Abstract
Main conclusion
Dynamic protein and phosphoprotein profiles uncovered the overall regulation of stomata movement against pathogen invasion and phosphorylation states of proteins involved in ABA, SA, calcium and ROS signaling, which may modulate the stomatal immune response.
Abstract
Stomatal openings represent a major route of pathogen entry into the plant, and plants have evolved mechanisms to regulate stomatal aperture as innate immune response against bacterial invasion. However, the mechanisms underlying stomatal immunity are not fully understood. Taking advantage of high-throughput liquid chromatography mass spectrometry (LC–MS), we performed label-free proteomic and phosphoproteomic analyses of enriched guard cells in response to a bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000. In total, 495 proteins and 1229 phosphoproteins were identified as differentially regulated. These proteins are involved in a variety of signaling pathways, including abscisic acid and salicylic acid hormone signaling, calcium and reactive oxygen species signaling. We also showed that dynamic changes of phosphoprotein WRKY transcription factors may play a crucial role in regulating stomata movement in plant immunity. The identified proteins/phosphoproteins and the pathways form interactive molecular networks to regulate stomatal immunity. This study has provided new insights into the multifaceted mechanisms of stomatal immunity. The differential proteins and phosphoproteins are potential targets for engineering or breeding of crops for enhanced pathogen defense.
Similar content being viewed by others
References
Agurla S, Gayatri G, Raghavendra AS (2017) Signal transduction components in guard cells during stomatal closure by plant hormones and microbial elicitors. Mech Plant Horm Signal Stress. https://doi.org/10.1002/9781118889022.ch30
Angel Torres M (2010) ROS in biotic interactions. Physiol Plant 138:414–429. https://doi.org/10.1111/j.1399-3054.2009.01326.x
Arnaud D, Hwang I (2015) A sophisticated network of signaling pathways regulates stomatal defenses to bacterial pathogens. Mol Plant 8:566–581. https://doi.org/10.1016/j.molp.2014.10.012
Arnaud D, Lee S, Takebayashi Y, Choi D, Choi J, Sakakibara H, Hwang I (2017) Cytokinin-mediated regulation of reactive oxygen species homeostasis modulates stomatal immunity in Arabidopsis. Plant Cell 29:543–559. https://doi.org/10.1105/tpc.16.00583
Assmann SM, Jegla T (2016) Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2. Curr Opin Plant Biol 33:157–167. https://doi.org/10.1016/j.pbi.2016.07.003
Birkenbihl RP, Liu S, Somssich IE (2017) Transcriptional events defining plant immune responses. Curr Opin Plant Biol 38:1–9. https://doi.org/10.1016/j.pbi.2017.04.004
Boudsocq M, Sheen J (2013) CDPKs in immune and stress signaling. Trends Plant Sci 18:30–40. https://doi.org/10.1016/j.tplants.2012.08.008
Buscaill P, Rivas S (2014) Transcriptional control of plant defence responses. Curr Opin Plant Biol 20:35–46. https://doi.org/10.1016/j.pbi.2014.04.004
Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671. https://doi.org/10.1038/nature06006
Chou MF, Schwartz D (2011) Biological sequence motif discovery using motif-x. Curr ProtocBioinform. https://doi.org/10.1002/0471250953.bi1315s35
David L, Harmon A, Chen S (2019) Plant immune responses - from guard cells and local responses to systemic defense against bacterial pathogens. Plant Signal Behav 14:e1588667. https://doi.org/10.1080/15592324.2019.1588667
Deininger P (1990) Molecular cloning: a laboratory manual. In: Sambrook J, Fritsch EF, Maniatis T (eds) Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1989 (in 3 volumes). https://doi.org/https://doi.org/10.1002/jobm.3620300824
Desclos-Theveniau M, Arnaud D, Huang T-Y, Lin GJ-C, Chen W-Y, Lin Y-C, Zimmerli L (2012) The Arabidopsis lectin receptor kinase LecRK-V5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000. PLoS Pathog 8(2):e1002513. https://doi.org/10.1371/journal.ppat.1002513
Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtRBOH F-mediated hydrogen peroxide synthesis. Plant J 47(6):907–916. https://doi.org/10.1111/j.1365-313X.2006.02842.x
Ding ZJ, Yan JY, Xu XY, Yu DQ, Li GX, Zhang SQ, Zheng SJ (2014) Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J 79:13–27. https://doi.org/10.1111/tpj.12538
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70. https://doi.org/10.1093/nar/gkq310
Du M, Zhai Q, Deng L, Li S, Li H, Yan L, Huang Z, Wang B, Jiang H, Huang T, Li C-B, Wei J, Kang L, Li J, Li C (2014) Closely related NAC transcription factors of tomato differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell 26:3167–3184. https://doi.org/10.1105/tpc.114.128272
Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte C-P, Schulze WX, Romeis T (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci U S A 110:8744–8749. https://doi.org/10.1073/pnas.1221294110
Durek P, Schmidt R, Heazlewood JL, Jones A, MacLean D, Nagel A, Kersten B, Schulze WX (2009) PhosPhAt: the Arabidopsis thaliana phosphorylation site database. an update. Nucleic Acids Res 38:D828–D834. https://doi.org/10.1093/nar/gkp810
Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50(12):2123–2132. https://doi.org/10.1093/pcp/pcp147
Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KA, Romeis T (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci 106(50):21425–21430. https://doi.org/10.1073/pnas.0912021106
Geng S, Misra BB, Armas E, Huhman DV, Alborn HT, Sumner LW, Chen S (2016) Jasmonate-mediated stomatal closure under elevated CO2 revealed by time-resolved metabolomics. Plant J 88(6):947–962. https://doi.org/10.1111/tpj.13296
Gimenez-Ibanez S, Boter M, Ortigosa A, Garcia-Casado G, Chini A, Lewsey MG, Ecker JR, Ntoukakis V, Solano R (2017) JAZ2 controls stomata dynamics during bacterial invasion. New Phytol 213:1378–1392. https://doi.org/10.1111/nph.14354
Gudesblat GE, Torres PS, Vojnov AA (2009) Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiol 149:1017–1027. https://doi.org/10.1104/pp.108.126870
Hetherington AM (2001) Guard cell signaling. Cell 107:711–714. https://doi.org/10.1016/S0092-8674(01)00606-7
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908. https://doi.org/10.1038/nature01843
Jalakas P, Huang Y-C, Yeh Y-H, Zimmerli L, Merilo E, Kollist H, Brosche M (2017) The role of enhanced responses to ABA1 (ERA1) in arabidopsis stomatal responses is beyond ABA signaling. Plant Physiol 174(2):665–671. https://doi.org/10.1104/pp.17.00220
Jeandroz S, Lamotte O, Astier J, Rasul S, Trapet P, Besson-Bard A, Bourque S, Nicolas-Frances V, Ma W, Berkowitz GA, Wendehenne D (2013) There's more to the picture than meets the eye: nitric oxide cross talk with Ca2+ signaling. Plant Physiol 163(2):459–470. https://doi.org/10.1104/pp.113.220624
Joshi-Saha A, Valon C, Leung J (2011) A brand new START: abscisic acid perception and transduction in the guard cell. Sci Signal 4(201):re4. https://doi.org/10.1126/scisignal.2002164
Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci U S A 105:7100–7105. https://doi.org/10.1073/pnas.0802332105
Khokon MAR, Okuma E, Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y (2011) Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant Cell Environ 34(3):434–443. https://doi.org/10.1111/j.1365-3040.2010.02253.x
Khokon MAR, Salam MA, Jammes F, Ye W, Hossain MA, Okuma E, Nakamura Y, Mori IC, Kwak JM, Murata Y (2017) MPK9 and MPK12 function in SA-induced stomatal closure in Arabidopsis thaliana. Biosci Biotech Biochem 81(7):1394–1400. https://doi.org/10.1080/09168451.2017.1308244
Kim T-H, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591. https://doi.org/10.1146/annurev-arplant-042809-112226
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in arabidopsis. Embo J 22(11):2623–2633. https://doi.org/10.1093/emboj/cdg277
Lawrence S, Pang Q, Kong W, Chen S (2018) Stomata Tape-Peel: an improved method for guard cell sample preparation. JoVE. https://doi.org/10.3791/57422
Lee SC, Lan W, Buchanan BB, Luan S (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci U S A 106(50):21419–21424. https://doi.org/10.1073/pnas.0910601106
Lee Y, Kim YJ, Kim M-H, Kwak JM (2016) MAPK cascades in guard cell signal transduction. Front Plant Sci 7:80. https://doi.org/10.3389/fpls.2016.00080
Li J, Besseau S, Toronen P, Sipari N, Kollist H, Holm L, Palva ET (2013) Defense-related transcription factors WRKY70 and WRKY54 modulate osmotic stress tolerance by regulating stomatal aperture in Arabidopsis. New Phytol 200(2):455–472. https://doi.org/10.1111/nph.12378
Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, Chen S, Zhou J-M (2014) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15(3):329–338. https://doi.org/10.1016/j.chom.2014.02.009
Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G (2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. Plos Biol 7(6):e1000139. https://doi.org/10.1371/journal.pbio.1000139
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324(5930):1064–1068. https://doi.org/10.1126/science.1172408
Melcher K, Ng L-M, Zhou XE, Soon F-F, Xu Y, Suino-Powell KM, Park S-Y, Weiner JJ, Fujii H, Chinnusamy V, Kovach A, Li J, Wang Y, Li J, Peterson FC, Jensen DR, Yong E-L, Volkman BF, Cutler SR, Zhu J-K, Xu HE (2009) A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462(7273):602–608. https://doi.org/10.1038/nature08613
Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126(5):969–980. https://doi.org/10.1016/j.cell.2006.06.054
Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101–122. https://doi.org/10.1146/annurev.phyto.121107.104959
Melotto M, Zhang L, Oblessuc PR, He SY (2017) Stomatal defense a decade later. Plant Physiol 174(2):561–571. https://doi.org/10.1104/pp.16.01853
Miyazono K-I, Miyakawa T, Sawano Y, Kubota K, Kang H-J, Asano A, Miyauchi Y, Takahashi M, Zhi Y, Fujita Y, Yoshida T, Kodaira K-S, Yamaguchi-Shinozaki K, Tanokura M (2009) Structural basis of abscisic acid signalling. Nature 462(7273):609–614. https://doi.org/10.1038/nature08583
Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15(4):349–357. https://doi.org/10.1016/j.pbi.2012.05.006
Montillet J-L, Leonhardt N, Mondy S, Tranchimand S, Rumeau D, Boudsocq M, Garcia AV, Douki T, Bigeard J, Lauriere C, Chevalier A, Castresana C, Hirt H (2013) An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in Arabidopsis. PLoS Biol 11(3):e1001513. https://doi.org/10.1371/journal.pbio.1001513
Munemasa S, Mori IC, Murata Y (2011) Methyl jasmonate signaling and signal crosstalk between methyl jasmonate and abscisic acid in guard cells. Plant Signal Behav 6(7):939–941. https://doi.org/10.4161/psb.6.7.15439
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ 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 13(11):2513–2523. https://doi.org/10.1105/tpc.13.11.2513
Murata Y, Mori IC, Munemasa S (2015) Diverse stomatal signaling and the signal integration mechanism. Annu Rev Plant Biol 66:369–392. https://doi.org/10.1146/annurev-arplant-043014-114707
Mustilli A-C, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14(12):3089–3099. https://doi.org/10.1105/tpc.007906
Okuda S, Watanabe Y, Moriya Y, Kawano S, Yamamoto T, Matsumoto M, Takami T, Kobayashi D, Araki N, Yoshizawa AC, Tabata T, Sugiyama N, Goto S, Ishihama Y (2017) jPOSTrepo: an international standard data repository for proteomes. Nucleic Acids Res 45(D1):D1107–D1111. https://doi.org/10.1093/nar/gkw1080
Panchal S, Melotto M (2017) Stomate-based defense and environmental cues. Plant Signal Behav 12(9):e1362517. https://doi.org/10.1080/15592324.2017.1362517
Panchal S, Roy D, Chitrakar R, Price L, Breitbach ZS, Armstrong DW, Melotto M (2016) Coronatine facilitates Pseudomonas syringae infection of Arabidopsis leaves at night. Front Plant Sci 7:880. https://doi.org/10.3389/fpls.2016.00880
Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581(12):2325–2336. https://doi.org/10.1016/j.febslet.2007.04.008
Pang Q, Zhang T, Wang Y, Kong W, Guan Q, Yan X, Chen S (2018) Metabolomics of early stage plant cell-microbe interaction using stable isotope labeling. Front Plant Sci 9:760. https://doi.org/10.3389/fpls.2018.00760
Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-FF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324(5930):1068–1071. https://doi.org/10.1126/science.1173041
Pei Z-M, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406(6797):731–734. https://doi.org/10.1038/35021067
Raghavendra A, Murata Y (2017) Editorial: Signal transduction in stomatal guard cells. Front Plant Sci 8:114. https://doi.org/10.3389/fpls.2017.00114
Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Annu Rev Phytopathol 49:317–343. https://doi.org/10.1146/annurev-phyto-073009-114447
Roy D, Panchal S, Rosa BA, Melotto M (2013) Escherichia coli O157:H7 induces stronger plant immunity than Salmonella enterica Typhimurium SL1344. Phytopathol 103(4):326–332. https://doi.org/10.1094/phyto-09-12-0230-fi
Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, Boken AK, Langum TJ, Smidt L, Boomsma DD, Emme NJ, Chen X, Finer JJ, Shen QJ, Rushton PJ (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotech J 10(1):2–11. https://doi.org/10.1111/j.1467-7652.2011.00634.x
Saito N, Munemasa S, Nakamura Y, Shimoishi Y, Mori IC, Murata Y (2008) Roles of RCN1, regulatory a subunit of protein phosphatase 2A, in methyl jasmonate signaling and signal crosstalk between methyl jasmonate and abscisic acid. Plant Cell Physiol 49(9):1396–1401. https://doi.org/10.1093/pcp/pcn106
Sawinski K, Mersmann S, Robatzek S, Böhmer M (2013) Guarding the green: pathways to stomatal immunity. Mol Plant-Microbe Interact 26(6):626–632. https://doi.org/10.1094/MPMI-12-12-0288-CR
Schellenberg B, Ramel C, Dudler R (2010) Pseudomonas syringae virulence factor syringolin A counteracts stomatal immunity by proteasome inhibition. Mol Plant-Microbe Interact 23(10):1287–1293. https://doi.org/10.1094/mpmi-04-10-0094
Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Biol 52(1):627–658. https://doi.org/10.1146/annurev.arplant.52.1.627
Schwartz D, Gygi SP (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat Biotechnol 23(11):1391–1398. https://doi.org/10.1038/nbt1146
Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu F-F, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468(7322):400–405. https://doi.org/10.1038/nature09430
Sirichandra C, Gu D, Hu H-C, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S, Kwak JM (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583(18):2982–2986. https://doi.org/10.1016/j.febslet.2009.08.033
Soon F-F, Ng L-M, Zhou XE, West GM, Kovach A, Tan MHE, Suino-Powell KM, He Y, Xu Y, Chalmers MJ, Brunzelle JS, Zhang H, Yang H, Jiang H, Li J, Yong E-L, Cutler S, Zhu J-K, Griffin PR, Melcher K, Xu HE (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335(6064):85–88. https://doi.org/10.1126/science.1215106
Sun Y, Yu D (2015) Activated expression of AtWRKY53 negatively regulates drought tolerance by mediating stomatal movement. Plant Cell Rep 34(8):1295–1306. https://doi.org/10.1007/s00299-015-1787-8
Sun X, Kang X, Ni M (2012) Hypersensitive to red and blue 1 and its modification by protein phosphatase 7 are implicated in the control of Arabidopsis stomatal aperture. PLoS Genet 8(5):e1002674. https://doi.org/10.1371/journal.pgen.1002674
Takemiya A, Sugiyama N, Fujimoto H, Tsutsumi T, Yamauchi S, Hiyama A, Tada Y, Christie JM, Shimazaki K-i (2013) Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nat Commun 4:2094. https://doi.org/10.1038/ncomms3094
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448(7154):661–665. https://doi.org/10.1038/nature05960
Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45(W1):W122–W129. https://doi.org/10.1093/nar/gkx382
Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14(6):310–317. https://doi.org/10.1016/j.tplants.2009.03.006
Toum L, Torres PS, Gallego SM, Benavídes MP, Vojnov AA, Gudesblat GE (2016) Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production. Front Plant Sci 7:1851. https://doi.org/10.3389/fpls.2016.01851
Trotta A, Wrzaczek M, Scharte J, Tikkanen M, Konert G, Rahikainen M, Holmstrom M, Hiltunen H-M, Rips S, Sipari N, Mulo P, Weis E, von Schaewen A, Aro E-M, Kangasjarvi S (2011) Regulatory subunit B gamma of protein phosphatase 2A prevents unnecessary defense reactions under low light in Arabidopsis. Plant Physiol 156(3):1464–1480. https://doi.org/10.1104/pp.111.178442
Tseng T-S, Briggs WR (2010) The Arabidopsis rcn1-1 mutation impairs dephosphorylation of Phot2, resulting in enhanced blue light responses. Plant Cell 22(2):392–402. https://doi.org/10.1105/tpc.109.066423
Underwood W, Melotto M, He SY (2007) Role of plant stomata in bacterial invasion. Cell Microbiol 9(7):1621–1629. https://doi.org/10.1111/j.1462-5822.2007.00938.x
Vizcaíno JA, Côté RG, Csordas A, Dianes JA, Fabregat A, Foster JM, Griss J, Alpi E, Birim M, Contell J, O'Kelly G, Schoenegger A, Ovelleiro D, Pérez-Riverol Y, Reisinger F, Ríos D, Wang R, Hermjakob H (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 41:D1063–D1069. https://doi.org/10.1093/nar/gks1262
Waadt R, Manalansan B, Rauniyar N, Munemasa S, Booker MA, Brandt B, Waadt C, Nusinow DA, Kay SA, Kunz H-H, Schumacher K, DeLong A, Yates JR III, Schroeder JI (2015) Identification of open stomatal-interacting proteins reveals interactions with sucrose non-fermenting1-related protein kinases 2 and with type 2A protein phosphatases that function in abscisic acid responses. Plant Physiol 169(1):760–779. https://doi.org/10.1104/pp.15.00575
Wang P, Song C-P (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytolog 178(4):703–718. https://doi.org/10.1111/j.1469-8137.2008.02431.x
Wang X-Q, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292(5524):2070–2072. https://doi.org/10.1126/science.1059046
Wang Y, Li Z, Liu D, Xu J, Wei X, Yan L, Yang C, Lou Z, Shui W (2014) Assessment of BAK1 activity in different plant receptor-like kinase complexes by quantitative profiling of phosphorylation patterns. J of Proteomics 108:484–493. https://doi.org/10.1016/j.jprot.2014.06.009
Withers J, Dong X (2017) Post-translational regulation of plant immunity. Curr Opin Plant Biol 38:124–132. https://doi.org/10.1016/j.pbi.2017.05.004
Xin X-F, He SY (2013) Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. AnnuRev Phytopathol 51:473–498. https://doi.org/10.1146/annurev-phyto-082712-102321
Yan Y, Stolz S, Chetelat A, Reymond P, Pagni M, Dubugnon L, Farmer EE (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19(8):2470–2483. https://doi.org/10.1105/tpc.107.050708
Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21(8):2220–2236. https://doi.org/10.1105/tpc.109.065730
Zeng W, He SY (2010) A prominent role of the flagellin receptor flagellin-sensing2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol 153(3):1188–1198. https://doi.org/10.1104/pp.110.157016
Zeng W, Brutus A, Kremer JM et al (2011) A genetic screen reveals Arabidopsis stomatal and/or apoplastic defenses against Pseudomonas syringae pv. tomato DC3000. PLoS Pathog 7(10):e1002291. https://doi.org/10.1371/journal.ppat.1002291
Zhang W, He SY, Assmann SM (2008) The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation. Plant J 56(6):984–996. https://doi.org/10.1111/j.1365-313X.2008.03657.x
Zhang T, Schneider JD, Zhu N, Chen S (2017) Identification of MAPK substrates using quantitative phosphoproteomics. Methods Mol Biol 1578:133–142. https://doi.org/10.1007/978-1-4939-6859-6_10
Zhang T, Meng L, Kong W, Yin Z, Wang Y, Schneider JD, Chen S (2018) Quantitative proteomics reveals a role of JAZ7 in plant defense response to Pseudomonas syringae DC3000. J Proteomics 175:114–126. https://doi.org/10.1016/j.jprot.2018.01.002
Zheng X-Y, Spivey NW, Zeng W, Liu P-P, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11(6):587–596. https://doi.org/10.1016/j.chom.2012.04.014
Acknowledgements
The authors would like to thank Dr. Craig Dufresne at the Thermo Fisher Scientific for assistance in label-free quantification analysis. This work was supported by a faculty retention fund provided by the University of Florida and partly by the National Natural Science Foundation of China (31570396).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing financial interest.
Additional information
Communicated by Anastasios Melis.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pang, Q., Zhang, T., Zhang, A. et al. Proteomics and phosphoproteomics revealed molecular networks of stomatal immune responses. Planta 252, 66 (2020). https://doi.org/10.1007/s00425-020-03474-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-020-03474-3