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. 2021 Feb 15;16(4):1876379. doi: 10.1080/15592324.2021.1876379

RIC7 plays a negative role in ABA-induced stomatal closure by inhibiting H2O2 production

Zi-Dan Zhu 1, Hai-Jing Sun 1, Jiao Li 1, Ya-Xin Yuan 1, Jun-Feng Zhao 1, Chun-Guang Zhang 1,✉, Yu-Ling Chen 1
PMCID: PMC7971284  PMID: 33586611

ABSTRACT

When plants encounter environmental stresses, phytohormone abscisic acid (ABA) accumulates quickly and efficiently reduces water loss by inducing stomatal closure. Reactive oxygen species (ROS) is an important regulator in ABA-induced stomatal closure, and ROS generation is modulated by multiple components in guard-cell ABA signaling. ROP interactive CRIB-containing protein 7 (RIC7) has been found to negatively regulate ABA-induced stomatal closure. However, the molecular details of the RIC7 function in this process are unclear. Here, by using two RIC7 overexpressing mutants, we confirmed the negative role of RIC7 in ABA-induced stomatal closure and found that guard cells of RIC7 overexpressing mutants generated less H2O2 than the wild type with ABA treatment, which were consistent with the reduced expression levels of ROS generation related NADPH oxidase genes AtRBOHD and AtRBOHF, and cytosolic polyamine oxidase genes PAO1 and PAO5 in the RIC7 overexpressing mutants. Furthermore, external applied H2O2 failed to rescue the defects of stomatal closure in RIC7 overexpressing mutants. These results suggest that RIC7 affects H2O2 generation in guard cells, and the function of H2O2 is dependent on RIC7 in ABA-induced stomatal closure, indicative of interdependency between RIC7 and H2O2 in ABA guard-cell signaling.

KEYWORDS: ABA, stomatal closure, RIC7, ✚-➔H2o2

ABA is a phytohormone that regulates plant growth and development and plays a vital role in responses to multiple environmental stresses. Stomatal aperture variation regulates the gas exchange between plant and environment, which optimizing the water loss from transpiration and photosynthetic CO2 assimilation. ABA accumulates quickly when the plants encounter abiotic stresses and enhances stomatal closure to reduce water loss. A series of cellular events happen during ABA regulation of stomatal closure, including cytosolic Ca2+ osscillation, activation of protein kinases and phosphatases, and reactive oxygen species (ROS) production.1–4 However, the regulatory mechanism of ABA-induced stomatal closure has not been completely understood.

Plants have a distinct small G protein family ROPs, and Arabidopsis (Arabidopsis thaliana) genome encodes 11 ROP genes that act as molecular switches in multiple processes, including interdigitated growth of pavement cells, 5 polar growth of pollen tubes,6 and polar auxin transport.7 ROPs have also been found to be involved in the response to environmental stresses. For example, several lines of evidence indicate that ROP2, ROP6, ROP10, and ROP11 play roles in ABA-induced stomatal closure;8–11 ROP2 and ROP7 negatively modulate red light-induced stomatal opening.12,14 ROP-specific guanine nucleotide exchange factors RopGEFs convert the GDP-bound inactive forms of ROPs into the GTP-bound active forms. There are 14 RopGEF members in Arabidopsis, and a certain process needs the activation of distinct Rop-GEFs and ROPs: RopGEF1 and RopGEF4 act as specific regulators of ROP11 in ABA-induced stomatal closure;10,15 ROP2 and ROP7 are activated by RopGEF2 in red light regulation of stomatal opening.14 Furthermore, the ROP interactive CRIB-containing proteins (RICs) have been found to act downstream of ROPs. For example, RIC7 interacts with ROP2 and plays a role in the light-induced stomatal opening by inhibiting the exocyst subunit Exo70B1.16 ROP2 and RIC7 negatively regulate ABA-induced stomatal closure.8,16 However, the mechanism of RIC7 action in ABA-induced stomatal closure is unclear. Here, we provided convincing evidence to support the interdependency between RIC7 and ROS generation in ABA induction of stomatal closure.

RIC7 plays a negative role in ABA-induced stomatal closure and ABA inhibition of seed germination

To investigate the role of RIC7 in ABA-induced stomatal closure, we obtained two T-DNA insertion ric7 mutants with the insertion sites in the promoter region of the RIC7 gene (Figure 1a). The qRT-PCR result indicated that the two ric7 mutants have higher RIC7 expression levels than the wild type (Figure 1b). Since the ric7-1 mutant is a RIC7 null mutant in the previous report,16 the two mutants with higher RIC7 levels were designated as ric7-2 and ric7-3 in this research. Next, we checked the stomatal response of the two ric7 mutants to light and ABA. The stomatal apertures of ric7-2 and ric7-3 were smaller than wild type after 2 h light illumination and were larger than wild type after 10 μM ABA treatment (Figure 2a), which are consistent with the stomatal response of RIC7 overexpression lines in the previous report 16 confirming that RIC7 plays a negative role in ABA-induced stomatal closure. Furthermore, we examined the seed germination rate of ric7 mutants with ABA treatment, and found that ric7-2 and ric7-3 mutants were also insensitive to ABA during seed germination: ric7-2 and ric7-3 mutants exhibited higher germination rates than the wild type with ABA treatment (Figure 2b), suggesting that RIC7 plays a negative role in ABA inhibition of seed germination.

Figure 1.

Figure 1.

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T-DNA insertions in promoter region of RIC7 gene led to higher RIC7 expression in ric7-2 and ric7-3 mutants. (a) The structure of RIC7 gene and the insertion site of ric7-2 and ric7-3 mutants. (b) Expressions of RIC7 in ric7-2 and ric7-3 mutants were higher than wild type (WT). (**, p < .01)

Figure 2.

Figure 2.

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RIC7 played a negative role in ABA-induced stomatal closure and ABA inhibition of seed germination. (a) Stomatal apertures of ric7-2 and ric7-3 mutants were larger than wild type after ABA treatment. (b) Seed germination rates of ric7-2 and ric7-3 mutants were higher than wild type (WT) in the MS medium containing different concentrations of ABA. (*, p < .05; **, p < .01)

Guard cells of ric7 mutants generated less ROS with ABA treatment

ROS generation is an important cellular event in ABA-induced stomatal closure and accumulates to the highest level in guard cells after 30 min ABA treatment.17 To investigate whether RIC7 affected H2O2 generation in ABA-induced stomatal closure, we checked the H2O2 levels in guard cells of the two ric7 mutants without or with 30 min ABA treatments. The results showed that both ric7-2 and ric7-3 mutants have a relatively lower H2O2 level in guard cells without ABA treatment. Although H2O2 production increased in guard cells of both wild type and the two ric7 mutants after ABA treatment, H2O2 accumulations in guard cells of ric7-2 and ric7-3 mutants were significantly lower than wild type (Figure 3 a and 3b), suggesting that RIC7 inhibits H2O2 generation in ABA-induced stomatal closure.

Figure 3.

Figure 3.

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H2O2 levels in guard cells of ric7-2 and ric7-3 mutants were lower than wild type without and with ABA treatment. The representative pictures (a) and statistical results (b) showing the H2O2 levels in guard cells of wild type (WT), ric7-2 and ric7-3 mutants. (bar = 5 μm; *, p < .05; **, p < .01)

Expression levels of genes responsible for ROS generation in ric7 mutants were lower than wild type in response to ABA

To investigate whether the lower ROS levels in ric7 mutants were due to the lower generation capability or higher scavenging activities, we checked the expression levels of genes responsible for the ROS generation (AtRBOHD/F and PAO1-5) and scavenging (CAT1-3 and SOD1-2) without or with ABA treatment, and showed here the expression levels of these genes with ABA treatment increased to at least twofold of the levels without ABA treatment in wild type or the expression levels of these genes exhibited a significant difference between ric7 mutants and wild type. AtRBOHD and AtRBOHF are the guard cell-expressed NADPH oxidase genes, and the expression of AtRBOHD has been found to reach the highest induction by ABA at 30 min.13 Therefore, the leaves were treated with ABA for 30 min, and the gene expression was detected by qRT-PCR in this research. The results showed that AtRBOHD and AtRBOHF expression levels increased upon ABA treatment, reaching about fourfold of the levels in untreated leaves of wild type; however, the expression levels of AtRBOHD or AtRBOHF with ABA treatment were significantly lower in ric7 mutants than wild type. Furthermore, polyamine oxidase (PAO) catalyzes the oxidation of the higher PA spermidine and spermine, which contributes to the H2O2 accumulation. Silencing the Arabidopsis cytosolic PAO1 and PAO5 leads to the reduced H2O2 generation with salt stress.18 Here, we showed that the expression levels of PAO1 and PAO5 increased upon ABA treatment, reaching twofold to fourfold of the levels in untreated leaves of wild type, whereas the expression levels of PAO1 and PAO5 with ABA treatment in ric7 mutants were greatly lower than the levels in wild type. The dynamic changes of cellular H2O2 level are determined by the balance between the generation and scavenging rates. We next checked the expression levels of catalases (CAT), the efficient scavengers of H2O2, upon ABA treatment, and found that CAT2 and CAT3 expression levels increased upon ABA treatment, reaching to over twofold higher than the levels in untreated leaves of wild type whereas the expression levels of CAT2 and CAT3 with ABA treatment in ric7 mutants were greatly lower than wild type (Figure 4). These results suggest that the lower H2O2 accumulation in guard cells of ric7 mutants is likely due to the reduced expression levels of the H2O2 generation related to AtRBOHD/F and PAO1/5 genes, not due to the higher expression of scavenging-related genes. Unexpectedly, the expression levels of AtRBOHD/F and PAO1/5 were higher in ric7-2 and ric7-3 mutants without ABA treatment. It has been shown that AtRBOHF were phosphorylated by OST1, an important kinase in ABA signaling,19 indicating that the activities of these enzymes were also post-translational regulated. These combined results suggest that the lower H2O2 accumulations in ric7 mutants with ABA treatment attribute to the lower expression of the genes responsible for H2O2 generation.

Figure 4.

Figure 4.

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The expression levels of H2O2 generation related genes AtRBOHD/F and PAO1/5, and the scavenging related genes CAT2/3 in ric7 mutants before and after ABA treatment. (**, p < .01)

H2O2 failed to induce stomatal closure in ric7 mutants as in wild type

To explore whether the reduced H2O2 productions in guard cells of ric7-2 and ric7-3 mutants were responsible for the reduced stomatal closure in response to ABA, we examined the effect of external applied H2O2 on stomatal closure of ric7-2 and ric7-3 mutants. Unexpectedly, H2O2 failed to induce stomatal closure of ric7-2 and ric7-3 mutants as in wild type: ric7-2 and ric7-3 mutants exhibited larger stomatal apertures than the wild type with H2O2 treatment (Figure 5), suggesting that RIC7 is required for the induction of stomatal closure by H2O2.

Figure 5.

Figure 5.

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External applied H2O2 failed to induce stomatal closure in ric7-2 and ric7-3 mutants as in wild type (WT). (**, p < .01)

ROS plays an essential role in multiple stimuli-induced stomatal closures,15,20,21 and ROS generation was regulated by GPA1, OST1, BAK1, or ABI1.22–25 Here, we provided convincing evidence to support that RIC7 inhibits guard-cell H2O2 generation induced by ABA (Figure 3), which is likely due to the lower expression levels of ROS generation related genes (Figure 4). At the same time, the external applied H2O2 failed to induce stomatal closure in ric7-2 and ric7-3 as in wild type (Figure 5), suggesting that the function of H2O2 is dependent on the existence of RIC7 in guard-cell ABA signaling. It has been shown that H2O2 forms a positive feedback loop with pepper CaWRKY27 expression in the response to heat stress.26 H2O2 also forms a feed-back regulation with anthocyanin, a plant water-soluble antioxidant: H2O2 induces accumulation of anthocyanin while anthocyanin affects ROS levels and the sensitivity of plants to ROS stress.27 Therefore, the conclusion in this research supports the interdependency of H2O2 and RIC7 in ABA-induced stomatal closure, which providing a new clue in the regulatory network of guard-cell signaling.

Materials and methods

Plant materials and growth conditions

The Arabidopsis used in this study was the Col-0 background, and ric7-2 (SALK_136344) and ric7-3 (SALK_150242) were T-DNA insertion mutants. Seedlings were grown in a greenhouse under long-day conditions (16-h-light/8-h-dark cycle), with a photon flux density of 150 μmol m−2 s−1 and a temperature of 18°C to 22°C. To check the expression levels of RIC7 in the ric7-2 and ric7-3 mutants, total RNA from leaves of three- to four-week-old plants was isolated using TRIzol (Invitrogen), and cDNA was prepared using the PrimeScript RT reagent kit (Takara). The relative expression of the RIC7 in the corresponding mutants was performed using SYBR Premix ExTaq (Takara). The primers used for qRT-PCR are F: 5’-GGACCGTCTGATAATGCCACTG-3’ and R: 5’-TCTAGTCCGACCACCAAACTCT-3’. The qRT-PCR was conducted in a Real-Time PCR System (ABI PRISM 7500; Applied Biosystems). Each experiment was repeated three times. For determination of seed germination with ABA treatment, seeds were sterilized with 75% (v/v) ethanol for 5 min and then rinsed with 95% (v/v) ethanol for 30 s. Seeds on the one-half MS medium supplemented with 0, 1, 2, 3, or 5 μM ABA were kept at 4°C for 48 h in darkness, and then incubated in the plant growth chamber (Percival). After 5 days, the seed germination rates of wild type and ric7 mutants were calculated.

Stomatal aperture assays

Stomatal aperture assays were performed essentially as described in 14. In brief, the fully expanded rosette leaves of three- to four-week-old plants were collected and illuminated with white light (150 μmol m−2 s−1) for 2 h, and then the epidermis was peeled and incubated in MES buffer (10 mM MES, 30 mM KCl, 0.1 mM CaCl2, pH 6.1) containing 10 μM ABA or 10 μM H2O2 for 2 h. The stomatal apertures before and after ABA or H2O2 treatments were determined under a microscope. Fifty stomata were randomly selected for three independent replicates. The data are presented as the means ± SE (n = 150).

Detection of the H2O2 level in guard cells

H2O2 detection in guard cells was performed as described previously.17 Abaxial epidermal strips were peeled from the leaves with open stomata and then were incubated in MES buffer containing 50 μM H2DCF-DA (Molecular Probes) in the dark for 15 min, washed for three times. The epidermal strips were then transferred to MES buffer containing 10 μM ABA for 30 min. H2O2 levels in guard cells were detected by CLSM with a setting of 488 nm excitation and 525 nm emission. The experiments were repeated at least three times with 30 cells for each treatment.

Checking the expression level of ROS generation and scavenging related genes

To check the expression levels of ROS generation and scavenging-related genes without or with ABA treatment, fully expanded rosette leaves of three- to four-week-old plants of wild type, ric7-2, and ric7-3 mutants were sprayed with 50 μM ABA. Half an hour later, the leaves were harvested and total RNA was isolated, and then cDNA was prepared using the PrimeScript RT reagent kit (Takara). Expression levels of the ROS generation and scavenging-related genes were detected using SYBR Premix ExTaq (Takara). The primers used for qRT-PCR are AtRBOHD, F, 5’- AGCTTCACAATTATTGCACGAG-3’, R, 5’- TCTCCAGTTAGGTTTAGCGAAG-3’; AtRBOHF, F, 5’-TATTGGAGACCATCTTGCTTGT-3’, R, 5’-CGTTAAAACCGGTTAGTCGATC-3’; PAO1, F, 5’-GTGTCGGTGGTAAAGAGTCTAA-3’, R, 5’- CTTTAACTTGAGAATCGCCGAG-3’; PAO5, F, 5’- TGCTGAATTGTTTAGTCCTCCT-3’, R, 5’- TTCTTTGAGACATCTCGACGAA-3’; CAT2, F, 5’- TGGGGCCTTCCTTTTAAGTTAT-3’, R, 5’- TGGGGCCTTCCTTTTAAGTTAT-3’; CAT3, F, 5’-CTTGTGGTTCCTGGAATCTACT-3’, R, 5’-AGGATCAAACTTTGAGGGGTAG-3’.

Funding Statement

This work was supported by the National Science Foundation of China (grant no. 32070191 to Y.-L.C.), and Natural Science Foundation of Hebei Province (grant no. C2019205168 to C.-G.Z.), and Scientific Research Foundation of Hebei Province for the Returned Overseas Chinese Scholars (to C.-G.Z.).

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

References

  • 1.Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese, A, Wellmann C, Al-Rasheid KAS, Grill E, et al. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca 2+ affinities. Proc Natl Acad Sci USA. 2010;107(17):1–6. doi: 10.1073/pnas.0912030107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Hauser F, Waadt R, Schroeder JI.. Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol. 2011;21(9):R346–355. doi: 10.1016/j.cub.2011.03.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Munemasa S, Hauser F, Park J, Waadt R, Brandt B, Schroeder JI.. Mechanisms of abscisic acid-mediated control of stomatal aperture. Curr Opin Plant Biol. 2015;28:154–162. doi: 10.1016/j.pbi.2015.10.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Wang P, Song CP.. Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol. 2008;178(4):703–718. doi: 10.1111/j.1469-8137.2008.02431.x. [DOI] [PubMed] [Google Scholar]
  • 5.Lin D, Ren H, Fu Y. ROP GTPase-mediated auxin signaling regulates pavement cell interdigitation in Arabidopsis thaliana. J Integr Plant Biol. 2015;57(1):31–39. doi: 10.1111/jipb.12281. [DOI] [PubMed] [Google Scholar]
  • 6.Gu Y, Vernoud V, Fu Y, Yang Z. ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J Exp Bot. 2003;54(380):93–101. doi: 10.1093/jxb/erg035. [DOI] [PubMed] [Google Scholar]
  • 7.Huang J-B, Liu H, Chen M, Li X, Wang M, Yang Y, Wang C, Huang J, Liu G, Liu Y, et al. ROP3 GTPase contributes to polar auxin transport and auxin responses and is important for embryogenesis and seedling growth in Arabidopsis. Plant Cell. 2014;26(9):3501–3518. doi: 10.1105/tpc.114.127902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Hwang J-U, Jeon BW, Hong D, Lee Y. Active ROP2 GTPase inhibits ABA- and CO2-induced stomatal closure. Plant Cell Environ. 2011;34(12):2172–2182. doi: 10.1111/j.1365-3040.2011.02413.x. [DOI] [PubMed] [Google Scholar]
  • 9.Lemichez E, Wu Y, Sanchez JP, Mettouchi A, Mathur J, Chua NH. Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev. 2001;15(14):1808–1816. doi: 10.1101/gad.900401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Li Z, Liu D. ROPGEF1 and ROPGEF4 are functional regulators of ROP11 GTPase in ABA-mediated stomatal closure in Arabidopsis. FEBS Lett. 2012;586(9):125–1253. doi: 10.1016/j.febslet.2012.03.040. [DOI] [PubMed] [Google Scholar]
  • 11.Zheng Z-L, Nafisi M, Tam A, Li H, Crowell DN, Chary SN, Schroeder JI, Shen J, Yang Z. Plasma Membrane–associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in arabidopsis. Plant Cell. 2002;14(11):2787–2797. doi: 10.1105/tpc.005611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Jeon BW, Hwang J-U, Hwang Y, Song W-Y, Fu Y, Gu Y, Bao F, Cho D, Kwak JM, Yang Z, et al. The arabidopsis small G protein ROP2 is activated by light in guard cells and inhibits light-induced stomatal opening. Plant Cell. 2008;20(1):75–87. doi: 10.1105/tpc.107.054544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in arabidopsis. Embo J. 2003;22(11):2623–2633. doi: 10.1093/emboj/cdg277 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Wang W, Liu Z, Bao L-J, Zhang -S-S, Zhang C-G, Li X, Li H-X, Zhang X-L, Bones AM, Yang Z-B, et al. The RopGEF2-ROP7/ROP2 pathway activated by phyB suppresses red light-induced stomatal opening. Plant Physiol. 2017;174(2):717–731. doi: 10.1104/pp.16.01727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Li Y, Xu SS, Gao J, Pan S, Wang GX. Glucose- and mannose-induced stomatal closure is mediated by ROS production, Ca 2+ and water channel in Vicia faba. Physiologia Plantarum. 2016;156(3):252–261. doi: 10.1111/ppl.12353. [DOI] [PubMed] [Google Scholar]
  • 16.Hong D, Jeon BW, Kim SY, Hwang J-U, Lee Y. The ROP2-RIC7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit Exo70B1 in Arabidopsis. New Phytol. 2016;209(2):624–635. doi: 10.1111/nph.13625. [DOI] [PubMed] [Google Scholar]
  • 17.Li X, Li J-H, Wang W, Chen N-Z, Ma T-S, Xi Y-N, Zhang X-L, Lin H-F, Bai Y, Huang S-J, et al. ARP2/3 complex-mediated actin dynamics is required for hydrogen peroxide-induced stomatal closure in Arabidopsis. Plant Cell Environ. 2014;37(7):1548–1560. doi: 10.1111/pce.12259. [DOI] [PubMed] [Google Scholar]
  • 18.Sagor GHM, Zhang S, Kojima S, Simm S, Berberich T, Kusano T. Reducing cytoplasmic polyamine oxidase activity in arabidopsis increases salt and drought tolerance by reducing reactive oxygen species production and increasing defense gene expression. Front Plant Sci. 2016;7:214. doi: 10.3389/fpls.2016.00214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Sirichandra C, Gu D, Hu H, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S, et al. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett. 2009;583(18):2982–2986. doi: 10.1016/j.febslet.2009.08.033. [DOI] [PubMed] [Google Scholar]
  • 20.Wang H-Q, Sun L-P, Wang L-X, Fang X-W, Li Z-Q, Zhang -F-F, Hu X, Qi C, He JM. Ethylene mediates salicylic-acid-induced stomatal closure by controlling reactive oxygen species and nitric oxide production in Arabidopsis. Plant Sci. 2020;294:110464. doi: 10.1016/j.plantsci.2020.110464. [DOI] [PubMed] [Google Scholar]
  • 21.Wang Z, Wang FX, Hong YC, Huang JR, Shi HZ, Zhu JK. Two chloroplast proteins suppress drought resistance by affecting ROS production in guard cells. Plant Physiol. 2016;172(4):2491–2503. doi: 10.1104/pp.16.00889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Murata Y, Pei Z-M, Mori IC, Schroeder J. Abscisic acid activation of plasma membrane Ca 2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell. 2001;13(11):2513–2523. doi: 10.1105/tpc.010210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Mustilli A-C, Merlot S, Vavasseur A, Fenzi F, Giraudat J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell. 2002;14(12):3089–3099. doi: 10.1105/tpc.007906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Shang Y, Dai C, Lee MM, Kwak JM, Nam KH. BRI1-associated receptor kinase 1 regulates guard cell ABA signaling mediated by Open Stomata 1 in Arabidopsis. Mol Plant. 2016;9(3):447–460. doi: 10.1016/j.molp.2015.12.014. [DOI] [PubMed] [Google Scholar]
  • 25.Zhang W, Jeon BW, Assmann SM. Heterotrimeric G-protein regulation of ROS signalling and calcium currents in Arabidopsis guard cells. J Exp Bot. 2011;62(7):2371–2379. doi: 10.1093/jxb/erq424. [DOI] [PubMed] [Google Scholar]
  • 26.Dang F, Lin J, Xue, B, Chen Y, Guan D, Wang Y, He S. CaWRKY27 negatively regulates H2O2-mediated thermotolerance in pepper (Capsicum annuum). Front Plant Sci. 2018;9:1633. doi: 10.3389/fpls.2018.01633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Xu ZH, Mahmood K, Rothstein SJ. ROS induces anthocyanin production via late biosynthetic genes and anthocyanin deficiency confers the hypersensitivity to ROS-generating stresses in Arabidopsis. Plant and Cell Physiology. 2017;58(8):1364–1377. doi: 10.1093/pcp/pcx073. [DOI] [PubMed] [Google Scholar]

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