Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure

Plant Physiology

Volumn 166, Issue 4, 2014, Pages 2065-2076

  Scuffi, Denise ^a   Álvarez, Consolación ^b   Laspina, Natalia ^a   Gotor, Cecilia ^b   Lamattina, Lorenzo ^a   García Mata, Carlos ^a  

^a UNIVERSIDAD NACIONAL DE MAR DEL PLATA   (Argentina)

^b CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; CELL SURFACE RECEPTOR; CYSTATHIONINE GAMMA LYASE; CYSTEINE; DES1 PROTEIN, ARABIDOPSIS; HYDROGEN SULFIDE; NITRIC OXIDE; PHYTOHORMONE; PYL2 PROTEIN, ARABIDOPSIS; PYL4 PROTEIN, ARABIDOPSIS; PYR1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; CYTOSOL; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PLANT STOMA; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYSTATHIONINE GAMMA-LYASE; CYSTEINE; CYTOSOL; HYDROGEN SULFIDE; MEMBRANE TRANSPORT PROTEINS; NITRIC OXIDE; PLANT GROWTH REGULATORS; PLANT STOMATA; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 84914166686     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.245373     Document Type: Article

References (75)

1. L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152: 656-669.
2. Álvarez C, García I, Moreno I, Pérez-Pérez ME, Crespo JL, Romero LC, Gotor C (2012) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24: 4621-4634.
3. Blatt MR (2000) Cellular signaling and volume control in stomatal movements in plants. Annu Rev Cell Dev Biol 16: 221-241.
4. L-cysteine desulphydrase activity in Brassica napus L. J Exp Bot 55: 2305-2312.
5. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
6. Coletta C, Papapetropoulos A, Erdelyi K, Olah G, Módis K, Panopoulos P, Asimakopoulou A, Gerö D, Sharina I, Martin E, et al (2012) Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci USA 109: 9161-9166.
7. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiol 133: 462-469.
8. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61: 651-679.
9. 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 Natl Acad Sci USA 99: 16314-16318.
10. Distéfano AM, García-Mata C, Lamattina L, Laxalt AM (2008) Nitric oxide-induced phosphatidic acid accumulation: a role for phospholipases C and D in stomatal closure. Plant Cell Environ 31: 187-194.
11. Dubovskaya LV, Bakakina YS, Kolesneva EV, Sodel DL, McAinsh MR, Hetherington AM, Volotovski ID (2011) cGMP-dependent ABAinduced stomatal closure in the ABA-insensitive Arabidopsis mutant abi1-1. New Phytol 191: 57-69.
12. 2S and NO interplay: hydrogen sulfide and nitroprusside react directly to give nitroxyl (HNO). A new pharmacological source of HNO. J Med Chem 56: 1499-1508.
13. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462: 660-664.
14. García-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol 128: 790-792.
15. García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188: 977-984.
16. 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: 66-73.
17. Harrington HM, Smith IK (1980) Cysteine metabolism in cultured tobacco cells. Plant Physiol 65: 151-155.
18. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901-908.
19. Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414: 481-486.
20. Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62: 41-46.
21. Kabil O, Banerjee R (2010) Redox biochemistry of hydrogen sulfide. J Biol Chem 285: 21903-21907.
22. 2S gas biology. Antioxid Redox Signal 13: 157-192.
23. 2+ signaling. Annu Rev Plant Biol 61: 561-591.
24. 2S, foes or friends for life? Redox Biol 1: 313-318.
25. Kubo S, Kurokawa Y, Doe I, Masuko T, Sekiguchi F, Kawabata A (2007) Hydrogen sulfide inhibits activity of three isoforms of recombinant nitric oxide synthase. Toxicology 241: 92-97.
26. Kuhn JM, Boisson-Dernier A, Dizon MB, Maktabi MH, Schroeder JI (2006) The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol 140: 127-139.
27. Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16: 596-615.
28. Leonhardt N, Vavasseur A, Forestier C (1999) ATP binding cassette modulators control abscisic acid-regulated slow anion channels in guard cells. Plant Cell 11: 1141-1152.
29. Li L, Bhatia M, Moore PK (2006) Hydrogen sulphide: a novel mediator of inflammation? Curr Opin Pharmacol 6: 125-129.
30. Li L, Hsu A, Moore PK (2009) Actions and interactions of nitric oxide, carbon monoxide and hydrogen sulphide in the cardiovascular system and in inflammation: a tale of three gases! Pharmacol Ther 123: 386-400.
31. Li L, Wang Y, Shen W (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25: 617-631.
32. Li ZG, Ding XJ, Du PF (2013a) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170: 741-747.
33. Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013b) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36: 1564-1572.
34. Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48: 931-935.
35. Lisjak M, Teklic T, Wilson ID, Wood M, Whiteman M, Hancock JT (2011) Hydrogen sulfide effects on stomatal apertures. Plant Signal Behav 6: 1444-1446.
36. Liu J, Hou L, Liu G, Liu X, Wang X (2011) Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chin Sci Bull 56: 3547-3553.
37. Liu J, Hou Z, Liu G, Hou L, 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.
38. López-Martín MC, Becana M, Romero LC, Gotor C (2008) Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol 147: 562-572.
39. Lozano-Juste J, 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.
40. 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: 1064-1068.
41. Mancardi D, Penna C, Merlino A, Del Soldato P, Wink DA, Pagliaro P (2009) Physiological and pharmacological features of the novel gasotransmitter: hydrogen sulfide. Biochim Biophys Acta 1787: 864-872.
42. Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25: 295-303.
43. 2S signals through protein S-sulfhydration. Sci Signal 2: ra72.
44. Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128: 13-16.
45. Nishimura N, Sarkeshik A, Nito K, Park SY, Wang A, Carvalho PC, Lee S, Caddell DF, Cutler SR, Chory J, et al (2010) PYR/PYL/RCAR family members are major in vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61: 290-299.
46. - donor NaHS releases nitric oxide from nitrosothiols, metal nitrosyl complex, brain homogenate and murine L1210 leukaemia cells. Pflugers Arch 457: 271-279.
47. Pandey S, Wang XQ, Coursol SA, Assmann SM (2002) Preparation and applications of Arabidopsis thaliana guard cell protoplasts. New Phytol 153: 517-526.
48. 2S-releasing enzymes of higher plants: from the field to the test tube and back. Plant Biol (Stuttg) 9: 582-588.
49. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TFF, et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071.
50. 2 sensing in the carotid body. Proc Natl Acad Sci USA 107: 10719-10724.
51. Ribeiro DM, Desikan R, Bright J, Confraria A, Harrison J, Hancock JT, Barros RS, Neill SJ, Wilson ID (2009) Differential requirement for NO during ABA-induced stomatal closure in turgid and wilted leaves. Plant Cell Environ 32: 46-57.
52. Rubio S, Rodrigues A, Saez A, Dizon MB, Galle A, Kim TH, Santiago J, Flexas J, Schroeder JI, Rodriguez PL (2009) Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid. Plant Physiol 150: 1345-1355.
53. Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, Rodriguez PL (2004) Gain-of-function and lossof-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J 37: 354-369.
54. Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Márquez JA, Cutler SR, Rodriguez PL (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60: 575-588.
55. Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65: 67-74.
56. Szabó C (2007) Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6: 917-935.
57. Tossi V, Amenta M, Lamattina L, Cassia R (2011) Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway. Plant Cell Environ 34: 909-921.
58. Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 106: 17588-17593.
59. Van Hoewyk D, Pilon M, Pilon-Smits EAH (2008) The functions of NifSlike proteins in plant sulfur and selenium metabolism. Plant Sci 174: 117-123.
60. 2S be the third endogenous gaseous transmitter? FASEB J 16: 1792-1798.
61. Wang RS, Pandey S, Li S, Gookin TE, Zhao Z, Albert R, Assmann SM (2011) Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells. BMC Genomics 12: 216.
62. 2+ channels at the plasma membrane of intact Arabidopsis guard cells. Plant Physiol 163: 566-577.
63. Whiteman M, Li L, Kostetski I, Chu SH, Siau JL, Bhatia M, Moore PK (2006) Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide. Biochem Biophys Res Commun 343: 303-310.
64. Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222: 377-383.
65. 2S in rat insulin-secreting cells and the underlying mechanisms. J Physiol 569: 519-531.
66. Yin Y, Adachi Y, Ye W, Hayashi M, Nakamura Y, Kinoshita T, Mori IC, Murata Y (2013) Difference in abscisic acid perception mechanisms between closure induction and opening inhibition of stomata. Plant Physiol 163: 600-610.
67. Yong QC, Hu LF, Wang S, Huang D, Bian JS (2010) Hydrogen sulfide interacts with nitric oxide in the heart: possible involvement of nitroxyl. Cardiovasc Res 88: 482-491.
68. Zeier J, Delledonne M, Mishina T, Severi E, Sonoda M, Lamb C (2004) Genetic elucidation of nitric oxide signaling in incompatible plantpathogen interactions. Plant Physiol 136: 2875-2886.
69. Zhang H, Dou W, Jiang CX, Wei ZJ, Liu J, Jones RL (2010a) Hydrogen sulfide stimulates b-amylase activity during early stages of wheat grain germination. Plant Signal Behav 5: 1031-1033.
70. Zhang H, Jiao H, Jiang CX, Wang SH, Wei ZJ, Luo JP, Jones RL (2010b) Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol Plant 32: 849-857.
71. Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010c) Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 52: 556-567.
72. Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51: 1086-1094.
73. Zhang H, Wang MJ, Hu LY, Wang SH, Hu KD, Bao LJ, Luo JP (2010d) Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ J Plant Physiol 57: 532-539.
74. Zhang H, Ye Y, Wang SH, Luo J, Tang J, Ma DF (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58: 243-250.
75. Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase D a 1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci USA 101: 9508-9513 2076.