Gasotransmitters and stomatal closure: Is there redundancy, concerted action, or both?

Frontiers in Plant Science

Volumn 7, Issue MAR2016, 2016, Pages

  Scuffi, Denise ^a   Lamattina, Lorenzo ^a   García Mata, Carlos ^a  

^a UNIVERSIDAD NACIONAL DE MAR DEL PLATA   (Argentina)

Author keywords

Gasotransmitter; Guard cell signaling; Hydrogen sulfide; Nitric oxide

Indexed keywords

EID: 84961712576     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00277     Document Type: Article

References (49)

1. Alvarez, C. Calo, L. Romero, L. C. García, I. and Gotor, C. (2010). An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol. 152, 656-669. doi: 10. 1104/pp. 109. 147975
2. Aroca, Á. Serna, A. Gotor, C. and Romero, L. C. (2015). S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol. 168, 334-342. doi: 10. 1104/pp. 15. 00009
3. Blatt, M. R. (2000). Cellular signaling and volume control in stomatal movements in plants. Annu. Rev. Cell Dev. Biol. 16, 221-241. doi: 10. 1146/annurev. cellbio. 16. 1. 221
4. Bright, J. Desikan, R. Hancock, J. T. Weir, I. S. and Neill, S. J. (2006). ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J. 45, 113-122. doi: 10. 1111/j. 1365-313X. 2005. 02615. x
5. Cao, Z. Huang, B. Wang, Q. Xuan, W. Ling, T. Zhang, B. et al. (2007). Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure inVicia faba and its proposed signal transduction pathway. Chin. Sci. Bull. 52, 2365-2373. doi: 10. 1007/s11434-007-0358-y
6. Castillo, M.-C. Lozano-Juste, J. González-Guzman, M. Rodriguez, L. Rodriguez, P. L. and Leon, J. (2015). Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci. Signal. 8, ra89. doi: 10. 1126/scisignal. aaa7981
7. Coletta, C. Papapetropoulos, A. Erdelyi, K. Olah, G. Módis, K. Panopoulos, P. et al. (2012). Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc. Natl. Acad. Sci. U. S. A. 109, 9161-9166. doi: 10. 1073/pnas. 1202916109
8. Cortese-Krott, M. M. Fernandez, B. O. Kelm, M. Butler, A. R. and Feelisch, M. (2015a). On the chemical biology of the nitrite/sulfide interaction. Nitric Oxide 46, 14-24. doi: 10. 1016/j. niox. 2014. 12. 009
9. Cortese-Krott, M. M. Fernandez, B. O. Santos, J. L. T. Mergia, E. Grman, M. Nagy, P. et al. (2014). Nitrosopersulfide (SSNO-) accounts for sustained NO bioactivity of S-nitrosothiols following reaction with sulfide. Redox Biol. 2, 234-244. doi: 10. 1016/j. redox. 2013. 12. 031
10. 2S interaction are S/N-hybrid species, polysulfides, and nitroxyl. Proc. Natl. Acad. Sci. U. S. A. 112, E4651-E4660. doi: 10. 1073/pnas. 1509277112
11. Cvetkovska, M. Dahal, K. Alber, N. A. Jin, C. Cheung, M. and Vanlerberghe, G. C. (2014). Knockdown of mitochondrial alternative oxidase induces the "stress state" of signaling molecule pools in Nicotiana tabacum, with implications for stomatal function. New Phytol. 203, 449-461. doi: 10. 1111/nph. 12773
12. García, I. Castellano, J. M. Vioque, B. Solano, R. Gotor, C. and Romero, L. C. (2010). Mitochondrial beta-cyanoalanine synthase is essential for root hair formation inArabidopsis thaliana. Plant Cell 22, 3268-3279. doi: 10. 1105/tpc. 110. 076828
13. Garcia-Mata, C. Gay, R. Sokolovski, S. Hills, A. Blatt, M. R. and Lamattina, L. (2003). Nitric oxide regulates K+ and Cl-channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc. Natl. Acad. Sci. U. S. A. 100, 11116-11121. doi: 10. 1073/pnas. 1434381100
14. García-Mata, C. and Lamattina, L. (2002). Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol. 128, 790-792. doi: 10. 1104/pp. 011020
15. García-Mata, C. and Lamattina, L. (2010). Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol. 188, 977-984. doi: 10. 1111/j. 1469-8137. 2010. 03465. x
16. García-Mata, C. and Lamattina, L. (2013). Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci. 201-202, 66-73. doi: 10. 1016/j. plantsci. 2012. 11. 007
17. He, J.-M. Zhang, Z. Wang, R.-B. and Chen, Y.-P. (2011). UV-B-induced stomatal closure occurs via ethylene-dependent NO generation in Vicia faba. Funct. Plant Biol. 38, 293. doi: 10. 1071/FP10219
18. Honda, K. Yamada, N. Yoshida, R. Ihara, H. Sawa, T. Akaike, T. et al. (2015). 8-Mercapto-cyclic GMP mediates hydrogen sulfide-induced stomatal closure in Arabidopsis. Plant Cell Physiol. 56, 1481-1489. doi: 10. 1093/pcp/pcv069
19. Hou, Z. Wang, L. Liu, J. Hou, L. and Liu, X. (2013). Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. J. Integr. Plant Biol. 55, 277-289. doi: 10. 1111/jipb. 12004
20. Hu, K.-D. Tang, J. Zhao, D.-L. Hu, L.-Y. Li, Y.-H. Liu, Y.-S. et al. (2014). Stomatal closure in sweet potato leaves induced by sulfur dioxide involves H2S and NO signaling pathways. Biol. Plant. 58, 676-680. doi: 10. 1007/s10535-014-0440-7
21. Jiang, B. Tang, G. Cao, K. Wu, L. and Wang, R. (2010). Molecular mechanism for H(2)S-induced activation of K(ATP) channels. Antioxid. Redox Signal. 12, 1167-1178. doi: 10. 1089/ars. 2009. 2894
22. Jin, Z. Shen, J. Qiao, Z. Yang, G. Wang, R. and Pei, Y. (2011). Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 414, 481-486. doi: 10. 1016/j. bbrc. 2011. 09. 090
23. Joudoi, T. Shichiri, Y. Kamizono, N. Akaike, T. Sawa, T. Yoshitake, J. et al. (2013). Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis. Plant Cell 25, 558-571. doi: 10. 1105/tpc. 112. 105049
24. Kim, T.-H. Böhmer, M. Hu, H. Nishimura, N. and Schroeder, J. I. (2010). Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 61, 561-591. doi: 10. 1146/annurev-arplant-042809-112226
25. Kolluru, G. K. Shen, X. and Kevil, C. G. (2013). A tale of two gases: NO and H2S, foes or friends for life? Redox Biol. 1, 313-318. doi: 10. 1016/j. redox. 2013. 05. 001
26. Kubo, S. Kurokawa, Y. Doe, I. Masuko, T. Sekiguchi, F. and Kawabata, A. (2007). Hydrogen sulfide inhibits activity of three isoforms of recombinant nitric oxide synthase. Toxicology 241, 92-97. doi: 10. 1016/j. tox. 2007. 08. 087
27. Lisjak, M. Srivastava, N. Teklic, T. Civale, L. Lewandowski, K. Wilson, I. et al. (2010). A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol. Biochem. 48, 931-935. doi: 10. 1016/j. plaphy. 2010. 09. 016
28. Lisjak, M. Teklić, T. Wilson, I. D. Wood, M. Whiteman, M. and Hancock, J. T. (2011). Hydrogen sulfide effects on stomatal apertures. Plant Signal. Behav. 6, 1444-1446. doi: 10. 4161/psb. 6. 10. 17104
29. Liu, J. Hou, L. Liu, G. Liu, X. and Wang, X. (2011). Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chin. Sci. Bull. 56, 3547-3553. doi: 10. 1007/s11434-011-4819-y
30. Liu, J. Hou, Z. Liu, G. Hou, L. and Liu, X. (2012). Hydrogen sulfide may function downstream of nitric oxide in ethylene-induced stomatal closure in Vicia faba L. J. Integr. Agric. 11, 1644-1653. doi: 10. 1016/S2095-3119(12)60167-1
31. Lo Faro, M. L. Fox, B. Whatmore, J. L. Winyard, P. G. and Whiteman, M. (2014). Hydrogen sulfide and nitric oxide interactions in inflammation. Nitric Oxide 41, 38-47. doi: 10. 1016/j. niox. 2014. 05. 014
32. Lozano-Juste, J. and León, J. (2010). Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR-and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol. 152, 891-903. doi: 10. 1104/pp. 109. 148023
33. Moreau, M. Lee, G. I. Wang, Y. Crane, B. R. and Klessig, D. F. (2008). AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J. Biol. Chem. 283, 32957-32967. doi: 10. 1074/jbc. M804838200
34. Mustafa, A. K. Gadalla, M. M. Sen, N. Kim, S. Mu, W. Gazi, S. K. et al. (2009a). H2S signals through protein S-sulfhydration. Sci. Signal. 2, ra72. doi: 10. 1126/scisignal. 2000464
35. Mustafa, A. K. Gadalla, M. M. and Snyder, S. H. (2009b). Signaling by gasotransmitters. Sci. Signal. 2, re2. doi: 10.1126/scisignal.268re2
36. Neill, S. J. Desikan, R. Clarke, A. and Hancock, J. T. (2002). Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128, 13-16. doi: 10. 1104/pp. 010707. shown
37. Papanatsiou, M. Scuffi, D. Blatt, M. R. and García-Mata, C. (2015). Hydrogen sulphide regulates inward-rectifying K+ channels in conjunction with stomatal closure. Plant Physiol. 168, 29-35. doi: 10. 1104/pp. 114. 256057
38. Predmore, B. L. Julian, D. and Cardounel, A. J. (2011). Hydrogen sulfide increases nitric oxide production from endothelial cells by an Akt-dependent mechanism. Front. Physiol. 2:104. doi: 10. 3389/fphys. 2011. 00104
39. Scuffi, D. Álvarez, C. Laspina, N. Gotor, C. Lamattina, L. and Garcia-Mata, C. (2014). Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol. 166, 2065-2076. doi: 10. 1104/pp. 114. 245373
40. She, X.-P. and Song, X.-G. (2008). Carbon monoxide-induced stomatal closure involves generation of hydrogen peroxide in Vicia faba guard cells. J. Integr. Plant Biol. 50, 1539-1548. doi: 10. 1111/j. 1744-7909. 2008. 00716. x
41. Shekhawat, G. S. and Verma, K. (2010). Haem oxygenase (HO): an overlooked enzyme of plant metabolism and defence. J. Exp. Bot. 61, 2255-2270. doi: 10. 1093/jxb/erq074
42. Sokolovski, S. Hills, A. Gay, R. Garcia-mata, C. Lamattina, L. and 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. doi: 10. 1111/j. 1365-313X. 2005. 02471. x
43. Song, X.-G. She, X.-P. Wang, J. and Sun, Y.-C. (2011). Ethylene inhibits darkness-induced stomatal closure by scavenging nitric oxide in guard cells of Vicia faba. Funct. Plant Biol. 38, 767-777. doi: 10. 1071/FP11055
44. Song, Y. Miao, Y. and Song, C. (2014). Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol. 201, 1121-1140. doi: 10. 1111/nph. 12565
45. Suh, S. J. Wang, Y. F. Frelet, A. Leonhardt, N. Klein, M. Forestier, C. et al. (2007). The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in Arabidopsis guard cells. J. Biol. Chem. 282, 1916-1924. doi: 10. 1074/jbc. M607926200
46. Wang, P. Du, Y. Hou, Y.-J. Zhao, Y. Hsu, C.-C. Yuan, F. et al. (2015). Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc. Natl. Acad. Sci. U. S. A. 112, 613-618. doi: 10. 1073/pnas. 1423481112
47. Wang, R. (2002). Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J. 16, 1792-1798. doi: 10. 1096/fj. 02-0211hyp
48. Xiao, M. Ma, J. Li, H. Jin, H. and Feng, H. (2010). Effects of hydrogen sulfide on alternative pathway respiration and induction of alternative oxidase gene expression in rice suspension cells. Z. Naturforsch. C. 65, 463-471. doi: 10. 1515/znc-2010-7-808
49. Zhao, W. Zhang, J. Lu, Y. and Wang, R. (2001). The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. EMBO J. 20, 6008-6016. doi: 10. 1093/emboj/20. 21. 6008