Abstract
Cadmium (Cd) toxicity inhibited the seedling growth while inducing the occurrences of lateral roots (LR) and adventitious roots (AR). Further study indicated that auxin and nitric oxide (NO) are involved in the processes. In this study, we chose model plant Arabidopsis thaliana and Cd-hyperaccumulator Solanum nigrum as material to examine the involvement of Cd-induced auxin redistribution in NO accumulation in plants and the effect of NO on Cd accumulation. For this aim, the histochemical staining, NO fluorescence probe (DAF-2DA) detections combined with the pharmacological study were used in this study. By using DR5:GUS staining analysis combined with NO fluorescence probe (DAF-2DA) detection, we found that Cd-induced NO accumulation is at least partly due to auxin redistribution in plants exposure to Cd. Supplementation with SNP donor S-nitrosoglutathione (GSNO) increased the number of LR and AR. In contrast, NO-scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethyl imidazoline-1-oxyl-3-oxide (cPTIO) reversed the effects of NO on modulating root system architecture and Cd accumulation. These results suggest that manipulation of the NO level is an effective approach to improve Cd tolerance in plants by modulating the development of LR and AR, and provide insights into novel strategies for phytoremediation.
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Abbreviations
- ABA:
-
Abscisic acid
- AR:
-
Adventitious root
- CAT:
-
Catalase
- cPTIO:
-
2-(4-carboxyphenyl)-4,4,5,5-tetramethyl imidazoline-1-oxyl- 3-oxide
- DAB:
-
3-diaminobenzidine
- DAF-2 DA:
-
4,5-diaminofluorescein diacetate
- DCFH-DA:
-
2,7-dichlorfluorescein-diacetate
- GSNO:
-
Sodium nitroprusside
- GUS:
-
3-glucuronidase
- IAA:
-
Indole acetic acid
- ICP-MS:
-
Inductively coupled plasma-mass spectroscopy
- LR:
-
Lateral root
- NBT:
-
Nitroblue tetrazolium
- NPA:
-
N-1- naphthylphthalamic acid
- NO:
-
Nitric oxide
- PR:
-
Primary root
- PVP:
-
Polyvinylpyrrolidone
- ROS:
-
Reactive oxygen species
- SOD:
-
Super- oxide dismutase
- TIBA:
-
2,3,5-triiodobenzoic acid
- X-Gluc:
-
5-bromo-4-chloro- 3-indolyl-β-D-glucuronic acid cyclohexyl-ammonium
References
Baker CJ, Mock NM (1994) An improved method for monitoring cell death in cell suspension and leaf disc Plant Soil assays using Evans blue. Plant Cell Tissue Org 39:7–12
Barroso JB, Corpas FJ, Carreras A, Rodriguez-Serrano M, Esteban FJ, Fernandez-Ocana A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Rio LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under Cd stress. J Exp Bot 57:1785–1794
Bartha B, Kolbert Z, Erdei L (2005) Nitric oxide production induced by heavy metals in Brassica juncea L. Czern. and Pisum sativum L. Acta Biol Szegediensis 49:9–12
Berkelaar E, Hale B (2000) The relationship between root morphology and cadmium accumulation in seedlings of two durum wheat cultivars. Can J Bot 78:81–387
Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, 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
Correa-Aragunde NM, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905
De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, Sanità di Toppi L, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228
Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459
Dhindsa RS, Plumb-Dhindsa P, Throne TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
Errabii T, Gandonou CB, Essalmani H, Abrini J, Idaomar M, Senhaji NS (2007) Effects of NaCl and mannitol induced stress on sugarcane (Saccharum sp.) callus cultures. Acta Physiol Plant 29:95–102
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif. Aes. Bull. 347. University of California Agricultura1 Experiment Station, Berkeley, pp 1–39
Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238
Kolberz Z, Bartha B, Erdei L (2008) Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordial. J Plant Physiol 165:967–975
Kopyra M, Gwózdz EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017
Lamattina L, Garcia-Mata C, Graziano M, Pagnusat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136
Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330
Libourel IGL, Bethke PC, De Michele R, Jones RL (2006) Nitric oxide gas stimulates germination of dormant Arabidopsis seeds: use of a flow-through apparatus for delivery of nitric oxide. Planta 223:813–820
Lozano-Juste J, León J (2010) Enhanced ABA-mediated Responses in nia1nia2noa1-2 Triple Mutant Impaired in NIA/NR- and AtNOA1-dependent NO Biosynthesis in Arabidopsis. Plant Physiol. doi:10.1104/pp.109.148023
Lu LL, Tian SK, Yang XE, Wang XC, Brown P, Li TQ, He ZL (2008) Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. J Exp Bot 59:3203–3213
Macek T, Mackova M, Pavlikova D, Szakova J, Truksa M, Singh Cundy A, Kotrba P, Yancey N, Scouten WH (2002) Accumulation of cadmium by transgenic tobacco. Acta Biotechnol 22:101–106
Martin M, Colman MJR, Gomez-Casati DF, Lamattina L, Zabaleta EJ (2009) Nitric oxide accumulation is required to protect against iron-mediated oxidative stress in frataxin-deficient Arabidopsis plants. FEBS Lett 583:542–548
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497
Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247
Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956
Parker DR, Norvell WA, Chaney RL (1995) Geochem-PC: a chemical speciation program for IBM compatibles. In: Loeppert RH, Schwab AP, Goldberg S (eds) Chemical equilibrium and reaction models. Soil Science Society of America, Madison, pp 253–269
Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105
Ramel F, Sulmon C, Bogard M, Couee I, Gouesbet G (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol 9:28–45
Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Río LA, 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
Schmidt W, Tittel J, Schikora A (2000) Role of hormones in the induction of iron deficiency responses in Arabidopsis roots. Plant Physiol 122:1109–1118
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
Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847
Sun BT, Jing Y, Chen KM, Song LL, Chen FJ, Zhang LX (2007) Protective effect of nitric oxide on iron deficiencyinduced oxidative stress in maize (Zea mays). J Plant Physiol 164:536–543
Tewari RK, Kim SY, Hahn EJ, Paek KY (2008) Involvement of nitric oxide-induced NADPH oxidase in adventitious root growth and antioxidant defense in Panax ginseng. Plant Biotechnol Rep 2:113–122
Ulmasov T, Murfett J, Hagen G, Guilfoyle T (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971
Vital SA, Fowler RW, Virgen A, Gossett DR, Banks SW, Rodriguez J (2008) Opposing roles for superoxide and nitric oxide in the NaCl stress-induced upregulation of antioxidant enzyme activity in cotton callus tissue. Environ Exp Bot 62:60–68
Wagner GJ (1993) Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51:173–212
Wang HH, Liang XL, Wan Q, Wang XM, Bi YR (2009) Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 230:293–307
Xu J, Yin HX, Liu XJ, Yuan T, Mi Q, Yang LL, Xie ZX, Wang WY (2009a) Nitric oxide alleviates Fe deficiency-induced stress in Solanum nigrum. Biol Plant 53:784–788
Xu J, Yin HX, Li X (2009b) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28:325–333
Xu J, Wang WY, Yin HX, Liu XJ, Sun H, Mi Q (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
Yang JD, Yun JY, Zhang TH, Zhao HL (2006) Presoaking with nitric oxide donor SNP alleviates heat shock damages in mung bean leaf discs. Bot Stud 47:129–136
Zhang LP, Mehta SK, Liu ZP, Yang ZM (2008) Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant Cell Physiol 49:411–419
Zhang S, Zhang H, Qin R, Jiang W, Liu D (2009) Cadmium induction of lipid peroxidation and effects on root tip cells and antioxidant enzyme activities in Vicia faba L. Ecotoxicology 18:814–823
Acknowledgments
This work was supported by the National Major Special Project on New Varieties Cultivation for Transgenic Organisms (2009ZX08009-130B), the National Basic Research Program of China (2009CB421102, 2009CB118305), the Science and Technology Key Project of Education Ministry, P. R. China (209133), the National Key Technologies R&D Program of China (2009BADA3B04) and the Knowledge Innovation Program of the Chinese Academy of Sciences (KSCX2-EW-Q-25, KZCX2-YW-447).
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Xu, J., Wang, W., Sun, J. et al. Involvement of auxin and nitric oxide in plant Cd-stress responses. Plant Soil 346, 107–119 (2011). https://doi.org/10.1007/s11104-011-0800-4
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DOI: https://doi.org/10.1007/s11104-011-0800-4