Abstract
The effects of nitric oxide (NO) on cadmium toxicity in Medicago truncatula seedlings were studied by investigating root growth and uptake of antioxidants, IAA and ions. Exposure to cadmium reduced root growth and NO accumulation, and increased the production of reactive oxygen species (ROS) in roots. Supplementation with NO improved root growth and reduced ROS accumulation in roots. The NO-scavenger cPTIO, the nitrate reductase (NR) inhibitor tungstate, and the NO synthase (NOS) inhibitor L-NAME all inhibited the accumulation of NO in roots and reversed the effects of NO in promoting the root growth and accumulation of proline and glutathione. Application of NO reduced auxin degradation by inhibiting the activity of IAA oxidase. Exogenous NO also enhanced the uptake of K+ and Ca2+. These results suggest that NO improves cadmium tolerance in plants by reducing oxidative damage, maintaining the auxin equilibrium and enhancing ion absorption.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anderson MD, Prasad TK, Stewart CR (1995) Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of Maize seedlings. Plant Physiol 109:1247–1257
Baker CJ, Mock NM (1994) An improved method for monitoring cell death in cell suspension and leaf disc assays using Evans blue. Plant Cell Tissue Org 39:7–12. doi:10.1007/BF00037585
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. doi:10.1093/jxb/erj175
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
Bates LS, Waldren RP, Tear ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207. doi:10.1007/BF00018060
Beligni MV, Lamattina L (2002) Nitric oxide interferes with plant photooxidative stress by detoxifying reactive oxygen species. Plant Cell Environ 25:737–748. doi:10.1046/j.1365-3040.2002.00857.x
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. doi:10.1104/pp.108.133348
Chaoui A, Ferjani EE (2005) Effects of cadmium and copper on antioxidant capacities, lignification and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. C R Biologies 328:23–31. doi:10.1016/j.crvi.2004.10.001
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. doi:10.1094/MPMI.2000.13.12.1380
Correa-Aragunde NM, Graziano ML, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905. doi:10.1007/s00425-003-1172-7
Correa-Aragunde N, Lanteri ML, Garcia-Mata C, Have A, Laxalt AM, Graziano M, Lamattina L (2007) Nitric oxide functions as intermediate in Auxin, Abscisic acid, and lipid signaling pathways. Plant Cell Monogr 5:1861–1370
Deng M, Moureaux T, Caboche M (1989) Tungstate, a molybdate analog inactivating nitrate reductase, deregulates the expression of the nitrate reductase structural gene. Plant Physiol 91:304–309. doi:10.1104/pp.91.1.304
Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–372. doi:10.1016/S1369-5266(99)00007-2
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. doi:10.1007/s11738-006-0006-1
Faivre-Rampant O, Kevers C, Gaspar T (2000) IAA-oxidase activity and auxin protectors in nonrooting rac mutant shoots of tobacco in vitro. Plant Sci 153:73–80. doi:10.1016/S0168-9452(99)00255-1
Farago ME, Mullen WA (1979) Plants which accumulate metals. IV. A possible copper-proline complex from the roots of Armeria maritima. Inorg Chim Acta 32:93–94. doi:10.1016/S0020-1693(00)91627-X
Gouvea CMCP, Souza JF, Magalhaes CAN, Martins IS (1997) NO releasing substances that induce growth elongation in maize root segments. Plant Growth Regul 21:183–187. doi:10.1023/A:1005837012203
Graziano M, Lamattina L (2007) Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. Plant J 52:949–960. doi:10.1111/j.1365-313X.2007.03283.x
Groppa MD, Rosales EP, Iannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry 69:2609–2615. doi:10.1016/j.phytochem.2008.07.016
Hernandez LE, Carpena-Ruiz R, Garate A (1996) Alterations in the mineral nutrition of pea seedlings exposed to cadmium. J Plant Nutr 19:1581–1598. doi:10.1080/01904169609365223
Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238. doi:10.1023/B:GROW.0000026514.98385.5c
Hu X, Neill S, Tang Z, Cai W (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670. doi:10.1104/pp.104.054494
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. doi:10.1007/s00425-006-0461-3
Kahn JS, Hanson JB (1957) The effect of calcium on potassium accumulation in corn and soybean roots. Plant Physiol 32:312–316. doi:10.1104/pp.32.4.312
Kopyra M, Stachon-Wilk M, Gwozdz EA (2006) Effects of exogenous nitric oxide on the antioxidant capacity of cadmium-treated soybean cell suspension. Acta Physiol Plant 28:525–536. doi:10.1007/s11738-006-0048-4
Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330. doi:10.1016/j.plantsci.2005.02.007
Lombardo MC, Graziano M, Polacco J, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33
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. doi:10.1002/1521-3846(200205) 22:1/2<101::AID-ABIO101>3.0.CO;2-N
Mendoza-Cozatl DG, Moreno-Sanchez R (2006) Control of glutathione and phytochelatin synthesis under cadmium stress. J Theor Biol 238:919–936. doi:10.1016/j.jtbi.2005.07.003
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. doi:10.1093/jexbot/53.372.1237
Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus satious L.) seed germination. Plant Cell Environ 20:600–608. doi:10.1111/j.1365-3040.1997.00072.x
Rodriguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gomez M, del Rio LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots: imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544. doi:10.1111/j.1365-3040.2006.01531.x
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. doi:10.1104/pp.108.131524
Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130. doi:10.1016/S0098-8472(98)00058-6
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. doi:10.1016/j.envexpbot.2007.12.005
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. doi:10.1105/tpc.004853
Sun BT, Jing Y, Chen KM, Song LL, Chen FJ, Zhang LX (2007) Protective effect of nitric oxide on iron deficiency-induced oxidative stress in maize (Zea mays). J Plant Physiol 164:536–543. doi:10.1016/j.jplph.2006.02.011
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. doi:10.1007/s11816-008-0052-9
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. doi:10.1016/j.envexpbot.2007.07.006
Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: a new player in plant signalling and defence response. Curr Opin Plant Biol 7:449–455. doi:10.1016/j.pbi.2004.04.002
Xu J, Yin HX, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28:325–333. doi:10.1007/s00299-008-0643-5
Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323. doi:10.1104/pp.127.1.315
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 (Taipei, Taiwan) 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. doi:10.1093/pcp/pcn017
Zhao LQ, Zhang F, Guo JK, Yang YL, Li BB, Zhang LX (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857. doi:10.1104/pp.103.030023
Zhu JK, Liu JP, Xiong LM (1998) Genetic Analysis of Salt Tolerance in Arabidopsis: Evidence for a Critical Role of Potassium Nutrition. Plant Cell 10:1181–1191
Acknowledgement
The research was supported by the Knowledge Innovation Program of the Chinese Academy of Sciences (Grant no. 0707013603).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible Editor: Juan Barcelo.
Rights and permissions
About this article
Cite this article
Xu, J., Wang, W., Yin, H. et al. Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326, 321–330 (2010). https://doi.org/10.1007/s11104-009-0011-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-009-0011-4