Skip to main content
Log in

Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Cadmium (Cd) is toxic to crown roots (CR), which are essential for maintaining normal growth and development in rice seedlings. Nitric oxide (NO) is an important signaling molecule that plays a pivotal role in plant root organogenesis. Here, the effects of Cd on endogenous NO content and root growth conditions were studied in rice seedlings. Results showed that similar to the NO scavenger, cPTIO, Cd significantly decreased endogenous NO content and CR number in rice seedlings, and these decreases were recoverable with the application of sodium nitroprusside (SNP, a NO donor). Microscopic analysis of root collars revealed that treatment with Cd and cPTIO inhibited CR primordia initiation. In contrast, although SNP partially recovered Cd-caused inhibition of CR elongation, treatment with cPTIO had no effect on CR elongation. l-NMMA, a widely used nitric oxide synthase (NOS) inhibitor, decreased endogenous NO content and CR number significantly, while tungstate, a nitrate reductase (NR) inhibitor, had no effect on endogenous NO content and CR number. Moreover, enzyme activity assays indicated that treatment with SNP inhibited NOS activity significantly, but had no effect on NR activity. All these results support the conclusions that a critical endogenous NO concentration is indispensable for rice CR primordia initiation rather than elongation, NOS is the main source for endogenous NO generation, and Cd decreases CR number by inhibiting NOS activity and thus decreasing endogenous NO content in rice seedlings.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

AR:

Adventitious roots

CR:

Crown roots

DTT:

Dithiothreitol

EDTA:

Ethylenediaminetetraacetic acid

FAD:

Flavin adenine dinucleotide

FMN:

Flavin mononucleotide

LR:

Lateral roots

NO:

Nitric oxide

NOS:

Nitric oxide synthase

NR:

Nitrate reductase

PR:

Primary root

SNP:

Sodium nitroprusside

References

  • Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ, Fernández-Ocaña A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Río LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793

    Article  PubMed  CAS  Google Scholar 

  • 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 Szeged 49:9–12

    Google Scholar 

  • Beligni MV, Lamattina L (2002) Nitric oxide interferes with plant photo-oxidative stress by detoxifying reactive oxygen species. Plant Cell Environ 25:737–748

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Chaki M, Fernández-Ocaña AM, Valderrama R, Carreras A, Esteban FJ, Luque F, Gómez-Rodríguez MV, Begara-Morales JC, Corpas FJ, Barroso JB (2009) Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower–mildew interaction. Plant Cell Physiol 50:265–279

    Article  PubMed  CAS  Google Scholar 

  • Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, León AM, Sandalio LM, del Río LA (2006) Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224:246–254

    Article  PubMed  CAS  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  PubMed  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 

  • Fusconi A, Repetto O, Bona E, Massa N, Gallo C, Dumas-Gaudot E, Berta G (2006) Effects of cadmium on meristem activity and nucleus ploidy in roots of Pisum sativum L. cv. Frisson seedlings. Environ Exp Bot 58:253–260

    Article  CAS  Google Scholar 

  • Fusconi A, Gallo C, Camusso W (2007) Effects of cadmium on root apical meristems of Pisum sativum L.: cell viability, cell proliferation and microtubule pattern as suitable markers for assessment of stress pollution. Mutat Res Genet Toxicol Environ Mutagen 632:9–19

    Article  CAS  Google Scholar 

  • Furchgott RF (1995) Special topics: nitric oxide. Annu Rev Physiol 57:659–682

    Article  Google Scholar 

  • Gouvêa CMCP, Souza JF, Magalhães ACN, Martins IS (1997) NO-releasing substances that induce growth elongation in maize root segments. Plant Growth Regul 21:183–187

    Article  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 

  • Guo B, Liang YC, Zhu YG, Zhao FJ (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 147:743–749

    Article  PubMed  CAS  Google Scholar 

  • Hochholdinger F, Park WJ, Sauer M, Woll K (2004) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci 9:42–48

    Article  PubMed  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 

  • Inukai Y, Miwa M, Nagato Y, Kitano H, Yamauchi A (2001) Characterization of rice mutants deficient in the formation of crown roots. Breed Sci 51:123–129

    Article  CAS  Google Scholar 

  • Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387–1396

    Article  PubMed  CAS  Google Scholar 

  • Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47

    Article  PubMed  CAS  Google Scholar 

  • Kaufman PB (1959) Development of the shoot of Oryza sativa L. III. Early stages in histogenesis of the stem and ontogeny of the adventitious root. Phytomorphology 9:382–404

    Google Scholar 

  • Kawata S, Harada J (1975) On the development of the crown root primordial in rice plants. Proc Crop Sci Soc Jpn 45:438–457

    Google Scholar 

  • Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218

    Article  PubMed  CAS  Google Scholar 

  • Kopyra M, Gwóźdź E (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 441:1011–1017

    Article  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 HJ, Wang SF, Yu XB, Yu J, He XW, Zhang SL, Shou HX, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43:47–56

    Article  PubMed  Google Scholar 

  • Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33

    PubMed  Google Scholar 

  • Lozano-Rodríguez E, Hernández LE, Bonay P, Carpena-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 

  • Malamy JE, Benfey PN (1997) Down and out in Arabidopsis: the formation of lateral roots. Trends Plant Sci 2:390–396

    Article  Google Scholar 

  • Metwally A, Finkemeier I, Georgi M, Dietz K (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281

    Article  PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytol 159:11–35

    Article  CAS  Google Scholar 

  • Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59:25–35

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    Article  PubMed  CAS  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 

  • Perrine-Walker FM, Gartner E, Hocart CH, Becker A, Rolfe BG (2007) Rhizobium-initiated rice growth inhibition caused by nitric oxide accumulation. Mol Plant Microbe Interact 20:283–292

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río 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

    Article  PubMed  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    PubMed  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 

  • Tamás L, Dudíková J, Ďurčeková K, Huttová J, Mistrík I, Zelinová V (2007) The impact of heavy metals on the activity of some enzymes along the barley root. Environ Exp Bot 62:86–91

    Article  Google Scholar 

  • Tewari RK, Hahn EJ, Paek KY (2008) Modulation of copper toxicity-induced oxidative damage by nitric oxide supply in the adventitious roots of Panax ginseng. Plant Cell Rep 27:171–181

    Article  PubMed  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 

  • Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, del Río LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461

    Google Scholar 

  • Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the root of Cassia tora L. Plant Cell Physiol 46:1915–1923

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Zhu L, Shou HX, Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46:1674–1681

    Article  PubMed  CAS  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 

  • Yeh CM, Chien PS, Huang HJ (2007) Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J Exp Bot 58:659–671

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  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  CAS  Google Scholar 

Download references

Acknowledgments

The research was supported by the National Nature Science Foundation (No: 30671255), National Key Technology Research and Development Programme (No: 2006BAK02A18) and Project of National Key Basic Research and Development (2002CB410804) of China. We thank Dr Mosun Chen for technical assistants with microscopic analysis of CR primordia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cheng Zhu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xiong, J., Lu, H., Lu, K. et al. Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta 230, 599–610 (2009). https://doi.org/10.1007/s00425-009-0970-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-0970-y

Keywords

Navigation