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Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall

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Abstract

To study the mechanisms of exogenous NO contribution to alleviate the cadmium (Cd) toxicity in rice (Oryza sativa), rice plantlets subjected to 0.2-mM CdCl2 exposure were treated with different concentrations of sodium nitroprusside (SNP, a NO donor), and Cd toxicity was evaluated by the decreases in plant length, biomass production and chlorophyll content. The results indicated that 0.1 mM SNP alleviated Cd toxicity most obviously. Atomic absorption spectrometry and fluorescence localization showed that treatment with 0.1 mM SNP decreased Cd accumulation in both cell walls and soluble fraction of leaves, although treatment with 0.1 mM SNP increased Cd accumulation in the cell wall of rice roots obviously. Treatment with 0.1 mM SNP in nutrient solution had little effect on the transpiration rate of rice leaves, but this treatment increased pectin and hemicellulose content and decreased cellulose content significantly in the cell walls of rice roots. Based on these results, we conclude that decreased distribution of Cd in the soluble fraction of leaves and roots and increased distribution of Cd in the cell walls of roots are responsible for the NO-induced increase of Cd tolerance in rice. It seems that exogenous NO enhances Cd tolerance of rice by increasing pectin and hemicellulose content in the cell wall of roots, increasing Cd accumulation in root cell wall and decreasing Cd accumulation in soluble fraction of leaves.

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Abbreviations

Cd:

Cadmium

DAF-FM DA:

4-Amino-5-methylamino-2′, 7′-difluorofluorescein diacetate

DTT:

Dithiothreitol

EDTA:

Ethylenediaminetetraacetic acid

GalA:

Galacturonic acid

HC1:

Hemicellulose 1

HC2:

Hemicellulose 2

NO:

Nitric oxide

PCs:

Phytochelatins

PPFD:

Photosynthetic photon flux density

PVPP:

Polyvinylpolypyrrolidone

ROS:

Reactive oxygen species

SNP:

Sodium nitroprusside

References

  • Bazzaz FA, Rolfe GL, Carlson RW (1974) Effect of cadmium on photosynthesis and transpiration of excised leaves of corn and sunflower. Physiol Plant 31:373–377

    Article  Google Scholar 

  • Belleghem FV, Cuypers A, Semane B, Smeets K, Vangronsveld J, d’Haen J, Valcke F (2007) Subcellular localization of cadmium in roots and leaves of Arabidopsis thaliana. New Phytol 173:495–508

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Libourel IGL, Reinöhl V, Jones RL (2006) Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta 223:805–812

    Article  PubMed  CAS  Google Scholar 

  • Carrier P, Baryla A, Havaux M (2003) Cadmium distribution and microlocalization in oilseed rape (Brassica napus) after long-term growth on cadmium-contaminated soil. Planta 216:939–950

    PubMed  CAS  Google Scholar 

  • Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216

    PubMed  CAS  Google Scholar 

  • Correa-Aragunde N, Lombardo C, Lamattina L (2008) Nitric oxide: an active nitrogen molecule that modulates cellulose synthesis in tomato roots. New Phytol 179:386–396

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  PubMed  CAS  Google Scholar 

  • Crawford NM, Guo FQ (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci 10:195–200

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Durner J, Klessig D (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374

    Article  PubMed  CAS  Google Scholar 

  • Ernst WHO, Verkleij JAC, Schat H (1992) Metal tolerance in plants. Acta Bot Neerl 41:229–248

    CAS  Google Scholar 

  • Foresi NP, Laxalt AM, Tonón CV, Casalongué CA, Lamattina L (2007) Extracellular ATP induces nitric oxide production in tomato cell suspensions. Plant Physiol 145:589–592

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Groppa MD, Rosales EP, Iannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry 69:2609–2615

    Article  PubMed  CAS  Google Scholar 

  • Haag-Kerwer A, Schafer H, Heiss S, Walter C, Rausch T (1999) Cadmium exposure in Brassica juncea causes a decline in transpiration rate and leaf expansion without effect on photosynthesis. J Exp Bot 50:1827–1835

    Article  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  PubMed  CAS  Google Scholar 

  • He JY, Zhu C, Ren YF, Yan YP, Cheng C, Jiang DA, Sun ZX (2008) Uptake, subcellular distribution, and chemical forms of cadmium in wild-type and mutant rice. Pedosphere 18:371–377

    Article  CAS  Google Scholar 

  • Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238

    Article  CAS  Google Scholar 

  • Hsu YT, Kao CH (2005) Abscisic acid accumulation and cadmium tolerance in rice seedlings. Physiol Plant 124:71–80

    Article  CAS  Google Scholar 

  • Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, Ecker JR, Kaplan J, Guerinot ML (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314:1295–1298

    Article  PubMed  CAS  Google Scholar 

  • Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne A, Kumar D, Zhou J, Shah J, Zhang S, Kachroo R, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97:8849–8855

    Article  PubMed  CAS  Google Scholar 

  • Knudson LL, Tibbitts TW, Edwards GE (1977) Measurement of ozone injury by determination of leaf chlorophyll concentration. Plant Physiol 60:606–608

    Article  PubMed  CAS  Google Scholar 

  • Kopyra M, Gwóźdź 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

    Article  CAS  Google Scholar 

  • Lamattina L, García-Mata C, Graziano M, Pagnussat G (2003) Nitrate oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136

    Article  PubMed  CAS  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Liu D, Kottke I, Adam D (2007) Localization of cadmium in the root cells of Allium cepa by energy dispersive X-ray analysis. Biol Plant 51:363–366

    Article  CAS  Google Scholar 

  • Lozano-Rodríguez E, Hernández L, Bonay P, Carpenz-Ruiz RO (1997) Distribution of cadmium in shoot and root tissues of maize and pea plants: physiological disturbances. J Exp Bot 48:123–128

    Article  Google Scholar 

  • Mata CG, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204

    Article  CAS  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395

    Article  PubMed  CAS  Google Scholar 

  • Nishizona H, Zchikawa H, Suzuki S, Ishii F (1987) The role of the root cell wall in heavy metal tolerance of Athyrium yokosense. Plant Soil 101:15–20

    Article  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248

    Article  PubMed  CAS  Google Scholar 

  • 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 135:279–285

    Article  PubMed  CAS  Google Scholar 

  • Redeker ES, Campenhout KV, Bervoets L, Reijnders H, Blust R (2007) Subcellular distribution of Cd in the aquatic oligochaete Tubifex tubifex, implications for trophic availability and toxicity. Environ Pollut 148:166–175

    Article  Google Scholar 

  • Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanism of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433

    PubMed  CAS  Google Scholar 

  • Sanità di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Schlegel H, Godbold DL, Huttermann A (1987) Whole plant aspects of heavy metal induced changes in CO2 uptake and water relations of spruce (Picea abies) seedlings. Physiol Plant 69:265–270

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vázquez S, Goldsbrough P, Carpena RO (2006) Assessing the relative contributions of phytochelatins and the cell wall to cadmium resistance in white lupin. Physiol Plant 128:487–495

    Article  Google Scholar 

  • Wagner GJ (1993) Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51:173–212

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Liu YG, Zeng GM, Chai LY, Song XC, Min ZY, Xiao X (2008) Subcellular distribution and chemical forms of cadmium in Bechmeria nivea (L.) Guad. Environ Exp Bot 63:389–395

    Article  Google Scholar 

  • Wendehenne D, Durner J, Klessig D (2004) Nitric oxide: a new player in plant signaling and defence responses. Curr Opin Plant Biol 7:449–455

    Article  PubMed  CAS  Google Scholar 

  • Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signaling in plants. Plant Cell Environ 31:622–631

    Article  PubMed  CAS  Google Scholar 

  • Xiong J, Lu H, Lu K, Duan Y, Zhu C (2009) Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta doi:10.1007/s00425-009-0970-y

  • Yang Y, Yan CQ, Cao BH, Hu HX, Chen JP, Jiang DA (2007) Some photosynthetic responses to salinity resistance are transferred into the somatic hybrid descendants from the wild soybean Glycine cyrtoloba ACC547. Physiol Plant 129:658–669

    Article  Google Scholar 

  • Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. The International Rice Research Institute, Manila

    Google Scholar 

  • Zhao DY, Tian QY, Li YH, Zhang WH (2007) Nitric oxide is involved in nitrate-induced inhibition of root elongation in Zea mays. Ann Bot Lond 100:497–503

    Article  PubMed  CAS  Google Scholar 

  • Zhong H, Läuchli A (1993) Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. J Exp Bot 44:773–778

    Article  CAS  Google Scholar 

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Acknowledgments

The research was supported by the National Nature Science Foundation (No: 30671255), National Key Technology Research and Development Programm (No: 2006BAK02A18) and Project of National Key Basic Research and Development (2002CB410804) of China.

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Authors and Affiliations

  1. State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, 310058, Hangzhou, People’s Republic of China

    Jie Xiong, Lingyao An, Han Lu & Cheng Zhu

  2. State Key Laboratory of Rice Biology, China National Rice Research Institute, 359 Tiyuchang Road, 310006, Hangzhou, People’s Republic of China

    Jie Xiong

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  1. Jie Xiong
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Correspondence to Cheng Zhu.

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Xiong, J., An, L., Lu, H. et al. Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230, 755–765 (2009). https://doi.org/10.1007/s00425-009-0984-5

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