Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Cytosolic alkalisation and nitric oxide production in UVB-induced stomatal closure in Arabidopsis thaliana

Xiao-Min Ge A , Yan Zhu A and Jun-Min He A B

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

B Corresponding author. Email: hejm@snnu.edu.cn

Functional Plant Biology 41(8) 803-811 http://dx.doi.org/10.1071/FP13222
Submitted: 29 July 2013  Accepted: 27 March 2014   Published: 28 April 2014

Abstract

The role and the interrelationship of cytosolic alkalisation and nitric oxide (NO) in UVB-induced stomatal closure were investigated in Arabidopsis thaliana (L.) Heynh. by stomatal bioassay and laser-scanning confocal microscopy. In response to 0.5 W m–2 UVB radiation, the rise of NO levels in guard cells occurred after cytosolic alkalisation but preceded stomatal closure. UVB-induced NO production and stomatal closure were both inhibited by NO scavengers, nitrate reductase (NR) inhibitors and a Nia25/Nia12 mutation, and also by butyrate. Methylamine induced NO generation and stomatal closure in the wild-type but not in the Nia25/Nia12 mutant or wild-type plants pretreated with NO scavengers or NR inhibitors while enhancing the cytosolic pH in guard cells under light. NO generation in wild-type guard cells was largely induced after 60 min of UVB radiation. The defect in UVB-induced NO generation in Nia25/Nia12 guard cells did not affect the changes of guard cell pH before 60 min of UVB radiation, but prevented the UVB-induced cytosolic alkalisation after 60 min of radiation. Meanwhile, exogenous NO caused a marked rise of cytosolic pH in guard cells. Together, our results show that cytosolic alkalisation and NR-dependent NO production coordinately function in UVB signalling in A. thaliana guard cells.

Additional keywords: cytosolic pH, nitric oxide, UVB irradiation.


References

Barkla BJ, Vera-Estrella R, Maldonado-Gama M, Pantoja O (1999) Abscisic acid induction of vacuolar H+-ATPase activity in Mesembryanthemum crystallinum is developmentally regulated. Plant Physiology 120, 811–820.
Abscisic acid induction of vacuolar H+-ATPase activity in Mesembryanthemum crystallinum is developmentally regulated.CrossRef | 1:CAS:528:DyaK1MXks1amtbo%3D&md5=079635a5cefabc48ce44d33818888d1fCAS | 10398716PubMed | open url image1

Blatt MR, Armstrong F (1993) K+ channels of stomatal guard cells: abscisic-acid-evoked control of the outward rectifier mediated by cytoplasmic pH. Planta 191, 330–341.
K+ channels of stomatal guard cells: abscisic-acid-evoked control of the outward rectifier mediated by cytoplasmic pH.CrossRef | 1:CAS:528:DyaK3sXmsVGksr0%3D&md5=f3618881d60778c302d5aafae3053d3bCAS | open url image1

Boonsirichai K, Sedbrook JC, Chen R, Gilroy S, Masson PH (2003) ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. The Plant Cell 15, 2612–2625.
ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes.CrossRef | 1:CAS:528:DC%2BD3sXpt1OrtbY%3D&md5=d235a762805881c9d70770ab4b59501eCAS | 14507996PubMed | open url image1

Brown BA, Jenkins GI (2008) UV-B signaling pathways with different fluence-rate response profiles are distinguished in mature Arabidopsis leaf tissue by requirement for UVR8, HY5, and HYH. Plant Physiology 146, 576–588.
UV-B signaling pathways with different fluence-rate response profiles are distinguished in mature Arabidopsis leaf tissue by requirement for UVR8, HY5, and HYH.CrossRef | 1:CAS:528:DC%2BD1cXjtFCmtL4%3D&md5=75a39b47937cc33ff1d9f1a33e2ca303CAS | 18055587PubMed | open url image1

Caldwell MM (1971) Solar ultraviolet radiation and the growth and development of higher plants. In Photophysiology, Vol. 6’. (Ed. AC Giese) pp. 131–177. (Academic Press: New York)

Davey MP, Susanti NI, Wargent JJ, Findlay JE, Paul Quick W, Paul ND, Jenkins GI (2012) The UV-B photoreceptor UVR8 promotes photosynthetic efficiency in Arabidopsis thaliana exposed to elevated levels of UV-B. Photosynthesis Research 114, 121–131.
The UV-B photoreceptor UVR8 promotes photosynthetic efficiency in Arabidopsis thaliana exposed to elevated levels of UV-B.CrossRef | 1:CAS:528:DC%2BC38Xhslansb3F&md5=dfb801c5db86d605bd4f290798fd1a91CAS | 23161229PubMed | open url image1

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 | 1:CAS:528:DC%2BD28XhtVylsL%2FP&md5=454340846f0c8560718bd74476b5555aCAS | 16961732PubMed | open url image1

Eisinger WR, Bogomolni RA, Taiz L (2003) Interactions between a blue-green reversible photoreceptor and a separate UV-B receptor in stomatal guard cells. American Journal of Botany 90, 1560–1566.
Interactions between a blue-green reversible photoreceptor and a separate UV-B receptor in stomatal guard cells.CrossRef | 1:CAS:528:DC%2BD3sXpvFykt70%3D&md5=2fc7404c8ed3da3a413179e14c30dacaCAS | 21653331PubMed | open url image1

Fasano JM, Swanson SJ, Blancaflor EB, Dowd PE, Kao T-H, Gilroy S (2001) Changes in root cap pH are required for the gravity response of the Arabidopsis root. The Plant Cell 13, 907–921.

Felle HH (2005) pH regulation in anoxic plants. Annals of Botany 96, 519–532.
pH regulation in anoxic plants.CrossRef | 1:CAS:528:DC%2BD2MXhtFGitLnK&md5=2ab7e006f10921619ca75715ae3a7e05CAS | 16024558PubMed | open url image1

Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants: balancing damage and protection. Plant Physiology 133, 1420–1428.
Ultraviolet-B radiation-mediated responses in plants: balancing damage and protection.CrossRef | 1:CAS:528:DC%2BD2cXhvFWg&md5=143ecf631aaa9792e0767942b638f54aCAS | 14681524PubMed | open url image1

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 & Environment 31, 1717–1724.
Nitric oxide production occurs after cytosolic alkalinization during stomatal closure induced by abscisic acid.CrossRef | 1:CAS:528:DC%2BD1cXhtl2hs7zN&md5=6ddcddbeacea248aca5cf58c1ae7cd89CAS | open url image1

Gonugunta VK, Srivastava N, Raghavendra AS (2009) Cytosolic alkalinization is a common and early messenger preceding the production of ROS and NO during stomatal closure by variable signals, including abscisic acid, methyl jasmonate and chitosan. Plant Signaling & Behavior 4, 561–564.
Cytosolic alkalinization is a common and early messenger preceding the production of ROS and NO during stomatal closure by variable signals, including abscisic acid, methyl jasmonate and chitosan.CrossRef | 1:CAS:528:DC%2BC3cXpvFelurk%3D&md5=2c97bf3cb4d1e95daf7c05bd92097754CAS | open url image1

Grabov A, Blatt MR (1997) Parallel control of the inward-rectifier K+ channel by cytosolic free Ca2+ and pH in Vicia guard cells. Planta 201, 84–95.
Parallel control of the inward-rectifier K+ channel by cytosolic free Ca2+ and pH in Vicia guard cells.CrossRef | 1:CAS:528:DyaK2sXisFyrsw%3D%3D&md5=53390c9ccdd52a15edf35e5042a92d93CAS | open url image1

Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100–103.
Identification of a plant nitric oxide synthase gene involved in hormonal signaling.CrossRef | 1:CAS:528:DC%2BD3sXnslSjs7o%3D&md5=4b228fca88024852730ab368e94ea391CAS | 14526079PubMed | open url image1

He J-M, Xu H, She X-P, Song X-G, Zhao W-M (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 | 1:CAS:528:DC%2BD2MXivFWjt74%3D&md5=0c32fc3ce0425b4fb95e33ea049975b2CAS | open url image1

He J-M, Zhang Z, Wang R-B, Chen Y-P (2011) UV-B-induced stomatal closure occurs via ethylene-dependent NO generation in Vicia faba. Functional Plant Biology 38, 293–302.
UV-B-induced stomatal closure occurs via ethylene-dependent NO generation in Vicia faba.CrossRef | 1:CAS:528:DC%2BC3MXktl2isrg%3D&md5=e39f4ea759899996f4cc0ac0f7aaa9a9CAS | open url image1

He J-M, Ma X-G, Zhang Y, Sun T-F, Xu F-F, Chen Y-P, Liu X, Yue M (2013) Role and interrelationship of Gα protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves. Plant Physiology 161, 1570–1583.
Role and interrelationship of Gα protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves.CrossRef | 1:CAS:528:DC%2BC3sXmvFKru7c%3D&md5=7f586cd4734a854004e7dd17422df511CAS | 23341360PubMed | open url image1

Heijde M, Ulm R (2012) UV-B photoreceptor-mediated signalling in plants. Trends in Plant Science 17, 230–237.
UV-B photoreceptor-mediated signalling in plants.CrossRef | 1:CAS:528:DC%2BC38XjtVOqurw%3D&md5=7c771513e73555db159feafde5076a3eCAS | 22326562PubMed | open url image1

Huang A-X, She X-P, Zhang Y-Y, Zhao J-L (2013) Cytosolic acidification precedes nitric oxide removal during inhibition of ABA induced stomatal closure by fusicoccin. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 60, 60–68.
Cytosolic acidification precedes nitric oxide removal during inhibition of ABA induced stomatal closure by fusicoccin.CrossRef | 1:CAS:528:DC%2BC3sXntVKq&md5=7545fc3bacfd954d5bbb618a2c3285a7CAS | open url image1

Irving HR, Gehring CA, Parish RW (1992) Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proceedings of the National Academy of Sciences of the United States of America 89, 1790–1794.
Changes in cytosolic pH and calcium of guard cells precede stomatal movements.CrossRef | 1:CAS:528:DyaK38Xitlaitb0%3D&md5=68922bd7947ea1848d1fef5e1e57b235CAS | 11607281PubMed | open url image1

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 Physiology 51, 1721–1730.
Cytosolic alkalization and cytosolic calcium oscillation in Arabidopsis guard cells response to ABA and MeJA.CrossRef | 1:CAS:528:DC%2BC3cXht1OgsrnF&md5=3cc13977b4931fd1a9bea5d304a01136CAS | open url image1

Jansen MAK, Bornman JF (2012) UV-B radiation: from generic stressor to specific regulator. Physiologia Plantarum 145, 501–504.
UV-B radiation: from generic stressor to specific regulator.CrossRef | 1:CAS:528:DC%2BC38Xht1Olu77M&md5=94bb5e1227bcdeb62bfbb07c25e76c0fCAS | open url image1

Jansen MAK, Noort REVD (2000) Ultraviolet-B radiation induces complex alterations in stomatal behaviour. Physiologia Plantarum 110, 189–194.
Ultraviolet-B radiation induces complex alterations in stomatal behaviour.CrossRef | 1:CAS:528:DC%2BD3cXnt1Cntb4%3D&md5=a5b625ac3abd3b16772b3f88b521a902CAS | open url image1

Li J, Yang L, Jin D, Nezames CD, Terzaghi W, Deng XW (2013) UV-B-induced photomorphogenesis in Arabidopsis. Protein & Cell 4, 485–492.
UV-B-induced photomorphogenesis in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC3sXht1CkurjJ&md5=37b70d2276fc9e52c4b2ff61d789781dCAS | open url image1

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.

Liu J, Liu GH, Hou LX, Liu X (2010) Ethylene-induced nitric oxide production and stomatal closure in Arabidopsis thaliana depending on changes in cytosolic pH. Chinese Science Bulletin 55, 2403–2409.
Ethylene-induced nitric oxide production and stomatal closure in Arabidopsis thaliana depending on changes in cytosolic pH.CrossRef | 1:CAS:528:DC%2BC3cXpvFensLg%3D&md5=2af2eab1881ff679e97e1ea600a45d96CAS | open url image1

Lovy-Wheeler A, Kunkel JG, Allwood EG, Hussey PJ, Hepler PK (2006) Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily. The Plant Cell 18, 2182–2193.
Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily.CrossRef | 1:CAS:528:DC%2BD28XhtVKgurnP&md5=0173478046ca4f0dda65b3a70b3cf8ffCAS | 16920777PubMed | open url image1

Ma YL, She XP, Yang SS (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. Science China Life Sciences 55, 974–983.
Sphingosine-1-phosphate (S1P) mediates darkness-induced stomatal closure through raising cytosol pH and hydrogen peroxide (H2O2) levels in guard cells in Vicia faba.CrossRef | 1:CAS:528:DC%2BC38XhslWru7bM&md5=384ef0656ec2d14c1d3ca61fa3f50073CAS | open url image1

Ma YL, She XP, Yang SS (2013) Cytosolic alkalization-mediated H2O2 and NO production are involved in darkness-induced stomatal closure in Vicia faba. Canadian Journal of Plant Science 93, 119–130.
Cytosolic alkalization-mediated H2O2 and NO production are involved in darkness-induced stomatal closure in Vicia faba.CrossRef | 1:CAS:528:DC%2BC3sXivVSru74%3D&md5=3a373e582c64fa547e8cd2babe99b6e5CAS | open url image1

Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proceedings of the National Academy of Sciences of the United States of America 104, 20 996–21 001.
Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs.CrossRef | 1:CAS:528:DC%2BD1cXksFWmsw%3D%3D&md5=aeb29876f024ea9a36ab67ffabf04278CAS | open url image1

Morales LO, Brosché M, Vainonen J, Jenkins GI, Wargent JJ, Sipari N, Strid A, Lindfors AV, Tegelberg R, Aphalo PJ (2013) Multiple roles for UV RESISTANCE LOCUS 8 in regulating gene expression and metabolite accumulation in Arabidopsis under solar UV radiation. Plant Physiology 161, 744–759.
Multiple roles for UV RESISTANCE LOCUS 8 in regulating gene expression and metabolite accumulation in Arabidopsis under solar UV radiation.CrossRef | 1:CAS:528:DC%2BC3sXmvFKqs70%3D&md5=2069fb8b9d756247e513b8b65e1993e0CAS | 23250626PubMed | open url image1

Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF (2008) AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. Journal of Biological Chemistry 283, 32 957–32 967.
AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase.CrossRef | 1:CAS:528:DC%2BD1cXhtlOjtLbO&md5=eff291f18852add910705746339111cbCAS | open url image1

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. Journal of Experimental Botany 59, 165–176.
Nitric oxide, stomatal closure, and abiotic stress.CrossRef | 1:CAS:528:DC%2BD1cXjsVamt70%3D&md5=53774ba911562bbf2eac3148b106e4caCAS | 18332225PubMed | open url image1

Nogués S, Allen DJ, Morison JIL, Baker NR (1999) Characterization of stomatal closure caused by ultraviolet-B radiation. Plant Physiology 121, 489–496.
Characterization of stomatal closure caused by ultraviolet-B radiation.CrossRef | 10517840PubMed | open url image1

Ramani S, Chelliah J (2007) UV-B-induced signaling events leading to enhanced-production of catharanthine in Catharanthus roseus cell suspension cultures. BMC Plant Biology 7, 61
UV-B-induced signaling events leading to enhanced-production of catharanthine in Catharanthus roseus cell suspension cultures.CrossRef | 17988378PubMed | open url image1

Rizzini L, Favory J-J, Cloix C, Faggionato D, O’Hara A, Kaiserli E, Baumeister R, Schäfer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332, 103–106.
Perception of UV-B by the Arabidopsis UVR8 protein.CrossRef | 1:CAS:528:DC%2BC3MXjvVyisL0%3D&md5=40b777587d2809f04a87b9dd9917d0aaCAS | 21454788PubMed | open url image1

Roos W, Evers S, Hieke M, Tschope M, Schumann B (1998) Shifts of intracellular pH distribution as a part of the signal mechanism leading to the elicitation of benzophenanthridine alkaloids. Plant Physiology 118, 349–364.
Shifts of intracellular pH distribution as a part of the signal mechanism leading to the elicitation of benzophenanthridine alkaloids.CrossRef | 1:CAS:528:DyaK1cXmslyqtro%3D&md5=153bd7e9b2f39aed9543611a1dc5199fCAS | 9765521PubMed | open url image1

Rozema J, Boelen P, Blokker P (2005) Depletion of stratospheric ozone over the Antarctic and Arctic: responses of plants of polar terrestrial ecosystems to enhanced UV-B, an overview. Environmental Pollution 137, 428–442.
Depletion of stratospheric ozone over the Antarctic and Arctic: responses of plants of polar terrestrial ecosystems to enhanced UV-B, an overview.CrossRef | 1:CAS:528:DC%2BD2MXlvFygurw%3D&md5=f349c95324d3c795901ccd1ae52a8bf7CAS | 16005756PubMed | open url image1

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 Physiology 134, 1536–1545.
Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure.CrossRef | 1:CAS:528:DC%2BD2cXjsFKmsLw%3D&md5=23f8e697815fe023a78a456e47d5ec74CAS | 15064385PubMed | open url image1

Swanson SJ, Jones RL (1996) Gibberellic acid induces vacuolar acidification in barley aleurone. The Plant Cell 8, 2211–2221.

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 Phytologist 181, 871–879.
An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation.CrossRef | 1:CAS:528:DC%2BD1MXjsFGiur8%3D&md5=d8ba2a1a3da6c5618d80a42660da905cCAS | 19140950PubMed | open url image1

Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292, 2070–2072.
G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells.CrossRef | 1:CAS:528:DC%2BD3MXksFOlu7k%3D&md5=4a6252652b1082d2ba3f193d0e0b1dd2CAS | 11408655PubMed | open url image1

Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signaling in plants. Plant, Cell & Environment 31, 622–631.
Nitric oxide synthesis and signaling in plants.CrossRef | 1:CAS:528:DC%2BD1cXlvFehur4%3D&md5=c4d379f5d9f3d98f5c41261fee2da1ceCAS | open url image1

Yalamanchili RD, Stratmann JW (2002) Ultraviolet-B activates components of the systemin signaling pathway in Lycopersicon peruvianum suspension-cultured cells. The Journal of Biological Chemistry 277, 28 424–28 430.
Ultraviolet-B activates components of the systemin signaling pathway in Lycopersicon peruvianum suspension-cultured cells.CrossRef | 1:CAS:528:DC%2BD38XmsVGqsbg%3D&md5=ed5a7dee1f82a8db3653ed922947f7a4CAS | open url image1

Zhao S-L, Sun L-R, Zhang H, Lu B-S, Ma L-Y, Hao F-S (2009) Exogenous NO-induced rise in cytosolic pH of Arabidopsis guard cells precedes stomatal closure. Progress in Natural Science 19, 1062–1067.

Zhao S-L, Sun L-R, Zhang H, Ma L-Y, Lu B-S, Hao F-S (2010) Cytoplasmic alkalization mediates exogenous nitric oxide-induced stomatal closure in Vicia faba. Acta Agronomica Sinica 36, 533–538.
Cytoplasmic alkalization mediates exogenous nitric oxide-induced stomatal closure in Vicia faba.CrossRef | 1:CAS:528:DC%2BC3cXotlSgt7k%3D&md5=783d84afd0449ef03091624713291543CAS | open url image1



Export Citation Cited By (1)