vacuole morphology in guard cells during stomatal closure.

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