Startseite The crosstalk between ABA, nitric oxide, hydrogen peroxide, and calcium in stomatal closing of Arabidopsis thaliana
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

The crosstalk between ABA, nitric oxide, hydrogen peroxide, and calcium in stomatal closing of Arabidopsis thaliana

  • Qing Li , Yi-Jie Wang , Chang-Kui Liu , Zhen-Ming Pei und Wu-Liang Shi EMAIL logo
Veröffentlicht/Copyright: 31. Oktober 2017
Veröffentlichen auch Sie bei De Gruyter Brill
Biologia
Aus der Zeitschrift Biologia Band 72 Heft 10

Abstract

Guard cells can integrate and process multiple complex signals from the environment and respond by opening and closing stomata in order to adapt to the environmental conditions changing. Over the past several years, considerable research progress has been made in our understanding of the role of calcium (Ca2+), nitric oxide (NO) and hydrogen peroxide (H2O2) as essential signal molecules that mediate abscisic acid (ABA)-induced stomatal closure. However, the sequence or epistasis of signaling cascade elements remains unknown. Here, we report that there are some relationships between extracellular Ca2+ induced cytosolic free Ca2+ increases (CICI) and ABA signal transduction in guard cell. ABA-induced stomatal closure in CASas mutant indicates that CAS activity is not required for ABA-induced stomatal closure, while exogenous Ca2+ failed to induce stomatal closure in CASas mutant and ABA-insensitive mutant, abi1 and abi2, indicating that extracellular Ca2+-induced stomatal closure via CAS requires some components of ABA signal pathway in guard cells. Hydrogen peroxide (H2O2), as a secondary messenger in the ABA-induced stomatal closure pathway, could not induce stomatal closure in CASas guard cells, it indicates that the functional CAS is required for H2O2 to induce stomatal closure. Nitric oxide (NO), another component of ABA-induced stomatal closure pathway, could induce stomatal closure in CASas guard cells while NO overproduction mutant-nox1 did not respond to exogenous high Ca2+, this demonstrates that NO acts downstream of CAS. Our results on the analysis of various Arabidopsis mutants indicate that NO and H2O2 maybe the points of connection between CICI and ABA signaling cascade in guard cell.

Acknowledgements

This research was supported by the project of technological guidance from College students’ innovative entrepreneurial training plan (2015821242 and 2015821269).

References

Allen G.J., Chu S.P., Schumacher K., Shimazaki C.T., Vafeados D., Kemper A., Hawke S.D., Tallman G., Tsien R.Y., Harper J.F., Chory J. & Schroeder J.I. 2000. Alteration of stimulus–specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Sci. 289: 2338–2342.10.1126/science.289.5488.2338Suche in Google Scholar

Allen G.J., Kuchitsu K., Chu S.P., Murata Y. & Schroeder J.I. 1999. Arabidopsis abi1–1 and abi2–1 phosphatase mutations reduce abscisic acid–induced cytoplasmic calcium rises in guard cells. Plant Cell 11: 1785–1798.10.1105/tpc.11.9.1785Suche in Google Scholar PubMed

Berridge M.J., Lipp P. & Bootman M. D. 2000. The versatility and universality of calcium signalling. Natur. Rev. Mol. Cell. Biol. 1: 11–21.10.1038/35036035Suche in Google Scholar

Clementi E. 1998. Role of nitric oxide and its intracellular signalling pathways in the control of Ca2+ homeostasis. Biochem. Pharmacol 55: 713–718.10.1016/S0006-2952(97)00375-4Suche in Google Scholar PubMed

Desikan R., Griffiths R., Hancock J. & Neill S. 2002. A new role for an old enzyme: nitrate reductase–mediated nitric oxide generation is required for abscisic acid–induced stomatal closure in Arabidopsis thaliana. Proc. Nat. Acad. Sci. USA. 99: 16314–16318.10.1073/pnas.252461999Suche in Google Scholar

Friso G., Giacomelli L., Ytterberg A.J., Peltier J.B., Rudella A., Sun Q. & Wijk K.J. 2004. In–depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16: 478–499.10.1105/tpc.017814Suche in Google Scholar

Garcia–Mata C., Gay R., Sokolovski S., Hills A., Lamattina L. & Blatt M.R. 2003. Nitric oxide regulates K+ and Cl channels in guard cells through a subset of abscisic acid–evoked signaling pathways. Proc. Nat. Acad. Sci. USA. 100: 11116–11121.10.1073/pnas.1434381100Suche in Google Scholar

Garcia–Mata C. & Lamattina L. 2003. Abscisic acid, nitric oxide and stomatal closure – is nitrate reductase one of the missing links? Trends. Plant Sci. 8: 20–26.10.1016/S1360-1385(02)00009-2Suche in Google Scholar

Gould K. S., Lamotte O., Klinguer A., Pugin A. & Wendehenne D. 2003. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26: 1851–1862.10.1046/j.1365-3040.2003.01101.xSuche in Google Scholar

Grabov, A., Blatt, M. R. 1998. Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proc. Nat. Acad. Sci. USA. 95: 4778–4783.10.1073/pnas.95.8.4778Suche in Google Scholar PubMed PubMed Central

Han S., Tang R., Anderson L. K., Woerner T. E., Pei Z. M. 2003. A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature 425: 196–200.10.1038/nature01932Suche in Google Scholar

Hetherington A.M. 2001. Guard cell signaling. Cell 107: 711–714.10.1016/S0092-8674(01)00606-7Suche in Google Scholar PubMed

Hetherington A.M. & Woodward F.I. 2003. The role of stomata in sensing and driving environmental change. Nature 424: 901–908.10.1038/nature01843Suche in Google Scholar PubMed

Irving H.R., Gehring C.A. & Parish R.W. 1992. Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc. Nat. Acad. Sci. USA. 89: 1790–1794.10.1073/pnas.89.5.1790Suche in Google Scholar PubMed PubMed Central

Lamotte O., Courtois C., Dobrowolska G., Besson A., Pugin A. & Wendehenne D. 2006. Mechanisms of nitric–oxide–induced increase of free cytosolic Ca2+ concentration in Nicotiana plumbaginifolia cells. Free Radic. Biol. Med. 40: 1369–1376.10.1016/j.freeradbiomed.2005.12.006Suche in Google Scholar PubMed

Lamotte O., Gould K., Lecourieux D., Sequeira–Legrand A., Lebrun–Garcia A., Durner J., Pugin A. & Wendehenne D. 2004. Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol. 135: 516–529.10.1104/pp.104.038968Suche in Google Scholar PubMed PubMed Central

Lemtiri–Chlieh F., MacRobbie E.A.C., Webb A.A.R., Manison N.F., Brownlee C., Skepper J.N., Chen J., Prestwich G. D. & Brearley C.A. 2003. Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc. Nat. Acad. Sci. USA. 100: 10091–10095.10.1073/pnas.1133289100Suche in Google Scholar PubMed PubMed Central

Leung J. & Giraudat J. 1998. Abscisic Acid Signal Transduction. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 49: 199–222.10.1146/annurev.arplant.49.1.199Suche in Google Scholar PubMed

McAinsh M., Brownlee C. & Hetherington A. 1990. ABA induced elevation of guard cell cytosolic calcium precedes stomatal closure in Commelina communis. Nature 343: 186–188.10.1038/343186a0Suche in Google Scholar

McAinsh M.R., Clayton H., Mansfield T.A. & Hetherington A.M. 1996. Changes in Stomatal Behavior and Guard Cell Cytosolic Free Calcium in Response to Oxidative Stress. Plant Physiol. 111: 1031–1042.10.1104/pp.111.4.1031Suche in Google Scholar PubMed PubMed Central

McAinsh M.R. & Hetherington A.M. 1998. Encoding specificity in Ca2+ signalling systems. Trends Plant Sci. 3: 32–36.10.1016/S1360-1385(97)01150-3Suche in Google Scholar

McAinsh M.R., Webb A., Taylor J.E. & Hetherington A.M. 1995. Stimulus–Induced Oscillations in Guard Cell Cytosolic Free Calcium. Plant Cell 7: 1207–1219.10.1105/tpc.7.8.1207Suche in Google Scholar PubMed PubMed Central

Neill S.J., Desikan R., Clarke A. & Hancock J.T. 2002. Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128: 13–16.10.1104/pp.010707Suche in Google Scholar PubMed

Nomura H., Komori T., Kobori M., Nakahira Y. & Shiina T. 2008. Evidence for chloroplast control of external Ca2+–induced cytosolic Ca2+ transients and stomatal closure. Plant J. 53: 988–998.10.1111/j.1365-313X.2007.03390.xSuche in Google Scholar PubMed

Pei Z.M., Kuchitsu K., Ward J.M., Schwarz M. & Schroeder J.I. 1997. Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild–type and abi1 and abi2 mutants. Plant Cell 9: 409–423.10.1105/tpc.9.3.409Suche in Google Scholar PubMed PubMed Central

Pei Z.M., Murata Y., Benning G., Thomine S., Klusener B., Allen G.J., Grill E. & Schroeder J.I. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731–734.10.1038/35021067Suche in Google Scholar PubMed

Peltier J.B., Ytterberg A.J., Sun Q. & van Wijk K.J. 2004. New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J. Biol. Chem. 279: 49367–49383.10.1074/jbc.M406763200Suche in Google Scholar PubMed

Schroeder J.I., Allen G.J., Hugouvieux V., Kwak J.M. & Waner D. 2001. Guard cell signal transduction. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 52: 627–658.10.1146/annurev.arplant.52.1.627Suche in Google Scholar PubMed

Schwartz A. 1985. Role of Ca and EGTA on Stomatal Movements in Commelina communis L. Plant Physiol. 79: 1003–1005.10.1104/pp.79.4.1003Suche in Google Scholar PubMed PubMed Central

Sheen J. 1998. Mutational analysis of protein phosphatase 2C involved in abscisic acid signal transduction in higher plants. Proc. Nat. Acad. Sci. USA. 95: 975–980.10.1073/pnas.95.3.975Suche in Google Scholar PubMed PubMed Central

Sokolovski S., Hills A., Gay R., Garcia–Mata C., Lamattina L. & Blatt M.R. 2005. Protein phosphorylation is a prerequisite for intracellular Ca2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. Plant J. 43: 520–529.10.1111/j.1365-313X.2005.02471.xSuche in Google Scholar PubMed

Tang R.H., Han S., Zheng H., Cook C.W., Choi C.S., Woerner T.E., Jackson R.B. & Pei Z.M. 2007. Coupling diurnal cytosolic Ca2+ oscillations to the CAS–IP3 pathway in Arabidopsis. Sci. 315: 1423–1426.10.1126/science.1134457Suche in Google Scholar PubMed

Vainonen J.P., Sakuragi Y., Stael S., Tikkanen M., Allahverdiyeva Y., Paakkarinen V., Aro E., Suorsa M., Scheller H. V., Vener A.V. & Aro E.M. 2008. Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. Febs J. 275: 1767–1777.10.1111/j.1742-4658.2008.06335.xSuche in Google Scholar PubMed

Vandelle E., Poinssot B., Wendehenne D., Bentejac M. & Alain P. 2006. Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen–activated protein kinases in BcPG1–elicited grapevine defenses. Mol. Plant Microbe Interact. 19: 429–440.10.1094/MPMI-19-0429Suche in Google Scholar PubMed

Wang P.T. & Song C.P. 2008. Guard–cell signalling for hydrogen peroxide and abscisic acid. New Phytologist 178: 703–718.10.1111/j.1469-8137.2008.02431.xSuche in Google Scholar PubMed

Weinl S., Held K., Schlucking K., Steinhorst L., Kuhlgert S., Hippler M. & Kudla J. 2008. A plastid protein crucial for Ca2+ – regulated stomatal responses. New Phytol. 179: 675–686.10.1111/j.1469-8137.2008.02492.xSuche in Google Scholar PubMed

Wu Y., Kuzma J., Marechal E., Graeff R., Lee H.C., Foster R. & Chua N.H. 1997. Abscisic acid signaling through cyclic ADP–ribose in plants. Sci. 278: 2126–2130.10.1126/science.278.5346.2126Suche in Google Scholar PubMed

Yang T. & Poovaiah B.W. 2003. Calcium/calmodulin–mediated signal network in plants. Trends Plant Sci. 8: 505–512.10.1016/j.tplants.2003.09.004Suche in Google Scholar PubMed

Abbreviations

CAS

Ca2+ sensing receptor

CASas

CAS antisense mutant

CICI

extracellular Ca2+ induced cytosolic free Ca2+ increases

H2O2

Hydrogen peroxide

NO

Nitric oxide

nox1

NO overproduction mutant

Received: 2016-11-20
Accepted: 2017-6-23
Published Online: 2017-10-31
Published in Print: 2017-10-26

© 2017 Institute of Botany, Slovak Academy of Sciences

Artikel in diesem Heft

  1. Cellular and Molecular Biology
  2. Therapeutic strategies to fight HIV-1 latency: progress and challenges
  3. Zoology
  4. Detection of schistosomiasis applicable for primary health care facilities in endemic regions of Africa
  5. Botany
  6. Genetic and morphological diversity in Geranium dissectum (Sec. Dissecta, Geraniaceae) populations
  7. Botany
  8. Optical properties of halophyte leaves are affected by the presence of salt on the leaf surface
  9. Botany
  10. The crosstalk between ABA, nitric oxide, hydrogen peroxide, and calcium in stomatal closing of Arabidopsis thaliana
  11. Botany
  12. Optimization of the pollen-tube pathway method of plant transformation using the Yellow Cameleon 3.6 calcium sensor in Solanum lycopersicum
  13. Cellular and Molecular Biology
  14. Differential effects of plant growth regulators on physiology, steviol glycosides content, and antioxidant capacity in micropropagated tissues of Stevia rebaudiana
  15. Zoology
  16. Characteristics of matrix of the invasive freshwater Ectoprocta species Pectinatella magnifica
  17. Zoology
  18. Relative growth and reproductive cycle of the hermaphroditic Cardites antiquatus (Mollusca: Bivalvia) collected from the Bizerte channel (northern Tunisia)
  19. Zoology
  20. Tegolophus glycyglabri sp. n. (Trombidiformes: Eriophyidae), a new species from Iran
  21. Zoology
  22. Karyotype characteristics and polymorphism peculiarities of Chironomus luridus (Diptera: Chironomidae) from Central and Northwest Caucasus
  23. Zoology
  24. Reptile surveys reveal high species richness in areas recovering from mining activity in the Brazilian Cerrado
  25. Zoology
  26. The porcupine as “Little Thumbling”: The role of Hystrix cristata in the spread of Helianthus tuberosus
  27. Cellular and Molecular Biology
  28. Distribution of telocytes in the corpus and cervix of human uterus: an immunohistochemical study
  29. Zoology
  30. First record of mermithid larva (Nematoda: Mermithidae) in Anopheles maculipennis complex (Diptera: Culicidae) imago in Central-Europe
Heruntergeladen am 21.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biolog-2017-0126/html
Button zum nach oben scrollen