Abstract
Nitric oxide (NO) is a ubiquitous signal molecule involved in multiple plant responses to environmental stress. In the recent years, the regulating role of NO on heavy metal toxicity in plants is realized increasingly, but knowledge of NO in alleviating aluminum (Al) toxicity is quite limited. In this article, NO homeostasis between its biosynthesis and elimination in plants is presented. Some genes involved in NO/Al network and their expressions are also introduced. Furthermore, the role of NO in Al toxicity and the functions in Al tolerance are discussed. It is proposed that Al toxicity may disrupt NO homeostasis, leading to endogenous NO concentration being lower than required for root elongation in plants. There are many evidences that pointed out that the exogenous NO treatments improve Al tolerance in plants through activating antioxidative capacity to eliminate reactive oxygen species. Most of the work with respect to NO regulating pathways and functions still has to be done in the future.
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Achary VMM, Jena S, Panda KK, Panda BB (2008) Aluminum induced oxidative stress and DNA damage in root cells of Allium cepa L. Ecotoxicol Environ Safe 70:300–310
Ahad A, Nick P (2006) Actin is bundled in activation-tagged tobacco mutants that tolerate aluminum. Planta. doi:10.1007/s00425-006-0359-0
Baluska F, Volkmann D, Menzel D (2005) Plant synapses: actin-based adhesion domains for cell-to-cell communication. Trends Plant Sci 10:106–111
Beligni MV, Lamattina L (1999) Is nitric oxide toxic or protective? Trends Plant Sci 4:299–300
Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650
Berthke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–341
Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Ann Rev Plant Biol 59:21–39
Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou J, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315
Bogdan C (2001) Nitric oxide and regulation of gene expression. Trends Cell Biol 11:66–75
Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122
Capone R, Tiwari BS, Levine A (2004) Rapid transmission of oxidative and nitrosative stress signals from roots to shoots in Arabidopsis. Plant Physiol Biochem 42:425–428
Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 13:1380–1384
Cooney RV, Harwood PJ, Custer LJ, Franke AA (1994) Light-mediated conversion of nitrogen dioxide to nitric oxide by carotenoids. Environ Heal Perspect 102:460–462
Crawford NM, Galli M, Tischner R, Heimer YM, Okamoto M, Mack A (2006) Response to Zemojtel et al.: plant nitric oxide synthase: back to square one. Trends Plant Sci 11:526–527
De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, di Toppi LS, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228
de Pinto MC, Tomassi F, de Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells. Plant Physiol 130:698–708
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
Diaz M, Achkor H, Titarenko E, Martinez MC (2003) The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Lett 543:136–139
Dordas C, Hasinoff BB, Igamberdiev AU, Manach N, Rivoal J, Hill RD (2003) Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J 35:763–770
Ezaki B, Yamamoto Y, Matsumoto H (1995) Cloning and sequencing of the cDNAs induced by aluminium treatment and Pi starvation in tobacco cultured cells. Physiol Plant 93:11–18
Ezaki B, Koyanagi M, Gardner RC, Matsumoto H (1997) Nucleotide sequence of a cDNA for GDP dissociation inhibitor (GDI) which is induced by aluminum (Al) ion stress in tobacco cell culture (accession no. AF012823) (PGR 97–133). Plant Physiol 115:314–316
Ezaki B, Sivaguru M, Ezaki Y, Matsumoto H, Gardner RC (1999) Acquisition of aluminum tolerance in Saccharomyces cerevisiae by expression of the BCB or NtGDI1 gene derived from plants. FEMS Microbiol Lett 171:81–87
Ezaki B, Katsuhara M, Kawamura M, Matsumoto H (2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiol 127:918–927
Flores-Perez U, Sauret-Gueto S, Gas E, Jarvis P, Rodrıguez-Concepcion M (2008) A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell 20:1303–1315
Gabaldon C, Ros-Gomez LV, Pedreno MA, Ros-Barcelo A (2005) Nitric oxide production by the differentiating xylem of Zinnia elegans. New Phytol 165:121–130
Garcia-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross-talk in guard cells. Plant Physiol 128:790–792
Gas E, Flores-Perez U, Sauret-Gueto S, Rodrıguez-Concepcion M (2009) Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21:18–23
Gow AJ, Luchsinger BP, Pawloski JR, Singel DJ, Stamler JS (1999) The oxyhemoglobin reaction of nitric oxide. Proc Natl Acad Sci USA 96:9027–9032
Guo FG, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103
He HY, He LF, Li XF, Gu MH (2006) Effects of sodium nitroprusside on mitochondrial function of rye and wheat root tip under aluminum stress. J Plant Physiol Mol Biol 32(2):239–244
He HY, He LF, Li XF, Gu MH (2007) Effect of SNP on adsorption of root tip cell wall rye and wheat under aluminum stress. J Guangxi Agric & Biol Sci 26(3):235–239
Hoekenga OA, Maron LG, Pineros MA, Cancado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H, Yamamoto Y, Koyama H, Kochian LV (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:9738–9743
Horemans N, Foyer CH, Potters G, Asard H (2000) Ascorbate function and associated transport systems in plants. Plant Physiol Biochem 38:531–540
Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238
Hu KD, Hu LY, Li YH, Zhang FQ, Zhang H (2007) Protective roles of nitric oxide on germination and antioxidant metabolism in wheat seeds under copper stress. Plant Growth Regul 53:173–183
Huang X, Uv R, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923
Igamberdiev AU, Hill RD (2004) Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot 55:2473–2482
Illéš P, Schlicht M, Pavlovkin J, Lichtscheidl I, Baluška F, Ovecka M (2006) Aluminum toxicity in plants: internalization of aluminum into cells of the transition zone in Arabidopsis root apices relates to changes in plasma membrane potential, endosomal behaviour and nitric oxide production. J Exp Bot 57:4201–4213
Innocenti G, Pucciariello C, Gleuher ML, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602
Ji Y, Toader V, Bennett BM (2002) Regulation of microsomal and cytosolic glutathione S-transferase activities by S-nitrosylation. Biochem Pharmacol 63:1397–1404
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260
Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu Rev Plant Biol 55:459–493
Koh YH, Suzuki K, Che W, Park YS, Miyamoto Y, Higashiyama S, Taniguchi N (2001) Inactivation of glutathione peroxidase by NO leads to the accumulation of H2O2 and the induction of HB-EGF via c-Jun NH2-terminal kinase in rat aortic smooth muscle cells. FASEB J 15:1472–1474
Koshland DE (1992) The molecule of the year. Science 258:1861
Kumar D, Klessing DF (2000) Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene and jasmonic acid. Mol Plant Microbe Interact 13:347–351
Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136
Lamotte O, Courtois C, Barnavon L (2005) Nitric oxide in plants: the biosynthesis and signaling properties of a fascinating molecule. Planta 221:1–4
Lind C, Gerdes R, Hamnell Y, Schuppe-Koistinen I, von LowenhielmHB HA, Cotgreave IA (2002) Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affinity purification and proteomic analysis. Arch Biochem Biophys 406:229–240
Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis thaliana. Plant Physiol 137:921–930
Liu YG, Wu RR, Wan Q, Xie GQ, Bi YR (2007) Glucose-6-phosphatedehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in red kidney bean roots. Plant Cell Physiol 48:511–522
Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–45
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Modolo LV, Augusto O, Almeida IM, Magalhaes JR, Salgado I (2005) Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett 579:3814–3820
Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF (2008) AtNOS/A1 is a functional Arabidopsis thaliana cGTPase and not a nitric oxide synthase. J Biol Chem 283:32957–32967
Navarre DA, Wendehenne D, Durner J, Noad R, Klessig DF (2000) Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol 122:573–582
Neill SJ, Desikan R, Clarke A, Hancock JT (2002a) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16
Neill SJ, Desikan R, Hancock JT (2002b) Hydrogen peroxide signaling. Curr Opin Biotechnol 5:388–395
Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35
Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956
Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the IAA-induced adventitious rooting process. Plant Physiol 132:1241–1248
Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286
Pan JW, Zhu MY, Chen H (2001) Aluminum induced cell death in root tip cells of barley. Environ Exp Bot 46:71–79
Panda SK, Yamamoto Y, Kondo H, Matsumoto H (2008) Mitochondrial alterations related to programmed cell death in tobacco cells under aluminum stress. C R Biologies 331:597–610
Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier J, Sonoda M, Lamb C, Delledonne M (2004) Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16:2785–2794
Planchet E, Jagadis-Gupta K, Sonoda M, Kaiser WM (2005) Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J 41:732–743
Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418
Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110
Rodriguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueno MC, del Rio AL, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide and calcium. Plant Physiol 150:229–243
Saviani EE, Orsi CH, Oliveira FP, Pinto-Maglio CAF, Salgado I (2002) Participation of the mitochondrial permeability transition pore in nitric oxide-induced plant cell death. FEBS Lett 510:136–140
Seregélyes C, Igamberdiev AU, Maassen A, Hennig J, Dudits D, Hill RD (2004) NO-degradation by alfalfa class 1 hemoglobin (Mhb1): a possible link to PR-1a gene expression in Mhb1-over producing tobacco plants. FEBS Lett 571:61–66
Sies H, Sharov VS, Klotz LO, Briviba K (1997) Glutathione peroxidase protects against peroxynitrite-mediated oxidations. A new function for selenoproteins as peroxynitrite reductase. J Biol Chem 272:27812–27817
Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167
Stohr C, Strube F, Marx G et al (2001) A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide form nitrite. Planta 212:835–841
Tabuchi A, Matsumoto H (2001) Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol Plant 112:353–358
Tewari RK, Hahn EJ, Paek KY (2008) Modulation of copper toxicityinduced oxidative damage by nitric oxide supply in the adventitious roots of Panax ginseng. Plant Cell Rep 27:171–181
Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322–331
Trujillo M, Alvarez MN, Peluffo G, Reeman BA, Radi R (1998) Xanthine oxidase-mediated decomposition of S-nitrosothiols. J Biol Chem 273:7828–7834
Tun NN, Holk A, Scherer GFE (2001) Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Lett 509:174–176
Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, FE Scherer G (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354
Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923
Wang WZ, Pan JW, Zheng K, Chen H, Shao HH, Guo YJ, Bian HW, Han N, Wang JH, Zhu MY (2009) Ced-9 inhibits Al-induced programmed cell death and promotes Al tolerance in tobacco. Biochem Biophys Res Commun 383:141–145
Wang HH, Huang JJ, Bi YR (2010) Nitrate reductase-dependent nitric oxide production is involved in aluminum tolerance in red kidney bean roots. Plant Sci 179(3):281–288
Wilkinson JQ, Crawford NM (1993) Identification and characterization of chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gen Genet 239:289–297
Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signaling in plants. Plant Cell Environ 31:622–631
Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765
Xu Jin, Wenying W, Hengxia Y, Xiaojing L, Hong S, Qin M (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330
Yakimova ET, Kapchina-Toteva VM, Woltering EJ (2007) Signal transduction events in aluminum-induced cell death in tomato suspension cells. J Plant Physiol 164:702–708
Yamamoto Y, Kobayashi Y, Devi SR, Rikishi S, Matsumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128:63–72
Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468:89–92
Yamasaki H, Shimoji H, Ohshiro Y, Sakihama Y (2001) Inhibitory effects of nitric oxide on oxidative phosphorylation in plant mitochondria. Nitric Oxide: Biology and Chemistry 5:261–270
Yang ZM, Wang J, Wang SW, Xu LL (2003) Salicylic acid-induced aluminum tolerance by modulation of citrate efflux from roots of Cassia tora L. Planta 217:168–174
Yu CC, Hung KT, Kao CH (2005) Nitric oxide reduces Cu toxicity and Cu-induced NH4+ accumulation in rice leaves. J Plant Physiol 162:1319–1330
Zeidler D, Zähringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J (2004) Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci USA 101:15811–15816
Zemojtel T, Frohlich A, Palmieri MC, Kolanczyk M, Mikula I, Wyrwicz LS, Wanker EE, Mundlos S, Vingron M, Martasek P et al (2006) Plant nitric oxide synthase: a never-ending story? Trends Plant Sci 11:524–525
Zhan J, Wang TJ, He HY, Li CZ, He LF (2011) Effects of SNP on AhSAG and AhBI-1 genes expression and amelioration of aluminum stress to peanut (Arachis hypoganea L.). Acta Agronomica Sinica 37:459–468
Zhang H, Li YH, Hu LY, Wang SH, Zhang FQ, Hu KD (2008a) Effects of exogenous nitric oxide donor on antioxidant metabolism in wheat leaves under aluminum stress. Russ J Plant Physiol 55:469–474
Zhang LP, Mehta SK, Liu ZP, Yang ZM (2008b) Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant Cell Physiol 49:411–419
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
Zhao MG, Chen L, Zhang LL, Zhang WH (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767
Zheng K, Pan JW, Ye L, Fu Y, Peng HZ, Wan BY, Gu Q, Bian HW, Han N, Wang JH, Kang B, Pan JH, Shao HH, Wang WZ, Zhu MY (2007) Programmed cell death-involved aluminum toxicity in yeast alleviated by antiapoptotic members with decreased calcium signals. Plant Physiol 143:38–49
Zottini M, Formentin E, Scattolin M, Carimi F, Lo Schiavo F, Terzi M (2002) Nitric oxide affects plant mitochondrial functionality in vivo. FEBS Lett 515:75–78
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We apologize to those colleagues whose work we did not review here. This work is supported by grants from the National Natural Science Foundation of China (grant nos. 30960181 and 30560070). No conflict of interest is declared.
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Handling Editor: Bhumi Nath Tripathi
Huyi He and Jie Zhan contributed equally to this review.
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He, H., Zhan, J., He, L. et al. Nitric oxide signaling in aluminum stress in plants. Protoplasma 249, 483–492 (2012). https://doi.org/10.1007/s00709-011-0310-5
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DOI: https://doi.org/10.1007/s00709-011-0310-5