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Plant function and evolutionary biology
RESEARCH ARTICLE

Ethylene inhibits darkness-induced stomatal closure by scavenging nitric oxide in guard cells of Vicia faba

Xi-Gui Song A B , Xiao-Ping She A C , Juan Wang A and Yi-Chao Sun A
+ Author Affiliations
- Author Affiliations

A School of Life Sciences, Shaanxi Normal University, Xi’an 710062, People’s Republic of China.

B The High School Affiliated to Shaanxi Normal University, Xi’an 710061, People’s Republic of China.

C Corresponding author. Email: shexiaoping530@163.com

Functional Plant Biology 38(10) 767-777 https://doi.org/10.1071/FP11055
Submitted: 24 February 2011  Accepted: 2 July 2011   Published: 16 September 2011

Abstract

The plant hormone ethylene regulates many aspects of plant growth and development. Despite the well-known relationship between ethylene and stress signalling, the involvement of ethylene in regulating stomatal movement is not completely explored. Here, the role and association between nitric oxide (NO) reduction and the inhibition of darkness-induced stomatal closure by ethylene was studied. Physiological data are provided that both ethylene-releasing compound 2-chloroethylene phosphonic acid (ethephon, ETH) and 1-aminocyclopropane-1-carboxylic acid (ACC), the immediate precursor of ethylene, reduced the levels of NO in Vicia faba L. guard cells, and then induced stomatal opening in darkness. In addition, ACC and ETH not only reduced NO levels in guard cells caused by exogenous NO (derived from sodium nitroprusside, SNP) in light, but also abolished NO that had been generated during a dark period and promoted stomatal opening. Interestingly, 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO) and hemoglobin (Hb), NO scavenger and the potent scavenger of NO/carbon monoxide (CO), respectively, also reduced NO levels by SNP and darkness. However, the above-mentioned effects of ACC and ETH were dissimilar to that of nitric oxide synthase (enzyme commission 1.14.13.39) inhibitor NG-nitro-L-Arg-methyl ester (L-NAME), which could neither reduce NO levels by SNP nor abolish NO that had been generated in the dark. Thus, it is concluded that ethylene reduces the levels of NO in V. faba guard cells via a pattern of NO scavenging, then induces stomatal opening in the dark.

Additional keywords: dark, guard cell, NO.


References

Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Molecular Biology 69, 451–462.
Hormone interactions in stomatal function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVOisL8%3D&md5=20339fe82bf23c7a53e15711f917a429CAS |

Adams DO, Yang SF (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proceedings of the National Academy of Sciences of the United States of America 76, 170–174.
Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhtFyisLo%3D&md5=5d904885bb59e15a32214e6df876ea8bCAS |

Alonso JM, Stepanova AN (2004) The ethylene signalling pathway. Science 306, 1513–1515.
The ethylene signalling pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVeqtrzI&md5=2357d66f334651aa0eebacb4a97f32a9CAS |

Benlloch-González M, Romera J, Cristescu S, Harren F, Fournier JM, Benlloch M (2010) K+ starvation inhibits water-stressinduced stomatal closure via ethylene synthesis in sunflower plants. Journal of Experimental Botany 61, 1139–1145.
K+ starvation inhibits water-stressinduced stomatal closure via ethylene synthesis in sunflower plants.Crossref | GoogleScholarGoogle Scholar |

Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annual Review of Cell and Developmental Biology 16, 1–18.
Ethylene: a gaseous signal molecule in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpvFOj&md5=2d820abafd58bb990b21a29b7fc16b82CAS |

Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241, 1086–1089.
Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXls1OnsLk%3D&md5=3f4f83c0038bee86101ec6724c1629d5CAS |

Bolwell GP (1999) Role of active oxygen species and NO in plant defence responses. Current Opinion in Plant Biology 2, 287–294.
Role of active oxygen species and NO in plant defence responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Oqu74%3D&md5=65d9453ec685586080f4dd623319545aCAS |

Chen YF, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Annals of Botany 95, 901–915.
Ethylene signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVWqtL8%3D&md5=910912536e3875432becce79db168b49CAS |

Cousson A, Cotelle V, Vavasseur A (1995) Induction of stomatal closure by vanadate or a light/dark transition involves Ca2+-calmodulin-dependent protein phosphorylations. Plant Physiology 109, 491–497.

Desikan R, Griffiths R, Hancock JT, Neill SJ (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. Proceedings of the National Academy of Sciences of the United States of America 99, 16314–16318.
A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1ent7w%3D&md5=053448d820cd23f5d5502cd9939166aaCAS |

Desikan R, Cheung MK, Clarke A, Golding S, Sagi M, Fluhr R, Rock C, Hancock JT, Neill SJ (2004) Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum. Functional Plant Biology 31, 913–920.
Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsleltbs%3D&md5=bf78ffddeef406cd0e0c8a395f9f4619CAS |

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. The Plant Journal 47, 907–916.
Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVylsL%2FP&md5=e446d7784fa0d158d6eddf075d0c345bCAS |

Fan LM, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signalling model. Current Opinion in Plant Biology 7, 537–546.
Guard cells: a dynamic signalling model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntV2msLo%3D&md5=af527e016283f526013fdbf7388613f5CAS |

Foissner I, Wendehenne D, Langebartels C, Durner J (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. The Plant Journal 23, 817–824.
In vivo imaging of an elicitor-induced nitric oxide burst in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnslWgt7k%3D&md5=12a3dcbb554c71251f1078b8dfb5affaCAS |

Frommhold I (1982) Effect of ethephon on stomatal opening in detached epidermal strips of tobacco leaves (Nicotiana tabacum L. cv. Samsun). Biologia Plantarum 24, 303–306.
Effect of ethephon on stomatal opening in detached epidermal strips of tobacco leaves (Nicotiana tabacum L. cv. Samsun).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xlslyqurc%3D&md5=8f9d210fcedae664ce8a49946c4a74d5CAS |

Garcia-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology 126, 1196–1204.
Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mvgs1GksA%3D%3D&md5=40e0d71881827c8681ab15863387a530CAS |

Garcia-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiology 128, 790–792.
Nitric oxide and abscisic acid cross talk in guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Gqtr4%3D&md5=0d3b080c2ef824410985a753849fa9b5CAS |

Garcia-Mata C, Lamattina L (2007) Abscisic acid (ABA) inhibits light-induced stomatal opening through calcium- and nitric oxide-mediated signaling pathways. Nitric Oxide 17, 143–151.
Abscisic acid (ABA) inhibits light-induced stomatal opening through calcium- and nitric oxide-mediated signaling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFemt7jE&md5=de9ae57d8c4ec6e37ad0b6f5f85a4b22CAS |

Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl– channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proceedings of the National Academy of Sciences of the United States of America 100, 11116–11121.
Nitric oxide regulates K+ and Cl channels in guard cells through a subset of abscisic acid-evoked signaling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnslymsro%3D&md5=f1c497602f5afc3d33f971cd3b32cbcbCAS |

Giulivo C (1986) Hormonal control of water transport in soil–plant–atmosphere continuum. Acta Horticulturae 179, 385–393.

Grefen C, Harter K (2004) Plant two-component systems: principles, functions, complexity and cross-talk. Planta 219, 733–742.
Plant two-component systems: principles, functions, complexity and cross-talk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnt1Gksr0%3D&md5=58c6b49929d26d9ceb3e13417eb18772CAS |

Gunderson CA, Taylor GE (1991) Ethylene directly inhibits foliar gas exchange in Glycine max. Plant Physiology 95, 337–339.
Ethylene directly inhibits foliar gas exchange in Glycine max.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXnvVymtA%3D%3D&md5=e874144474f63b5d2cb7ceb7ca4377ceCAS |

Guo H, Ecker JR (2004) The ethylene signalling pathway: new insights. Current Opinion in Plant Biology 7, 40–49.
The ethylene signalling pathway: new insights.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFWqtg%3D%3D&md5=695b9893331898db04f58906394bc490CAS |

Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, Yoo SD, Hwang I, Zhu T, Schäfer E, Kudla J, Harter K (2004) The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO Journal 23, 3290–3302.
The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmslWht7c%3D&md5=e6eb401b33b47c69665d16b7a288c8feCAS |

He JM, Xu H, She XP, Song XG, Zhao WM (2005) The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean. Functional Plant Biology 32, 237–247.
The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFWjt74%3D&md5=5b209944cd6ae9660e01367112ca97eeCAS |

He JM, Yue XZ, Wang RB, Zhang Y (2011) Ethylene mediates UV-B-induced stomatal closure via peroxidase-dependent hydrogen peroxide synthesis in Vicia faba L. Journal of Experimental Botany 62, 2657–2666.
Ethylene mediates UV-B-induced stomatal closure via peroxidase-dependent hydrogen peroxide synthesis in Vicia faba L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVyksL8%3D&md5=46f241877461e08c1be4e10c0a1a9416CAS |

Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424, 901–908.
The role of stomata in sensing and driving environmental change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsV2isLw%3D&md5=279221af22fe8663599fd2f5149b4f5cCAS |

Hwang I, Chen HC, Sheen J (2002) Two-component signal transduction pathways in Arabidopsis. Plant Physiology 129, 500–515.
Two-component signal transduction pathways in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvV2jsb0%3D&md5=a080b419cb55baeb6136152842919d13CAS |

Johnson PR, Ecker JR (1998) The ethylene gas signal transduction pathway: a molecular perspective. Annual Review of Genetics 32, 227–254.
The ethylene gas signal transduction pathway: a molecular perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvFWlsw%3D%3D&md5=4d2c30951e1d61beaa9d538e7a6d6712CAS |

Jones ML, Woodson WR (1999) Differential expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in Carnation. Plant Physiology 119, 755–764.
Differential expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in Carnation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFSksLo%3D&md5=750aa22fd3a623dc40ee697115c9c4c8CAS |

Kende H (1993) Ethylene biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 44, 283–307.
Ethylene biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsFKisbo%3D&md5=7884f068bb94a741a77c74abef1f2127CAS |

Kendrick MD, Chang C (2008) Ethylene signaling: new levels of complexity and regulation. Current Opinion in Plant Biology 11, 479–485.
Ethylene signaling: new levels of complexity and regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFCgu7fL&md5=6490e9f594ba017f51531796d2a3f7fcCAS |

Kieber JJ (1997) The ethylene response pathway in Arabidopsis. Annual Review of Plant Physiology and Plant Molecular Biology 48, 277–296.
The ethylene response pathway in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1ent7s%3D&md5=fe5a6c3c26e063c05c4a82c616028c04CAS |

Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T (1998) Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Analytical Chemistry 70, 2446–2453.
Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsVWqtb4%3D&md5=90dc3fc1d055a9913b3ecd000c977514CAS |

Lamar CA, Mahesh VB, Brann DW (1996) Regulation of gonadotrophin-releasing hormone (GnRH) secretion by heme molecules: a regulatory role for carbon monoxide? Endocrinology 137, 790–793.
Regulation of gonadotrophin-releasing hormone (GnRH) secretion by heme molecules: a regulatory role for carbon monoxide?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XntVCmtw%3D%3D&md5=6dd7c783ab16086c51aa7eee166b3963CAS |

Leshem YY, Pinchasov Y (2000) Non-invasion photoacustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria anannasa (Duch) and avocados Persea americana (Mill.). Journal of Experimental Botany 51, 1471–1473.
Non-invasion photoacustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria anannasa (Duch) and avocados Persea americana (Mill.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtVWns7g%3D&md5=67576bcd971aad26612242545b11c748CAS |

Levitt LK, Stein DB, Rubinstein B (1987) Promotion of stomatal opening by indoleacetic acid and ethrel in epidermal strips of Vicia faba L. Plant Physiology 85, 318–321.
Promotion of stomatal opening by indoleacetic acid and ethrel in epidermal strips of Vicia faba L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXjs1Sr&md5=3959453e46328374463d5367f3790618CAS |

Li J, Qiu LY, Zhao FG, Hou LX, Liu X (2007) The role of nitric oxide in ethylene-induced stomatal closure in Vica faba L. Journal of Plant Physiology and Molecular Biology 33, 349–353.

Liu X, Zhang SQ, Lou CH (2003) Involvement of nitric oxide in the signal transduction of salicylic acid regulating stomatal movement. Chinese Science Bulletin 48, 449–452.

Madhavan S, Chrominiski A, Smith BN (1983) Effect of ethylene on stomatal opening in tomato and carnation leaves. Plant & Cell Physiology 24, 569–572.

Magalhaes JR, Monte DC, Durzan D (2000) Nitric oxide and ethylene emission in Arabidopsis thaliana. Physiology and Molecular Biology of Plants 6, 117–127.

Mansfield TA, Hetherington AM, Atkinson CJ (1990) Some aspects of stomatal physiology. Annual Review of Plant Physiology and Plant Molecular Biology 41, 55–75.
Some aspects of stomatal physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXksFGkuro%3D&md5=ee2718eaa325937aae1a2d5cd963b954CAS |

Merritt F, Kemper A, Tallman G (2001) Inhibitors of ethylene biosynthesis inhibit auxin-induced stomatal opening in epidermis detached from leaves of Vicia faba L. Plant & Cell Physiology 42, 223–230.
Inhibitors of ethylene biosynthesis inhibit auxin-induced stomatal opening in epidermis detached from leaves of Vicia faba L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFynu7k%3D&md5=61f7ed34363ef53c8ae40f4cdc3c55ecCAS |

Mills G, Hayes F, Wilkinson S, Davies WJ (2009) Chronic exposure to increasing background ozone impairs stomatal functioning in grassland species. Global Change Biology 15, 1522–1533.
Chronic exposure to increasing background ozone impairs stomatal functioning in grassland species.Crossref | GoogleScholarGoogle Scholar |

Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signalling in stomatal guard cells. Plant Physiology 128, 13–16.
Nitric oxide is a novel component of abscisic acid signalling in stomatal guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVSluw%3D%3D&md5=a8e4376aa536c689f4d940d7ef717961CAS |

Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytologist 159, 11–35.
Nitric oxide signalling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlslaltrs%3D&md5=d584f92974acfd007daf1891260b2ab4CAS |

Ouaked F, Rozhon W, Lecourieux D, Hirt H (2003) A MAPK pathway mediates ethylene signaling in plants. EMBO Journal 22, 1282–1288.
A MAPK pathway mediates ethylene signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1yrsbw%3D&md5=ffab67ba5fa2d5927c59546d63f70dfbCAS |

Pallas JE, Kays SJ (1982) Inhibition of photosynthesis by ethylene – a stomatal effect. Plant Physiology 70, 598–601.
Inhibition of photosynthesis by ethylene – a stomatal effect.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XlsF2ksLs%3D&md5=a4458b96b8671248a14128e394f77f67CAS |

Pedroso MC, Magalhaes JR, Durzan D (2000) A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm callus cells and foliar tissues. Journal of Experimental Botany 51, 1027–1036.
A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm callus cells and foliar tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktVClu7k%3D&md5=2ebb54a583c487dad2ab04b8ce9f8563CAS |

Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker JR (1995) Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139, 1393–1409.

Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 52, 627–658.
Guard cell signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWgsbc%3D&md5=34041c4bcd325ee02dcf438a82fed47fCAS |

She XP, Huang AX (2004) Change of nitric oxide and NADPH-diaphorase during the generation and the development of adventitious roots in mung bean hypocotyls cuttings. Acta Botanica Sinica 46, 1049–1055.

She XP, Song XG (2006) Cytokinin- and auxin-induced stomatal opening is related to the change of nitric oxide levels in guard cells in broad bean. Physiologia Plantarum 128, 569–579.

She XP, Song XG (2008) Pharmacological evidence indicates that MAPKK/CDPK modulate NO levels in darkness-induced stomatal closure of broad bean. Australian Journal of Botany 56, 347–357.
Pharmacological evidence indicates that MAPKK/CDPK modulate NO levels in darkness-induced stomatal closure of broad bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFylsbo%3D&md5=ae971842688dddc13a4ee57b429fb019CAS |

She XP, Song XG, He JM (2004) Role and relationship of nitric oxide and hydrogen peroxide in light/dark-regulated stomatal movement in Vicia faba. Acta Botanica Sinica 46, 1292–1300.

Song XG, She XP, Zhang B (2008) Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis. Physiologia Plantarum 132, 514–525.
Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWktbg%3D&md5=1a4b9d466cda64a4845587e8027c5d11CAS |

Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiology 138, 2337–2343.
Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXps12ltr0%3D&md5=1cae121eb88d8f15b1e45c4c7233b7ceCAS |

Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2006) Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis. Journal of Experimental Botany 57, 2259–2266.
Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvF2mu70%3D&md5=54cffbf01030e01012e83853837a1b1dCAS |

Tissera P, Ayres PG (1986) Endogenous ethylene affects the behavior of stomata in epidermis isolated from rust infected faba bean (Vicia faba L.). New Phytologist 104, 53–61.
Endogenous ethylene affects the behavior of stomata in epidermis isolated from rust infected faba bean (Vicia faba L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XlvVOrsL8%3D&md5=dfd0070aad57d3ff56c7a5abf2c64e15CAS |

Wang KLC, Yoshida H, Lurin C, Ecker JR (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428, 945–950.
Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsV2mtro%3D&md5=0ddcb830b8a02cbcda3a98a79a3dfe80CAS |

Wang YB, Feng HY, Qu Y, Cheng JQ, Zhao ZG, Zhang MX, Wang XL, An LZ (2006) The relationship between reactive oxygen species and nitric oxide in ultraviolet-B-induced ethylene production in leaves of maize seedlings. Environmental and Experimental Botany 57, 51–61.
The relationship between reactive oxygen species and nitric oxide in ultraviolet-B-induced ethylene production in leaves of maize seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslSks7o%3D&md5=0323bfdc9a4dbf6f183d948952b0ae43CAS |

Wilkinson S, Davies WJ (2009) Ozone suppresses soil drying- and abscisic acid (ABA)-induced stomatal closure via an ethylenedependent mechanism. Plant, Cell & Environment 32, 949–959.
Ozone suppresses soil drying- and abscisic acid (ABA)-induced stomatal closure via an ethylenedependent mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtValtbnL&md5=b754d6b1ed10000de069603a1061082bCAS |

Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant, Cell & Environment 33, 510–525.
Drought, ozone, ABA and ethylene: new insights from cell to plant to community.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltV2hurs%3D&md5=7ff6bcfef3fea72c38cb0ad40ab89c05CAS |

Wills RBH, Ku VVV, Leshem YY (2000) Fumigation with nitric oxide to extend the postharvest life of strawberries. Postharvest Biology and Technology 18, 75–79.
Fumigation with nitric oxide to extend the postharvest life of strawberries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnsVKnsL8%3D&md5=cc95b0fce7ed735177e6558c5994ea14CAS |

Young TE, Meeley RB, Gallie DR (2004) ACC synthase expression regulates leaf performance and drought tolerance in maize. The Plant Journal 40, 813–825.
ACC synthase expression regulates leaf performance and drought tolerance in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFWgtQ%3D%3D&md5=0a5bf8738f3e3734ce23ed59340a7cc3CAS |

Zeiger E (1983) The biology of stomatal guard cells. Annual Review of Plant Physiology 34, 441–474.
The biology of stomatal guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmsVyqtw%3D%3D&md5=b417a8a8b148d8a5e51885ba21fbc211CAS |

Zhu SH, Liu MC, Zhou J (2006) Inhibition by nitric oxide of ethylene biosynthesis and lipoxygenase activity in peach fruit during storage. Postharvest Biology and Technology 42, 41–48.
Inhibition by nitric oxide of ethylene biosynthesis and lipoxygenase activity in peach fruit during storage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCrtLnN&md5=cb0008c767bdb363074acc2c8756035cCAS |