Skip to main content

Advertisement

SpringerLink
Log in

Nitric oxide-induced proteomic analysis in rice leaves

  • Original Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Nitric oxide (NO) is a ubiquitous bimolecule that regulates various physiological processes in plants. Despite the widespread study of NO in plants, the involvement of NO in proteomic regulation has been poorly investigated compared to the physiological processes. To explore the NO-induced proteomic regulation in rice leaves, 2-week-old leaves were exposed to sodium nitroprusside for 12 h. Protein profiles were analyzed by two-dimensional gel electrophoresis. A total of 53 NO-regulated proteins were identified by the matrix-assisted laser desorption/ionization-time of flight mass spectrometry analysis. Out of these proteins, 41 were up-regulated, 7 were down-regulated, and 5 were newly induced. The identified proteins were involved in photosynthesis, carbohydrate and energy metabolism, growth and development, metabolite biosynthesis, signal transduction, lignin modification, and defense response. Importantly, several key proteins including glutathione reductase, monodehydroascorbate reductase, dehydroascorbate reductase, ascorbate peroxidase, superoxide dismutase, catalase, 2-cysteine peroxiredoxin, peroxidase (newly induced), and glutathione S-transferase were significantly up-regulated in rice leaves and these proteins were associated with the ascorbate–glutathione cycle and ROS homeostasis system in plants. Thus, the identification of several key and newly induced proteins has provided a new insight into NO-mediated overall molecular response in plants.

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

Similar content being viewed by others

References

  • Adamu TA, Mun B-G, Lee S-U, Hussain A, Yun B-W (2018) Exogenously applied nitric oxide enhances salt tolerance in rice (Oryza sativa L.) at seedling stage. Agronomy 8:276

    Article  Google Scholar 

  • Alam I, Sharmin SA, Kim KH, Kim YG, Lee JJ, Lee BH (2013) An improved plant leaf protein extraction method for high resolution two-dimensional polyacrylamide gel electrophoresis and comparative proteomics. Biotech Histochem 88:61–75

    Article  CAS  PubMed  Google Scholar 

  • Aloisi I, Cai G, Serafini-Fracassini D, Del Duca S (2016) Polyamines in pollen: from microsporogenesis to fertilization. Front Plant Sci 7:155

    PubMed  PubMed Central  Google Scholar 

  • Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kosmala A (2011) Are nitric oxide donors a valuable tool to study the functional role of nitric oxide in plant metabolism? Plant Biol 13:747–756

    Article  CAS  PubMed  Google Scholar 

  • Badri DV, Loyola-Vargas VM, Du J, Stermitz FR, Broeckling CD, Iglesias-Andreu L, Vivanco JM (2008) Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytol 179:209–223

    Article  CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2016) Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front Plant Sci 7:152

    Article  PubMed  PubMed Central  Google Scholar 

  • Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W, Van Staveren M, Stiekema W, Drost L, Ridley P, Hudson SA, Patel K, Murphy G, Piffanelli P, Wedler H, Wedler E, Wambutt R, Weitzenegger T (1998) Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391:485

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Calderón A, Lázaro-Payo A, Iglesias-Baena I, Camejo D, Lázaro JJ, Sevilla F, Jiménez A (2017) Glutathionylation of pea chloroplast 2-Cys Prx and mitochondrial Prx IIF affects their structure and peroxidase activity and sulfiredoxin deglutathionylates only the 2-Cys Prx. Front Plant Sci 8:118

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Zou T, McCormick S (2016) S-Adenosylmethionine synthetase 3 is important for pollen tube growth. Plant Physiol 172:244–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho H, Ryu H, Rho S, Hill K, Smith S, Audenaert D, Park J, Han S, Beeckman T, Bennett MJ, Hwang D, De Smet I, Hwang I (2014) A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nat Cell Biol 16:66–76

    Article  CAS  PubMed  Google Scholar 

  • Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222

    Article  CAS  PubMed  Google Scholar 

  • Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diao Q-N, Song Y-J, Shi D-M, Qi H-Y (2016) Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersicon esculentum Mill.) seedling. J Zhejiang Univ Sci B 17:916–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diet A, Abbas K, Bouton C, Guillon B, Tomasello F, Fourquet S, Toledano MB, Drapier J-C (2007) Regulation of peroxiredoxins by nitric oxide in immunostimulated macrophages. J Biol Chem 282:36199–36205

    Article  CAS  PubMed  Google Scholar 

  • Fan H, Guo S, Jiao Y, Zhang R, Li J (2007) Effects of exogenous nitric oxide on growth, active oxygen species metabolism, and photosynthetic characteristics in cucumber seedlings under NaCl stress. Front Agric China 1:308–314

    Article  Google Scholar 

  • Gao X, Cox KL, He P (2014) Functions of calcium-dependent protein kinases in plant innate immunity. Plants 3:160–176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garg B, Vaid N, Tuteja N (2014) In-silico analysis and expression profiling implicate diverse role of EPSPS family genes in regulating developmental and metabolic processes. BMC Res Notes 7:58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261

    Article  CAS  PubMed  Google Scholar 

  • Gomi K, Yamamato H, Akimitsu K (2003) Epoxide hydrolase: a mRNA induced by the fungal pathogen Alternaria alternata on rough lemon (Citrus jambhiri Lush). Plant Mol Biol 53:189–199

    Article  CAS  PubMed  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 

  • Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4:419

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Nahar K, Hossain MS, Anee TI, Parvin K, Fujita M (2017) Nitric oxide pretreatment enhances antioxidant defense and glyoxalase systems to confer PEG-induced oxidative stress in rapeseed. J Plant Interact 12:323–331

    Article  CAS  Google Scholar 

  • Hayat S, Hasan SA, Mori M, Fariduddin Q, Ahmad A (2010) Nitric oxide: chemistry, biosynthesis, and physiological role. In: Hayat S et al (eds) Nitric oxide in plant physiology. Wiley-VCH, Germany, pp 1–16

  • Hill AC, Bennett J (1970) Inhibition of apparent photosynthesis by nitrogen oxides. Atmos Environ 4:341–348

    Article  CAS  Google Scholar 

  • Hisamatsu T, King RW, Helliwell CA, Koshioka M (2005) The involvement of gibberellin 20-oxidase genes in phytochrome-regulated petiole elongation of Arabidopsis. Plant Physiol 138:1106–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ho C-L, Noji M, Saito M, Saito K (1999) Regulation of serine biosynthesis in Arabidopsis : crucial role of plastidic 3-phosphoglycerate dehydrogenase in non-photosynthetic tissues. J Biol Chem 274:397–402

    Article  CAS  PubMed  Google Scholar 

  • Hussain A, Mun B-G, Imran QM, Lee S-U, Adamu TA, Shahid M, Kim K-M, Yun B-W (2016) Nitric oxide mediated transcriptome profiling reveals activation of multiple regulatory pathways in Arabidopsis thaliana. Front Plant Sci 7:975

    PubMed  PubMed Central  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 

  • Junge W, Nelson N (2015) ATP synthase. Ann Rev Biochem 84:631–657

    Article  CAS  PubMed  Google Scholar 

  • Khatai L, Goessler W, Lorencova H, Zangger K (2004) Modulation of nitric oxide-mediated metal release from metallothionein by the redox state of glutathione in vitro. Eur J Biochem 271:2408–2416

    Article  CAS  PubMed  Google Scholar 

  • Komatsu S, Yano H (2006) Update and challenges on proteomics in rice. Proteomics 6:4057–4068

    Article  CAS  PubMed  Google Scholar 

  • Lee K-W, Rahman MA, Kim K-Y, Choi GJ, Cha J-Y, Cheong MS, Shohael AM, Jones C, Lee S-H (2018) Overexpression of the alfalfa DnaJ-like protein (MsDJLP) gene enhances tolerance to chilling and heat stresses in transgenic tobacco plants. Turk J Biol 42:12–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S (2015) The Arabidopsis thaliana TCP transcription factors: a broadening horizon beyond development. Plant Signal Behav 10:e1044192

    PubMed  PubMed Central  Google Scholar 

  • Li S-B, Xie Z-Z, Hu C-G, Zhang J-Z (2016) A review of auxin response factors (ARFs) in plants. Front Plant Sci 7:47

    PubMed  PubMed Central  Google Scholar 

  • Mirza H, Hossain MA, Fujita M (2010) Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. Am J Plant Physiol 5:295–324

    Article  Google Scholar 

  • Morisseau C (2013) Role of epoxide hydrolases in lipid metabolism. Biochimie 95:91–95

    Article  CAS  PubMed  Google Scholar 

  • Oikawa T, Koshioka M, Kojima K, Yoshida H, Kawata M (2004) A role of OsGA20ox1, encoding an isoform of gibberellin 20-oxidase, for regulation of plant stature in rice. Plant Mol Biol 55:687–700

    Article  CAS  PubMed  Google Scholar 

  • Park C-J, Seo Y-S (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 31:323–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parry MAJ, Keys AJ, Madgwick PJ, Carmo-Silva AE, Andralojc PJ (2008) Rubisco regulation: a role for inhibitors. J Exp Bot 59:1569–1580

    Article  CAS  PubMed  Google Scholar 

  • Ponniah SK, Shang Z, Akbudak MA, Srivastava V, Manoharan M (2017) Down-regulation of hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase, cinnamoyl CoA reductase, and cinnamyl alcohol dehydrogenase leads to lignin reduction in rice (Oryza sativa L. ssp. japonica cv. Nipponbare). Plant Biotechnol Rep 11:17–27

    Article  Google Scholar 

  • Rahman MA, Alam I, Kim Y-G, Ahn N-Y, Heo S-H, Lee D-G, Liu G, Lee B-H (2015) Screening for salt-responsive proteins in two contrasting alfalfa cultivars using a comparative proteome approach. Plant Physiol Biochem 89:112–122

    Article  CAS  PubMed  Google Scholar 

  • Rahman MA, Kim Y-G, Alam I, Liu G, Lee H, Lee JJ, Lee B-H (2016) Proteome analysis of alfalfa roots in response to water deficit stress. JIA 15:1275–1285

    CAS  Google Scholar 

  • Reddy MSS, Chen F, Shadle G, Jackson L, Aljoe H, Dixon RA (2005) Targeted down-regulation of cytochrome P450 enzymes for forage quality improvement in alfalfa (Medicago sativa L.). Proc Nat Acad Sci USA 102:16573–16578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizwan M, Mostofa MG, Ahmad MZ, Imtiaz M, Mehmood S, Adeel M, Dai Z, Li Z, Aziz O, Zhang Y, Tu S (2018) Nitric oxide induces rice tolerance to excessive nickel by regulating nickel uptake, reactive oxygen species detoxification and defense-related gene expression. Chemosphere 191:23–35

    Article  CAS  PubMed  Google Scholar 

  • Rőszer T (2012) Nitric oxide synthesis in the chloroplast. The biology of subcellular nitric oxide. Springer, Berlin, pp 49–66

    Book  Google Scholar 

  • Sami F, Faizan M, Faraz A, Siddiqui H, Yusuf M, Hayat S (2018) Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide 73:22–38

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Aguayo I, Rodríguez-Galán JM, García R, Torreblanca J, Pardo JM (2004) Salt stress enhances xylem development and expression of S-adenosyl-l-methionine synthase in lignifying tissues of tomato plants. Planta 220:278–285

    Article  CAS  PubMed  Google Scholar 

  • Sang J-R, Jiang M, Lin F, Li J, Xu S-C (2008) Role of nitric oxide in abscisic acid-induced subcellular antioxidant defense of maize leaves. J Plant Physiol Mol Biol 33:553–566

    Google Scholar 

  • Sharmin SA, Alam I, Rahman MA, Kim K-H, Kim Y-G, Lee B-H (2013) Mapping the leaf proteome of Miscanthus sinensis and its application to the identification of heat-responsive proteins. Planta 238:459–474

    Article  CAS  PubMed  Google Scholar 

  • Singh PK, Indoliya Y, Chauhan AS, Singh SP, Singh AP, Dwivedi S, Tripathi RD, Chakrabarty D (2017) Nitric oxide mediated transcriptional modulation enhances plant adaptive responses to arsenic stress. Sci Rep 7:3592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song Y, Chen Q, Ci D, Shao X, Zhang D (2014) Effects of high temperature on photosynthesis and related gene expression in poplar. BMC Plant Biol 14:111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzin V, Galili G (2010) The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. Arabidopsis Book 8:e0132

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Meng Y, Li B, Ma X, Lai Y, Si E, Yang K, Xu X, Shang X, Wang H, Wang D (2015) Physiological and proteomic analyses of salt stress response in the halophyte Halogeton glomeratus. Plant Cell Environ 38:655–669

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Cai X, Xu C, Wang Q, Dai S (2016) Drought-responsive mechanisms in plant leaves revealed by proteomics. Int J Mol Sci 17:1706

    Article  CAS  PubMed Central  Google Scholar 

  • Yang L, Tian D, Todd CD, Luo Y, Hu X (2013) Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity. J Proteome Res 12:1316–1330

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Ji J, Harris-Shultz KR, Wang H, Wang H, Abd-Allah EF, Luo Y, Hu X (2016) The dynamic changes of the plasma membrane proteins and the protective roles of nitric oxide in rice subjected to heavy metal cadmium stress. Front Plant Sci 7:190

    PubMed  PubMed Central  Google Scholar 

  • Yudina RS (2012) Malate dehydrogenase in plants: its genetics, structure, localization and use as a marker. ABB 3:370–377

    Article  CAS  Google Scholar 

  • Zeng L, Deng R, Guo Z, Yang S, Deng X (2016) Genome-wide identification and characterization of glyceraldehyde-3-phosphate dehydrogenase genes family in wheat (Triticum aestivum). BMC Genom 17:240

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2015R1D1A1A01060495). We thank all co-researchers of National Institute of Animal Science (NIAS) for their contribution with helpful discussion and valuable comments to make this research meaningful.

Author information

Author notes

  1. Ki-Won Lee and Md. Atikur Rahman contributed equally to this work.

Authors and Affiliations

  1. Molecular Breeding Laboratory, Grassland and Forages Division, National Institute of Animal Science, Rural Development Administration, Cheonan, 31000, Republic of Korea

    Ki-Won Lee, Md. Atikur Rahman & Sang-Hoon Lee

  2. Division of Applied Life Sciences (BK21Plus), and ILAS, Gyeongsang National University, Jinju, 52828, Republic of Korea

    Yong-Goo Kim & Byung-Hyun Lee

  3. Department of Biotechnology, College of Life Science and Biotechnology, Yonsei University, Seoul, 03722, Republic of Korea

    Dong-Gi Lee

  4. Feed and Forage Biosciences, International Livestock Research Institute, PO Box 5689, Addis Ababa, Ethiopia

    Chris Stephen Jones

Authors
  1. Ki-Won Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Md. Atikur Rahman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sang-Hoon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yong-Goo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dong-Gi Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chris Stephen Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Byung-Hyun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Byung-Hyun Lee.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1313 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, KW., Rahman, M.A., Lee, SH. et al. Nitric oxide-induced proteomic analysis in rice leaves. Plant Biotechnol Rep 13, 375–387 (2019). https://doi.org/10.1007/s11816-019-00544-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-019-00544-1

Keywords

Search

Navigation