Advertisement

Planta

, Volume 244, Issue 4, pp 831–841 | Cite as

Stomatal closure induced by phytosphingosine-1-phosphate and sphingosine-1-phosphate depends on nitric oxide and pH of guard cells in Pisum sativum

  • Mallikarjuna Rao Puli
  • Pidakala Rajsheel
  • Vetcha Aswani
  • Srinivas Agurla
  • Kazuyuki Kuchitsu
  • Agepati S. RaghavendraEmail author
Original Article

Abstract

Main conclusion

Phyto-S1P and S1P induced stomatal closure in epidermis of pea ( Pisum sativum ) by raising the levels of NO and pH in guard cells.

Phosphosphingolipids, such as phytosphingosine-1-phosphate (phyto-S1P) and sphingosine-1-phosphate (S1P), are important signaling components during drought stress. The biosynthesis of phyto-S1P or S1P is mediated by sphingosine kinases (SPHKs). Although phyto-S1P and S1P are known to be signaling components in higher plants, their ability to induce stomatal closure has been ambiguous. We evaluated in detail the effects of phyto-S1P, S1P and SPHK inhibitors on signaling events leading to stomatal closure in the epidermis of Pisum sativum. Phyto-S1P or S1P induced stomatal closure, along with a marked rise in nitric oxide (NO) and cytoplasmic pH of guard cells, as in case of ABA. Two SPHK inhibitors, DL-threo dihydrosphingosine and N’,N’-dimethylsphingosine, restricted ABA-induced stomatal closure and prevented the increase of NO or pH by ABA. Modulators of NO or pH impaired both stomatal closure and increase in NO or pH by phyto-S1P/S1P. The stomatal closure by phyto-S1P/S1P was mediated by phospholipase D and phosphatidic acid (PA). When present, PA elevated the levels of pH, but not NO of guard cells. Our results demonstrate that stomatal closure induced by phyto-S1P and S1P depends on rise in pH as well as NO of guard cells. A scheme of signaling events initiated by phyto-S1P/S1P, and converging to cause stomatal closure, is proposed.

Keywords

Abscisic acid LCB signaling Pea Phosphosphingolipids Sphingosine kinase Stomata 

Abbreviations

ABA

Abscisic acid

DL-threo DHS

DL-threo dihydrosphingosine

DMS

N’,N’-dimethylsphingosine

LCB

Long chain base

LCBP

Long chain base phosphate

NO

Nitric oxide

PA

Phosphatidic acid

PLD

Phospholipase D

phyto-S1P

Phytosphingosine-1-phosphate

S1P

Sphingosine-1-phosphate

SLAC

Slow anion channel

SPHK

Sphingosine kinase

Notes

Acknowledgments

This work was supported by grants (to ASR) from the Department of Biotechnology (No. BT/PR9227/PBD/16/748/2007), Council of Scientific and Industrial Research (CSIR, No. 38(1195)/08/EMR-II), JC Bose Fellow of Department of Science and Technology (No. SR/S2/JCB-06/2006), and Department of Science and Technology-Japanese Society for Promotion of Science (No. DST/INT/JSPS/P-121/10) project (to ASR & KK). MRP, PR, VA, and SA were all supported by Research Fellowships from CSIR/UGC, New Delhi, India. The facilities in our Department and School were supported by grants from DST-FIST, UGC-SAP-CAS and DBT-CREBB, all from New Delhi, India. We thank Ms Nalini, Technical Assistant, Central Instrumentation Laboratory, for her help in using the confocal microscope.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

References

  1. Blatt MR (2000) Cellular movements and volume control in stomatal movements in plants. Annu Rev Cell Dev Biol 16:221–241CrossRefPubMedGoogle Scholar
  2. Cantrel C, Vazquez T, Puyaubert J, Rezé N, Lesch M, Kaiser WM, Dutilleul C, Guillas I, Zachowski A, Baudouin E (2011) Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytol 189:415–427CrossRefPubMedGoogle Scholar
  3. Chalfant CE, Speigel S (2005) Sphingosine 1-phosphate and ceramide 1-phosphate: expanding roles in cell signaling. J Cell Sci 118:4605–4612CrossRefPubMedGoogle Scholar
  4. Coursol S, Fan LM, Stunff HL, Spiegel S, Gilroy S, Assmann SM (2003) Sphingolipid signaling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423:651–654CrossRefPubMedGoogle Scholar
  5. Coursol S, Stunff HL, Lynch DV, Gilroy S, Assmann SM, Spiegel S (2005) Arabidopsis sphingosine kinase and the effects of phytosphingosine-1-phospate on stomatal aperture. Plant Physiol 137:724–737CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679CrossRefPubMedGoogle Scholar
  7. Da Silva D, Lachaud C, Cotelle V, Brière C, Grat S, Mazars C, Thuleau P (2011) Nitric oxide production is not required for dihydrosphingosine-induced cell death in tobacco BY-2 cells. Plant Signal Behav 6:736–739CrossRefPubMedPubMedCentralGoogle Scholar
  8. Distéfano AM, Scuffi D, García-Mata C, Lamattina L, Laxalt AM (2012) Phospholipase Dδ is involved in nitric oxide-induced stomatal closure. Planta 236:1899–1907CrossRefPubMedGoogle Scholar
  9. García-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol 128:790–792CrossRefPubMedPubMedCentralGoogle Scholar
  10. García-Mata C, Lamattina L (2013) Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201–202:66–73CrossRefPubMedGoogle Scholar
  11. Gardiner J, Collings DA, Harper JD, Marc J (2003) The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis. Plant Cell Physiol 44:687–696CrossRefPubMedGoogle Scholar
  12. Gayatri G, Agurla S, Raghavendra AS (2013) Nitric oxide in guard cells as an important secondary messenger during stomatal closure. Front Plant Sci 4:425CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gonugunta VK, Srivastava N, Puli MR, Raghavendra AS (2008) Nitric oxide production occurs after cytosolic alkalinization during stomatal closure induced by abscisic acid. Plant Cell Environ 31:1717–1724CrossRefPubMedGoogle Scholar
  14. Guillas I, Zachowski A, Baudouin E (2011) A matter of fat: interaction between nitric oxide and sphingolipid signaling in plant cold response. Plant Signal Behav 6:140–142CrossRefPubMedPubMedCentralGoogle Scholar
  15. Guillas I, Puyaubert J, Baudouin E (2013) Nitric oxide-sphingolipid interplays in plant signaling: a new enigma from the Sphinx? Front Plant Sci 4:1–7CrossRefGoogle Scholar
  16. Guo L, Mishra G, Taylor K, Wang X (2011) Phosphatidic acid binds and stimulates Arabidopsis sphingosine kinases. J Biol Chem 286:13336–13345CrossRefPubMedPubMedCentralGoogle Scholar
  17. Guo L, Wang X (2012) Crosstalk between phospholipase D and sphingosine kinase in plant stress signaling. Front Plant Sci 3:1–7CrossRefGoogle Scholar
  18. Guo L, Mishra G, Markham J, Li M, Tawfall A, Welti R et al (2012) Connections between sphingosine kinase and phospholipase D in the abscisic acid signaling pathway in Arabidopsis. J Biol Chem 287:8286–8296CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24:1695–1708CrossRefPubMedPubMedCentralGoogle Scholar
  20. Irving HR, Gehring CA, Parish RW (1992) Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc Natl Acad Sci USA 89:1790–1794CrossRefPubMedPubMedCentralGoogle Scholar
  21. Islam MM, Hossain MA, Jannat R, Munemasa S, Nakamura Y, Mori IC, Murata Y (2010) Cytosolic alkalization and cytosolic calcium oscillation in Arabidopsis guard cells response to ABA and MeJA. Plant Cell Physiol 51:1721–1730CrossRefPubMedGoogle Scholar
  22. Islam MN, Jacquemot MP, Coursol S, Ng CKY (2012) Sphingosine in plants: more riddles from the sphinx? New Phytol 193:51–57CrossRefPubMedGoogle Scholar
  23. Joshi-Saha A, Valon C, Leung J (2011) A brand new START: abscisic acid perception and transduction in the guard cell. Sci Signal 4:re4CrossRefPubMedGoogle Scholar
  24. Kim TH, 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 61:561–591CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kolla AR, Raghavendra AS (2007) Nitric oxide is a signaling intermediate during bicarbonate-induced stomatal closure in Pisum sativum. Physiol Plant 130:91–98CrossRefGoogle Scholar
  26. Lynch DV, Chen M, Cahoon EB (2009) Lipid signaling in Arabidopsis: no sphingosine? No problem! Trends Plant Sci 14:463–466CrossRefPubMedGoogle Scholar
  27. Ma Y, She X, Yang S (2012) Sphingosine-1-phosphate (S1P) mediates darkness-induced stomatal closure through raising cytosol pH and hydrogen peroxide (H2O2) levels in guard cells in Vicia faba. Sci China Life Sci 55:974–983CrossRefPubMedGoogle Scholar
  28. Michaelson LV, Zäuner S, Markham JE, Haslam RP, Desikan R, Mugford S, Albrecht S, Warnecke D, Sperling P, Heinz E, Napier JA (2009) Functional characterization of a higher plant sphingolipid Δ4-desaturase: defining the role of sphingosine and sphingosine-1-phosphate in Arabidopsis. Plant Physiol 149:487–498CrossRefPubMedPubMedCentralGoogle Scholar
  29. Minamioka H, Imai H (2009) Sphingoid long-chain base composition of glucosylceramides in Fabaceae: a phylogenetic interpretation of Fabaceae. J Plant Res 122:415–419CrossRefPubMedGoogle Scholar
  30. Mori IC, Murata Y (2011) ABA signaling in stomatal guard cells: lessons from Commelina and Vicia. J Plant Res 124:477–487CrossRefPubMedGoogle Scholar
  31. Nakagawa N, Kato M, Takahashi Y, Shimazaki K, Tamura K, Tokuji Y et al (2012) Degradation of long chain base-1-phosphate (LCBP) in Arabidopsis: functional characterization of LCBP phosphatase involved in the dehydration stress response. J Plant Res 125:439–449CrossRefPubMedGoogle Scholar
  32. Ng CKY, Carr K, McAinsh MR, Powell B, Hetherington AM (2001) Drought-induced guard cell signal transduction involves sphingosine 1-phosphate. Nature 410:596–599CrossRefPubMedGoogle Scholar
  33. Puli MR, Raghavendra AS (2012) Pyrabactin, an ABA agonist, induced stomatal closure and changes in signaling components of guard cell in abaxial epidermis of Pisum sativum. J Exp Bot 63:1349–1356CrossRefPubMedGoogle Scholar
  34. Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signaling. Trends Plant Sci 15:395–401CrossRefPubMedGoogle Scholar
  35. Sheard LB, Zheng N (2009) Signal advance for abscisic acid. Nature 462:575–576CrossRefPubMedGoogle Scholar
  36. Sirichandra C, Wasilewska A, Vlad F, Valon C, Leung J (2009) The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. J Exp Bot 60:1439–1463CrossRefPubMedGoogle Scholar
  37. Song Y, Miao Y, Song CP (2014) Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol 201:1121–1140CrossRefPubMedGoogle Scholar
  38. Spiegel S, Milstien S (2002) Sphingosine 1-phosphate a key cell signaling molecule. J Biol Chem 277:25851–25854CrossRefPubMedGoogle Scholar
  39. Srivastava N, Gonugunta VK, Puli MR, Raghavendra AS (2009) Nitric oxide production occurs downstream of reactive oxygen species in guard cells during stomatal closure induced by chitosan in abaxial epidermis of Pisum sativum. Planta 229:757–765CrossRefPubMedGoogle Scholar
  40. Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545CrossRefPubMedPubMedCentralGoogle Scholar
  41. Uraji M, Katagiri T, Okuma E, Ye W, Hossain MA, Masuda C et al (2012) Cooperative function of PLDδ and PLDα1in abscisic acid induced stomatal closure. Plant Physiol 159:450–460CrossRefPubMedPubMedCentralGoogle Scholar
  42. Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G et al (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signaling. Nature 452:487–493CrossRefPubMedPubMedCentralGoogle Scholar
  43. Worrall D, Liang YK, Alvarez S, Holroyd GH, Spiegel S, Panagopulos M et al (2008) Involvement of sphingosine kinase in plant cell signaling. Plant J 56:64–72CrossRefPubMedPubMedCentralGoogle Scholar
  44. Zhang W (2011) Roles of heterotrimeric G proteins in guard cell ion channel regulation. Plant Signal Behav 6:986–990CrossRefPubMedPubMedCentralGoogle Scholar
  45. Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci USA 101:9508–9513CrossRefPubMedPubMedCentralGoogle Scholar
  46. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R et al (2009) Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Mallikarjuna Rao Puli
    • 1
  • Pidakala Rajsheel
    • 1
  • Vetcha Aswani
    • 1
  • Srinivas Agurla
    • 1
  • Kazuyuki Kuchitsu
    • 2
  • Agepati S. Raghavendra
    • 1
    Email author
  1. 1.Department of Plant Sciences, School of Life SciencesUniversity of HyderabadHyderabadIndia
  2. 2.Department of Applied Biological SciencesTokyo University of ScienceNodaJapan

Personalised recommendations