Extracellular ATP mediates H2S-regulated stomatal movements and guard cell K+ current in a H2O2-dependent manner in Arabidopsis

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• 作者：Lanxiang Wang (1) r> Xiaoyan Ma (2) r> Yongmei Che (1) r> Lixia Hou (1) r> Xin Liu (1) r> Wei Zhang (2) r>r>1. Shandong Key Laboratory of Plant Biotechnology in University ; College of Life Sciences ; Qingdao Agricultural University ; Qingdao ; 266109 ; China r> 2. Key Laboratory of Plant Cell Engineering and Germplasm Innovation ; Ministry of Education ; College of Life Sciences ; Shandong University ; Jinan ; 250100 ; China r>
• 关键词：Hydrogen sulfide (H2S) ; K+ current ; Extracellular ATP (eATP) ; Hydrogen peroxide (H2O2) ; Stomatal closure ; Arabidopsis thaliana
• 刊名：Chinese Science Bulletin
• 出版年：2015
• 出版时间：February 2015
• 年：2015
• 卷：60
• 期：4
• 页码：419-427
• 全文大小：1,061 KB
• 参考文献：1. Kim TH, B枚hmer M, Hu H et al (2001) Guard cell signal transduction network: advances in understanding abscisic acid, CO_plus-plus">2, and Cap class="a-plus-plus">2+p> signaling. Annu Rev Plant Biol 61:561鈥?91 rnal" href="http://dx.doi.org/10.1146/annurev-arplant-042809-112226" target="_blank" title="It opens in new window">CrossRef r> 2. Fan LM, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7:537鈥?46 rnal" href="http://dx.doi.org/10.1016/j.pbi.2004.07.009" target="_blank" title="It opens in new window">CrossRef r> 3. Garc铆a-Mata C, Lamattina L (2013) Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201:66鈥?3 rnal" href="http://dx.doi.org/10.1016/j.plantsci.2012.11.007" target="_blank" title="It opens in new window">CrossRef r> 4. Kajimura M, Fukuda R, Bateman RM et al (2010) Interaction of multiple gas-transducing systems: hallmarks and uncertainties of CO, NO and H_plus-plus">2S gas biology. Antioxid Redox Signal 13:157鈥?92 rnal" href="http://dx.doi.org/10.1089/ars.2009.2657" target="_blank" title="It opens in new window">CrossRef r> 5. Tan BH, Wong PT, Bian JS (2010) Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56:3鈥?0 rnal" href="http://dx.doi.org/10.1016/j.neuint.2009.08.008" target="_blank" title="It opens in new window">CrossRef r> 6. Lisjak M, Tekli膰 T, Wilson ID et al (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36:1607鈥?616 rnal" href="http://dx.doi.org/10.1111/pce.12073" target="_blank" title="It opens in new window">CrossRef r> 7. Garc铆a-Mata C, Lamattina L (2010) Hydrogen sulphide a novel gasotransmitter involved in guard cell signaling. New Phytol 188:977鈥?84 rnal" href="http://dx.doi.org/10.1111/j.1469-8137.2010.03465.x" target="_blank" title="It opens in new window">CrossRef r> 8. Hou ZH, Wang LX, Liu J et al (2013) Hydrogen sulfide regulates ethylene-induced stomatal closure in / Arabidopsis thaliana. J Integr Plant Biol 55:277鈥?89 rnal" href="http://dx.doi.org/10.1111/jipb.12004" target="_blank" title="It opens in new window">CrossRef r> 9. Liu J, Hou LX, Liu GH et al (2011) Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of / Arabidopsis thaliana. Chin Sci Bull 56:3547鈥?553 rnal" href="http://dx.doi.org/10.1007/s11434-011-4819-y" target="_blank" title="It opens in new window">CrossRef r> 10. Lisjak M, Srivastava N, Tekli膰 T et al (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931鈥?35 rnal" href="http://dx.doi.org/10.1016/j.plaphy.2010.09.016" target="_blank" title="It opens in new window">CrossRef r> 11. Lisjak M, Tekli膰 T, Wilson ID et al (2011) Hydrogen sulfide effects on stomatal apertures. Plant Signal Behav 6:1444鈥?446 rnal" href="http://dx.doi.org/10.4161/psb.6.10.17104" target="_blank" title="It opens in new window">CrossRef r> 12. Ye Q, Hou ZH, Liu J et al (2011) H_plus-plus">2O_plus-plus">2 involvement in H_plus-plus">2S-induced stomatal closure of / Arabidopsis thaliana L. Plant Physiol J 47:1195鈥?200 (in Chinese) r> 13. Kim SY, Sivaguru M, Stacey G (2006) Extracellular ATP in plants, visualization, localization, and analysis of physiological significance in growth and signaling. Plant Physiol 142:984鈥?92 rnal" href="http://dx.doi.org/10.1104/pp.106.085670" target="_blank" title="It opens in new window">CrossRef r> 14. Chivasa S, Ndimba BK, Simon WJ et al (2005) Extracellular ATP functions as an endogenous external metabolite regulating plant cell viability. Plant Cell 17:3019鈥?034 rnal" href="http://dx.doi.org/10.1105/tpc.105.036806" target="_blank" title="It opens in new window">CrossRef r> 15. Clark G, Wu M, Wat N et al (2010) Both the stimulation and inhibition of root hair growth induced by extracellular nucleotides in / Arabidopsis are mediated by nitric oxide and reactive oxygen species. Plant Mol Biol 74:423鈥?35 rnal" href="http://dx.doi.org/10.1007/s11103-010-9683-7" target="_blank" title="It opens in new window">CrossRef r> 16. Jeter CR, Tang W, Henaff E et al (2004) Evidence of a novel cell signaling role for extracellular adenosine triphosphates and diphosphates in / Arabidopsis. Plant Cell 16:2652鈥?664 rnal" href="http://dx.doi.org/10.1105/tpc.104.023945" target="_blank" title="It opens in new window">CrossRef r> 17. Weerasinghe RR, Swanson SJ, Okada SF et al (2009) Touch induces ATP release in / Arabidopsis roots that is modulated by the heterotrimeric G-protein complex. FEBS Lett 583:2521鈥?526 rnal" href="http://dx.doi.org/10.1016/j.febslet.2009.07.007" target="_blank" title="It opens in new window">CrossRef r> 18. Thomas C, Rajagopal A, Windsor B et al (2000) A role for ectophosphatase in xenobiotic resistance. Plant Cell 12:519鈥?33 rnal" href="http://dx.doi.org/10.1105/tpc.12.4.519" target="_blank" title="It opens in new window">CrossRef r> 19. Klein M, Perfus-Barbeoch L, Frelet A et al (2003) The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. Plant J 33:119鈥?29 rnal" href="http://dx.doi.org/10.1046/j.1365-313X.2003.016012.x" target="_blank" title="It opens in new window">CrossRef r> 20. Gaedeke N, Klein M, Kolukisaoglu U et al (2001) The / Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J 20:1875鈥?887 rnal" href="http://dx.doi.org/10.1093/emboj/20.8.1875" target="_blank" title="It opens in new window">CrossRef r> 21. Bodin P, Burnstock G (2001) Purinergic signaling ATP release. Neurochem Res 26:959鈥?69 rnal" href="http://dx.doi.org/10.1023/A:1012388618693" target="_blank" title="It opens in new window">CrossRef r> 22. Clark G, Fraley D, Steinebrunner I et al (2011) Extracellular nucleotides and apyrases regulate stomatal aperture in / Arabidopsis. Plant Physiol 156:1740鈥?753 r> 23. Clark G, Darwin C, Mehta V et al (2013) Effects of chemical inhibitors and apyrase enzyme further document a role for apyrases and extracellular ATP in the opening and closing of stomates in / Arabidopsis. Plant Signal Behav 8:e26093 r> 24. Assmann SM (1993) Signal transduction in guard cells. Annu Rev Cell Biol 9:345鈥?75 rnal" href="http://dx.doi.org/10.1146/annurev.cb.09.110193.002021" target="_blank" title="It opens in new window">CrossRef r> 25. Zhao X, Qiao XR, Yuan J et al (2012) Nitric oxide inhibits blue light-induced stomatal opening by regulating the Kp class="a-plus-plus">+p> influx in guard cells. Plant Sci 184:29鈥?5 rnal" href="http://dx.doi.org/10.1016/j.plantsci.2011.12.007" target="_blank" title="It opens in new window">CrossRef r> 26. Lemtiri-Chlieh F, Berkowitz GA (2004) Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of / Arabidopsis leaf guard and mesophyll cells. J Biol Chem 279:35306鈥?5312 rnal" href="http://dx.doi.org/10.1074/jbc.M400311200" target="_blank" title="It opens in new window">CrossRef r> 27. Zhang W, Nilson SE, Assmann SM (2008) Isolation and whole-cell patch clamping of / Arabidopsis guard cell protoplasts. CSH Protoc. doi:pan class="a-plus-plus non-url-ref">10.1101/pdb.prot5014 r> 28. 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 56:984鈥?96 rnal" href="http://dx.doi.org/10.1111/j.1365-313X.2008.03657.x" target="_blank" title="It opens in new window">CrossRef r> 29. Hou ZH, Che YM, Wang LX et al (2012) H_plus-plus">2S functions downstream of H_plus-plus">2O_plus-plus">2 in mediating ethylene-induced stomatal closure in Arabidopsis thaliana. Plant Physiol J 48:1193鈥?199 (in Chinese) r> 30. Klein M, Geisler M, Suh SJ et al (2004) Disruption of AtMRP4, a guard cell plasma membrane ABCC-type ABC transporter, leads to deregulation of stomatal opening and increased drought susceptibility. Plant J 39:219鈥?36 rnal" href="http://dx.doi.org/10.1111/j.1365-313X.2004.02125.x" target="_blank" title="It opens in new window">CrossRef r> 31. Suh SJ, Wang YF, Frelet A et al (2007) The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in / Arabidopsis guard cells. J Biol Chem 282:1916鈥?924 r> 32. Wu SJ, Liu YS, Wu JY (2008) The signaling role of extracellular ATP and its dependence on Cap class="a-plus-plus">2+p> flux in elicitation of / Salvia miltiorrhiza hairy root cultures. Plant Cell Physiol 49:617鈥?24 r> 33. Hao LH, Wang WX, Chen C et al (2012) Extracellular ATP promotes stomatal opening of / Arabidopsis thaliana through heterotrimeric G protein 伪 subunit and reactive oxygen species. Mol Plant 5:852鈥?64 rnal" href="http://dx.doi.org/10.1093/mp/ssr095" target="_blank" title="It opens in new window">CrossRef r> 34. L眉 D, Wang W, Miao C et al (2013) ATHK1 acts downstream of hydrogen peroxide to mediate ABA signaling through regulation of calcium channel activity in / Arabidopsis guard cells. Chin Sci Bull 58:336鈥?43 r> 35. Hosy E, Vavasseur A, Mouline K et al (2003) The / Arabidopsis outward Kp class="a-plus-plus">+p> channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci USA 100:5549鈥?554 r> 36. Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581:2325鈥?336 rnal" href="http://dx.doi.org/10.1016/j.febslet.2007.04.008" target="_blank" title="It opens in new window">CrossRef r> 37. Sato A, Sato Y, Fukao Y et al (2009) Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase. Biochem J 424:439鈥?48 rnal" href="http://dx.doi.org/10.1042/BJ20091221" target="_blank" title="It opens in new window">CrossRef r> 38. Becker D, Hoth S, Ache P et al (2003) Regulation of the ABA-sensitive / Arabidopsis potassium channel gene / GORK in response to water stress. FEBS Lett 554:119鈥?26 r> 39. Buckler KJ (2012) Effects of exogenous hydrogen sulphide on calcium signalling, background (TASK) K channel activity and mitochondrial function in chemoreceptor cells. Pfl眉gers Arch-Eur J Physiol 463:743鈥?54 rnal" href="http://dx.doi.org/10.1007/s00424-012-1089-8" target="_blank" title="It opens in new window">CrossRef r> 40. Takahashi Y, EbisuY Kinoshita T et al (2013) bHLH transcription factors that facilitate Kp class="a-plus-plus">+p> uptake during stomatal opening are repressed by abscisic acid through phosphorylation. Sci Signal 6:ra48 r> 41. Munemasa S, Oda K, Watanabe-Sugimoto M et al (2007) The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in / Arabidopsis guard cells, specific impairment of ion channel activation and second messenger production. Plant Physiol 143:1398鈥?407 rnal" href="http://dx.doi.org/10.1104/pp.106.091298" target="_blank" title="It opens in new window">CrossRef r> 42. Vahisalu T, Kollist H, Wang YF et al (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signaling. Nature 452:487鈥?91 rnal" href="http://dx.doi.org/10.1038/nature06608" target="_blank" title="It opens in new window">CrossRef r>
• 刊物主题：Science, general; Life Sciences, general; Physics, general; Chemistry/Food Science, general; Earth Sciences, general; Engineering, general;
• 出版者：Springer Berlin Heidelberg
• ISSN：1861-9541

文摘

Hydrogen sulfide (H2S) is a newly discovered gaseous signaling molecule and involved in ethylene and ABA-induced stomatal closure. As an important factor, extracellular ATP (eATP) was believed to participate in regulation of stomatal closing. However, the mechanism by which eATP mediates H2S-regulated stomatal closure remains unclear. Here, we employed Arabidopsis wild-type and mutant lines of ATP-binding cassette transporters (Atmrp4, Atmrp5 and their double mutant Atmrp4/5) to study the function of eATP in H2S-regulated stomatal movement. Our results indicated that H2S affected stomatal closing through stimulating guard cell outward K+ current. Moreover, we found that H2S induced eATP generation by regulating the activity of an ABC transporter. The inhibitor of ABC transporters, glibenclamide (Gli), could impair H2S-regulated stomatal closure and reduce H2S-dependent eATP accumulation in Atmrp4 and Atmrp5 mutants. In addition, the promotion effect of H2S on outward K+ currents was diminished in Atmrp4/5 double mutant. Our data suggested that hydrogen peroxide (H2O2) is required for H2S-induced stomatal closure, and the production of H2O2 is regulated by eATP via NADPH oxidase. Based on this work, we conclude that H2S-induced stomatal closure requires ABC transporter-dependent eATP production and subsequent NADPH oxidase-dependent H2O2 accumulation.