Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis

Plant Physiology

Volumn 165, Issue 2, 2014, Pages 759-773

  Xie, Yanjie ^a   Mao, Yu ^a   Zhang, Wei ^a   Lai, Diwen ^a   Wang, Qingya ^a   Shen, Wenbiao ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84901809875     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.237925     Document Type: Article

References (74)

1. +-sensing ion channel. FEBS Lett 486: 93-98
2. Akita S, Moss DN (1973) The effect of an oxygen-free atmosphere on net photosynthesis and transpiration of barley (Hordeum vulgare L.) and wheat (Triticum aestivum L.) leaves. Plant Physiol 52: 601-603
3. An Z, Jing W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59: 815-825
4. Aubert Y, Vile D, Pervent M, Aldon D, Ranty B, Simonneau T, Vavasseur A, Galaud JP (2010) RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol 51: 1975-1987
5. Becker D, Hoth S, Ache P, Wenkel S, Roelfsema MR, Meyerhoff O, Hartung W, Hedrich R (2003) Regulation of the ABA-sensitive Arabidopsis potassium channel gene GORK in response to water stress. FEBS Lett 554: 119-126
6. 2+ signaling. Mol Plant 1: 218-228
7. 2 synthesis. Plant J 45: 113-122
8. Cavazza C, Martin L, Mondy S, Gaillard J, Ratet P, Fontecilla-Camps JC (2008) The possible role of an [FeFe]-hydrogenase-like protein in the plant responses to changing atmospheric oxygen levels. J Inorg Biochem 102: 1359-1365
9. Chaerle L, Saibo N, Van Der Straeten D (2005) Tuning the pores: towards engineering plants for improved water use efficiency. Trends Biotechnol 23: 308-315
10. Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis. Plant Physiol 154: 810-819
11. Cui W, Gao C, Fang P, Lin G, Shen W (2013) Alleviation of cadmium toxicity in Medicago sativa by hydrogen-rich water. J Hazard Mater 260: 715-724
12. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61: 651-679
13. 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
14. Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47: 907-916
15. Desmard M, Foresti R, Morin D, Dagouassat M, Berdeaux A, Denamur E, Crook SH, Mann BE, Scapens D, Montravers P, et al (2012) Differential antibacterial activity against Pseudomonas aeruginosa by carbon monoxide-releasing molecules. Antioxid Redox Signal 16: 153-163
16. Dordas C, Rivoal J, Hill RD (2003) Plant haemoglobins, nitric oxide and hypoxic stress. Ann Bot (Lond) 91: 173-178
17. Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6: 559-569
18. + channels in plants. Trends Plant Sci 14: 383-390
19. Ederli L, Morettini R, Borgogni A, Wasternack C, Miersch O, Reale L, Ferranti F, Tosti N, Pasqualini S (2006) Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiol 142: 595-608
20. 2 production via Chlamydomonas reinhardtii. Trends Biotechnol 29: 595-600
21. Forestier M, King P, Zhang L, Posewitz M, Schwarzer S, Happe T, Ghirardi ML, Seibert M (2003) Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur J Biochem 270: 2750-2758
22. García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188: 977-984
23. 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
24. Hao LH, Wang WX, Chen C, Wang YF, Liu T, Li X, Shang ZL (2012) Extracellular ATP promotes stomatal opening of Arabidopsis thaliana through heterotrimeric G protein a subunit and reactive oxygen species. Mol Plant 5: 852-864
25. Haworth M, Elliott-Kingston C, McElwain JC (2011) Stomatal control as a driver of plant evolution. J Exp Bot 62: 2419-2423
26. He JM, Ma XG, Zhang Y, Sun TF, Xu FF, Chen YP, Liu X, Yue M (2013) Role and interrelationship of Ga protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves. Plant Physiol 161: 1570-1583
27. + channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci USA 100: 5549-5554
28. Hu H, Li P, Wang Y, Gu R (2014) Hydrogen-rich water delays postharvest ripening and senescence of kiwifruit. Food Chem 156: 100-109
29. Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218: 938-946
30. Ito M, Hirayama M, Yamai K, Goto S, Ito M, Ichihara M, Ohno K (2012) Drinking hydrogen water and intermittent hydrogen gas exposure, but not lactulose or continuous hydrogen gas exposure, prevent 6-hydroxydopamineinduced Parkinson's disease in rats. Med Gas Res 2: 15
31. Itoh T, Fujita Y, Ito M, Masuda A, Ohno K, Ichihara M, Kojima T, Nozawa Y, Ito M (2009) Molecular hydrogen suppresses FcepsilonRImediated signal transduction and prevents degranulation of mast cells. Biochem Biophys Res Commun 389: 651-656
32. + loss via a GORK channel. J Exp Bot 64: 2255-2268
33. Jin Q, Zhu K, Cui W, Xie Y, Han B, Shen W (2013) Hydrogen gas acts as a novel bioactive molecule in enhancing plant tolerance to paraquatinduced oxidative stress via the modulation of heme oxygenase-1 signalling system. Plant Cell Environ 36: 956-969
34. Kanamaru K, Wang R, Su W, Crawford NM (1999) Ser-534 in the hinge 1 region of Arabidopsis nitrate reductase is conditionally required for binding of 14-3-3 proteins and in vitro inhibition. J Biol Chem 274: 4160-4165
35. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22: 2623-2633
36. Lambeck I, Chi JC, Krizowski S, Mueller S, Mehlmer N, Teige M, Fischer K, Schwarz G (2010) Kinetic analysis of 14-3-3-inhibited Arabidopsis thaliana nitrate reductase. Biochemistry 49: 8177-8186
37. Liesche J, Schulz A (2012) In vivo quantification of cell coupling in plants with different phloem-loading strategies. Plant Physiol 159: 355-365
38. Lin Y, Zhang W, Qi F, Cui W, Xie Y, Shen W (2014) Hydrogen-rich water regulates cucumber adventitious root development in a heme oxygenase-1/ carbon monoxide-dependent manner. J Plant Physiol 171: 1-8
39. Loutfy N, El-Tayeb MA, Hassanen AM, Moustafa MF, Sakuma Y, Inouhe M (2012) Changes in the water status and osmotic solute contents in response to drought and salicylic acid treatments in four different cultivars of wheat (Triticum aestivum). J Plant Res 125: 173-184
40. 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
41. Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17: 9-15
42. Mazars C, Thuleau P, Lamotte O, Bourque S (2010) Cross-talk between ROS and calcium in regulation of nuclear activities. Mol Plant 3: 706-718
43. Meyer J (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64: 1063-1084
44. Mondy S, Lenglet A, Cosson V, Pelletier S, Pateyron S, Gilard F, Scholte M, Brocard L, Couzigou JM, Tcherkez G, et al (2014) GOLLUM [FeFe]-hydrogenase-like proteins are essential for plant development in normoxic conditions and modulate energy metabolism. Plant Cell Environ 37: 54-69
45. Morimoto K, Kimura T, Sakka K, Ohmiya K (2005) Overexpression of a hydrogenase gene in Clostridium paraputrificum to enhance hydrogen gas production. FEMS Microbiol Lett 246: 229-234
46. Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59: 165-176
47. Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5: 388-395
48. Oharazawa H, Igarashi T, Yokota T, Fujii H, Suzuki H, Machide M, Takahashi H, Ohta S, Ohsawa I (2010) Protection of the retina by rapid diffusion of hydrogen: administration of hydrogen-loaded eye drops in retinal ischemia-reperfusion injury. Invest Ophthalmol Vis Sci 51: 487-492
49. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, Katsura K, Katayama Y, Asoh S, Ohta S (2007) Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med 13: 688-694
50. Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581: 2325-2336
51. Pape M, Lambertz C, Happe T, Hemschemeier A (2012) Differential expression of the Chlamydomonas [FeFe]-hydrogenase-encoding HYDA1 gene is regulated by the copper response regulator1. Plant Physiol 159: 1700-1712
52. Renwick GM, Giumarro C, Siegel SM (1964) Hydrogen metabolism in higher plants. Plant Physiol 39: 303-306
53. 2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol 151: 1197-1206
54. Sun AZ, Nie SJ, Xing D (2012) Nitric oxide-mediated maintenance of redox homeostasis contributes to NPR1-dependent plant innate immunity triggered by lipopolysaccharides. Plant Physiol 160: 1081-1096
55. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14: 691-699
56. Torres V, Ballesteros A, Fernández VM, Núñez M (1984) Expression of hydrogenase activity in cereals. Ann N Y Acad Sci 434: 296-298
57. Tossi V, Cassia R, Bruzzone S, Zocchi E, Lamattina L (2012) ABA says NO to UV-B: a universal response? Trends Plant Sci 17: 510-517
58. Tossi V, Lamattina L, Cassia R (2009) An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytol 181: 871-879
59. + currents. New Phytol 198: 1039-1048
60. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51: 1821-1839
61. Van Ree K, Gehl B, Chehab EW, Tsai YC, Braam J (2011) Nitric oxide accumulation in Arabidopsis is independent of NOA1 in the presence of sucrose. Plant J 68: 225-233
62. Wang P, Du Y, Li Y, Ren D, Song CP (2010) Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22: 2981-2998
63. Wang WH, Yi XQ, Han AD, Liu TW, Chen J, Wu FH, Dong XJ, He JX, Pei ZM, Zheng HL (2012) Calcium-sensing receptor regulates stomatal closure through hydrogen peroxide and nitric oxide in response to extracellular calcium in Arabidopsis. J Exp Bot 63: 177-190
64. Wilkins KA, Bancroft J, Bosch M, Ings J, Smirnoff N, Franklin-Tong VE (2011) Reactive oxygen species and nitric oxide mediate actin reorganization and programmed cell death in the self-incompatibility response of Papaver. Plant Physiol 156: 404-416
65. 2 enhances Arabidopsis salt tolerance by manipulating ZAT10/12-mediated antioxidant defence and controlling sodium exclusion. PLoS ONE 7: e49800
66. Xie Y, Mao Y, Lai D, Zhang W, Zheng T, Shen W (2013) Roles of NIA/NR/ NOA1-dependent nitric oxide production and HY1 expression in the modulation of Arabidopsis salt tolerance. J Exp Bot 64: 3045-3060
67. Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Gu Q, Xu DK, Yang Q, Shen WB (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66: 280-292
68. Xu S, Zhu S, Jiang Y, Wang N, Wang R, Shen W, Yang J (2013) Hydrogenrich water alleviates salt stress in rice during seed germination. Plant Soil 370: 47-57
69. Xuan Y, Zhou S, Wang L, Cheng Y, Zhao L (2010) Nitric oxide functions as a signal and acts upstream of AtCaM3 in thermotolerance in Arabidopsis seedlings. Plant Physiol 153: 1895-1906
70. Yan J, Tsuichihara N, Etoh T, Iwai S (2007) Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening. Plant Cell Environ 30: 1320-1325
71. Zeng J, Zhang M, Sun X (2013) Molecular hydrogen is involved in phytohormone signaling and stress responses in plants. PLoS ONE 8: e71038
72. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase Da1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21: 2357-2377
73. Zhao MG, Chen L, Zhang LL, Zhang WH (2009) Nitric reductasedependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151: 755-767
74. Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144: 206-217