Skip to main content
SpringerLink
Log in

Nitric oxide production and scavenging in waterlogged roots of rape seedlings

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

When plant roots are waterlogged, plants can experience hypoxic stress. Large quantities of nitric oxide (NO) can be generated under hypoxic conditions as a result of nitrate reduction. Our objective was to investigate the molecular mechanisms behind NO production and scavenging (turnover) in waterlogged roots of rape (‘Tammi’ variety) seedlings by surveying waterlogging-responsive genes. Waterlogging for up to 72 h enhanced NO production rapidly in the roots. Of 53,107 genes assayed, 9,692 showed a twofold change in expression within 36 h of waterlogging. Two nitrate reductase (NaR) genes (TC201891, TC161540) and four nitrite reductase (NiR) genes (TC168889, TC164215, TC163914, TC185634) were potentially involved in NO production in response to waterlogging stress. Strong hypoxic induction of non-symbiotic hemoglobin (Hb) gene (TC165566), which increased 656- and 645-fold at 36 and 72 h of waterlogging, respectively, could oxidize the NO overproduced in the roots. Our results suggested that reduction of nitrate to NO by NaR and NiR and subsequent NO turnover by Hb provide a mechanism for maintaining bioenergetics in waterlogged roots. The up-regulation of many additional waterlogging-responsive genes with potential roles in the anaerobic respiration, sucrose and starch degradation, glycolysis, and pyruvate metabolism, may acclimate the plant to waterlogging-induced hypoxic condition.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. Gene Ontol Consort, Nat Genet 25:25–29

    Article  CAS  Google Scholar 

  • Benamar A, Rolletschek H, Borisjuk L, Avelange-Macherel MH, Curien G, Mostefai HA, Andriantsitohaina R, Macherel D (2008) Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta 1777:1268–1275

    Article  CAS  PubMed  Google Scholar 

  • Borisjuk L, Macherel D, Benamar A, Wobus U, Rolletschek H (2007) Low oxygen sensing and balancing in plant seeds: a role for nitric oxide. New Phytol 176:813–823

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform 11:485

    Article  Google Scholar 

  • Dolferus R, Klok EJ, Ismond K, Delessert C, Wilson S, Good A, Peacock J, Dennis L (2001) Molecular basis of the anaerobic response in plants. IUBMB Life 51:79–82

    Article  CAS  PubMed  Google Scholar 

  • Dordas C, Hasinoff BB, Igamberdiev AU, Manac’h 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

    Article  CAS  PubMed  Google Scholar 

  • Ghigo D, Riganti C, Gazzano E, Costamagna C, Bosia A (2006) Cycling of NADPH by glucose 6-phosphate dehydrogenase optimizes the spectrophotometric assay of nitric oxide synthase activity in cell lysates. Nitric Oxide 15:148–153

    Article  CAS  PubMed  Google Scholar 

  • Gupta KJ, Igamberdiev AU (2011) The anoxic plant mitochondrion as a nitrite: NO reductase. Mitochondrion 11:537–543

    Article  CAS  PubMed  Google Scholar 

  • Gupta KJ, Igamberdiev AU, Manjunatha G, Segu S, Moran JF, Neelawarne B, Bauwe H, Kaiser WM (2011) The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Sci 181:520–526

    Article  CAS  PubMed  Google Scholar 

  • Hebelstrup KH, Igamberdiev AU, Hill RD (2007) Metabolic effects of hemoglobin gene expression in plants. Gene 398:86–93

    Article  CAS  PubMed  Google Scholar 

  • Hoffman NE, Bent AF, Hanson AD (1986) Induction of lactate dehydrogenase isozymes by oxygen deficit in barley root tissue. Plant Physiol 82:658–663

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Horchani F, Prevot M, Boscari A, Evangelisti E, Meilhoc E, Bruand C, Raymond P, Boncompagni E, Aschi-Smiti S, Puppo A, Brouquisse R (2011) Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol 155:1023–1036

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Hill RD (2004) Nitrate, NO and hemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot 55:2473–2482

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Hill RD (2009) Plant mitochondrial function during anaerobiosis. Ann Bot 103:259–268

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Seregelyes C, Manac’h N, Hill RD (2004) NADH-dependent metabolism of nitric oxide in alfalfa root cultures expressing barley hemoglobin. Planta 219:95–102

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Bykova NV, Hill RD (2006) Nitric oxide scavenging by barley hemoglobin is facilitated by a monodehydroascorbate reductase-mediated ascorbate reduction of methemoglobin. Planta 223:1033–1040

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Bykova NV, Shah JK, Hill RD (2010) Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol Plant 138:393–404

    Article  CAS  PubMed  Google Scholar 

  • Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ku Y-G, Park W, Bang J-K, Jang Y-S, Kim Y-B, Bae H-J, Suh M-C, Ahn S-J (2009) Physological response, fatty acid composition and yield component of Brassica napus L. under short-term waterlogging. J Bio-Environ Cont 18:142–147

    Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee Y-H, Kim K-S, Jang Y-S, Hwang J-H, Lee D-H, Choi I-H (2014) Global gene expression responses to waterlogging in leaves of rape seedlings. Plant Cell Rep 33:289–299

    Article  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by rna-seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Ricard B, VanToai R, Chourey P, Saglio P (1998) Evidence for the critical role of sucrose synthase for anoxic tolerance of maize roots using a double mutant. Plant Physiol 116:1323–1331

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stoimenova M, Libourel IGL, Ratcliffe RG, Kaiser WM (2003) The role of nitrate reduction in the anoxic metabolism of roots. II. Anoxic metabolism of tobacco roots with or without nitrate reductase activity. Plant Soil 253:155–167

    Article  CAS  Google Scholar 

  • Stoimenova M, Igamberdiev AU, Gupta KJ, Hill RD (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226:465–474

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NaR-dependent formation of active nitrogen species. FEBS Lett 468:89–92

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by a grant from the Rural Development Administration (Project No: PJ008761) in Republic of Korea.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Bioenergy Crop Research Center, National Institute of Crop Science, Rural Development Administration, Muan, 533-834, Republic of Korea

    Yong-Hwa Lee, Kwang-Soo Kim, Young-Seok Jang & In-Hu Choi

Authors
  1. Yong-Hwa Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kwang-Soo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Young-Seok Jang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. In-Hu Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yong-Hwa Lee.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, YH., Kim, KS., Jang, YS. et al. Nitric oxide production and scavenging in waterlogged roots of rape seedlings. Genes Genom 36, 691–699 (2014). https://doi.org/10.1007/s13258-014-0202-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-014-0202-0

Keywords

Search

Navigation