Top

Published in:

Open Access 01-12-2019 | Short report

Melatonin is responsible for rice resistance to rice stripe virus infection through a nitric oxide-dependent pathway

Authors: Rongfei Lu, Zhiyang Liu, Yudong Shao, Feng Sun, Yali Zhang, Jin Cui, Yijun Zhou, Wenbiao Shen, Tong Zhou

Published in: Virology Journal | Issue 1/2019

Abstract

Rice stripe virus (RSV) causes one of the most important rice virus diseases of plants in East Asia. However, the molecular mechanisms controlling rice resistance to RSV infection are largely unknown. Recently, several studies presented a novel model that melatonin (MT) and nitric oxide (NO) participate in the plant-pathogen interaction in a synergetic manner. In this study, there was a difference in MT content between two rice varieties that correlated with one being susceptible and one being resistant to RSV, which suggested that MT is related to RSV resistance. In addition, a test with two NO biosynthesis inhibitors revealed that NO inhibitor were able to increase the disease incidence of RSV. A pharmacological experiment with exogenous MT and NO showed that increased MT and NO in the MT-pretreated plants led to lower disease incidences; however, only NO increased in a NO-releasing reagent [sodium nitroprusside (SNP)] pretreated plants. The expressions level of OsPR1b and OsWRKY 45 were significantly induced by MT and NO. These results suggest that rice resistance to RSV can be improved by increased MT through a NO-dependent pathway.

Available only for authorised users

Milne RG. The Filamentous Plant Viruses. In: Milne RG, editor. The Plant Viruses. New York: Plenum Press; 1988. p. 297–329.CrossRef

Sun F, Yuan X, Zhou T, Fan Y, Zhou Y. Arabidopsis is susceptible to Rice stripe virus infections. J Phytopathol. 2011;159:767–72.CrossRef

Toriyama S. Rice stripe virus: prototype of a new group of viruses that replicate in plants and insects. Microbiol Sci. 1986;3:347.PubMed

Yamashit S, Doi Y, Yora K. Intracellular appearance of rice stripe virus. Ann Phytopathol Soc Jpn. 1985;51:637–41.CrossRef

Lerner A, Case J, Takahashi Y, Lee TH. Isolation of melatonin, the pineal gland factor that lightens melanocytes. J Amer Chem Soc. 1958;80:10.CrossRef

Arnao MB, Hernándezruiz J. The physiological function of melatonin in plants. Plant Signal Behav. 2006;1:89–95.PubMedPubMedCentralCrossRef

Reiter R, Tan D, Fuentesbroto L. Melatonin: a multitasking molecule. Prog Brain Res. 2010;181:127–51.PubMedCrossRef

Liang C, Zheng G, Li W, Wang Y, Hu B, Wang H, et al. Melatonin delays leaf senescence and enhances salt stress tolerance in Rice. J Pineal Res. 2015;59:91.PubMedCrossRef

Zhang N, Sun Q, Zhang H, Zhao C, Li L, Chen M. Roles of melatonin in abiotic stress resistance in plants. J Exp Bot. 2015;66:647.PubMedCrossRef

10.

Bonilla E, Valero N, Chacín-Bonilla L, Medina-Leendertz SJ. Melatonin and viral infections. J Pineal Res. 2004;36:73–9.PubMedCrossRefPubMedCentral

11.

Lee H, Byeon Y, Back K. Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco. J Pineal Res. 2014;57:262–8.PubMedCrossRef

12.

Arnao MB, Hernández-Ruiz J. Functions of melatonin in plants. J Pineal Res. 2015;59:133.PubMedCrossRef

13.

Shi H, Chen Y, Tan D, Reiter R, Chan Z, He C. Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis. J Pineal Res. 2015;59:102–8.PubMedCrossRef

14.

James SL. Role of nitric oxide in parasitic infections. Microbiol Rev. 1995;59:533–47.PubMedPubMedCentral

15.

Akaike T, Maeda H. Nitric oxide and virus infection. Immunology. 2000;101:300–8.PubMedPubMedCentralCrossRef

16.

Hong JK, Yun BW, Kang JG, Raja MU, Kwon E, Sorhagen K, et al. Nitric oxide function and signalling in plant disease resistance. J Exp Bot. 2008;59:147–54.PubMedCrossRef

17.

Perchepied L, Balagué C, Riou C, Claudel-Renard C, Rivière N, Grezes-Besset B, et al. Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Mol Plant Microbe In. 2010;23:846–60.CrossRef

18.

Madhu B, Singh K, Saminathan M, Singh R, Shivasharanappa N, Sharma A, et al. Role of nitric oxide in the regulation of immune responses during rabies virus infection in mice. Virus disease. 2016;27:387–99.PubMedCrossRefPubMedCentral

19.

Gupta KJ, Fernie AR, Kaiser WM, Dongen JT. On the origins of nitric oxide. Trends Plant Sci. 2011;16:160–8.PubMedCrossRef

20.

Crawford NM. Mechanisms for nitric oxide synthesis in plants. J Exp Bot. 2006;57:471–8.PubMedCrossRef

21.

Besson-Bard A, Pugin A, Wendehenne D. New insights into nitric oxide signaling in plants. The Annual Review of Plant Biology. 2008;59:21–39.PubMedCrossRef

22.

Kang K, Lee K, Park S, Byeon Y, Back K. Molecular cloning of rice serotonin N-acetyltransferase, the penultimate gene in plant melatonin biosynthesis. J Pineal Res. 2013;55:7.PubMedCrossRef

23.

Tossi V, Lamattina L, Cassia R. An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytol. 2009;181:871–9.PubMedCrossRef

24.

Han B, Yang Z, Xie Y, Nie L, Cui J, Shen W. Arabidopsis HY1 confers cadmium tolerance by decreasing nitric oxide production and improving iron homeostasis. Mol Plant. 2013;7:388–403.PubMedCrossRef

25.

Zhou Y, Liu H, Wang G, Huang X, Cheng Z, Chen Z, et al. Immuno-detection of Rice stripe virus carried by small brown planthopper. Jiangsu Agric Sci. 2004;1:50–1.

26.

Zhou T, Wang Y, Wu LJ, Fan Y, Zhou Y. The research on method of artificial inoculation and identification on rice resistance to rice black dwarf virus. The Chinese society of plant pathology. 2011;04.

27.

Balcerczyk A, Soszynski M, Bartosz G. On the specificity of 4-amino-5-methylamino-2′.,7′-difluorofluorescein as a probe for nitric oxide. Free Radic Biol Med. 2005;39:327–35.PubMedCrossRef

28.

Qi F, Xiang Z, Kou N, Cui W, Xu D, Wang R, et al. Nitric oxide is involved in methane-induced adventitious root formation in cucumber. Physiol Plant. 2017;159:366–77.PubMedCrossRef

29.

Fang P, Lu R, Sun F, Lan Y, Shen W, Du L, et al. Assessment of reference gene stability in rice stripe virus and Rice black streaked dwarf virus infection rice by quantitative real-time PCR. Virol J. 2015;12:175–85.PubMedPubMedCentralCrossRef

30.

Kenneth JL, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2^−ΔΔCt method. Methods. 2001;25:402–8.CrossRef

31.

Lozano-Juste J, León J. Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol. 2009;52:891–903.

32.

Sanz L, Fernándezmarcos M, Modrego A, Lewis DR, Muday GK, Pollmann S, et al. Nitric oxide plays a role in stem cell niche homeostasis through its interaction with auxin. Plant Physiol. 2014;166:1972–84.PubMedPubMedCentralCrossRef

33.

Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, et al. Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell. 2007;19:2064–76.PubMedPubMedCentralCrossRef

34.

Nahar K, Kyndt T, Vleesschauwer DD, Höfte M, Gheysen G. The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol. 2011;57:305–16.CrossRef

35.

Natarajan S, Luthria D, Bae H, Lakshman D, Mitra A. Transgenic soybeans and soybean protein analysis: an overview. J Agric Food Chem. 2013;61:11736–43.PubMedCrossRef

36.

Zhao H, Xu L, Su T, Jiang Y, Hu L, Ma F. Melatonin regulates carbohydrate metabolism and defenses against Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis thaliana. J Pineal Res. 2015;59:109.PubMedCrossRef

37.

Kantar Ş, Türközkan N, Bircan FS, Paşaoğlu ÖT. Beneficial effects of melatonin on serum nitric oxide, homocysteine, and ADMA levels in fructose-fed rats. Pharm Biol. 2015;53:1035–41.PubMedCrossRef

38.

Pozo D, Reiter R, Calvo J, Guerrero J. Physiological concentrations of melatonin inhibit nitric oxide synthase in rat cerebellum. Life Sci. 1994;55:455–60.CrossRef

39.

Aydogan S, Yerer MB, Goktas A. Melatonin and nitric oxide. J Endocrinol Investig. 2006;29:281.CrossRef

40.

Wang Q, Liu Y, He J, Zheng X, Hu J, Liu Y, et al. STV11 encodes a sulphotransferase and confers durable resistance to rice stripe virus. Nat Commun. 2014;5:4768.PubMedCrossRef

41.

Song F, Goodman RM. Activity of nitric oxide is dependent on, but is partially required for function of, salicylic acid in the signaling pathway in tobacco systemic acquired resistance. Mol Plant Microbe. 2001;14:1458–62.CrossRef

42.

Shimono M, Koga H, Akagi A, Hayashi N, Goto S, Sawada M, et al. Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol Plant Pathol. 2012;13:83.PubMedCrossRef

43.

Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, et al. WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot. 2013;64:5085.PubMedPubMedCentralCrossRef

44.

Qian Y, Tan D, Reiter R, Shi H. Comparative metabolomic analysis highlights the involvement of sugars and glycerol in melatonin-mediated innate immunity against bacterial pathogen in Arabidopsis. Sci Rep. 2015;5:15815.PubMedPubMedCentralCrossRef

Title: Melatonin is responsible for rice resistance to rice stripe virus infection through a nitric oxide-dependent pathway
Authors: Rongfei Lu
Zhiyang Liu
Yudong Shao
Feng Sun
Yali Zhang
Jin Cui
Yijun Zhou
Wenbiao Shen
Tong Zhou
Publication date: 01-12-2019
Publisher: BioMed Central
Published in: Virology Journal / Issue 1/2019
Electronic ISSN: 1743-422X
DOI: https://doi.org/10.1186/s12985-019-1228-3

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Melatonin is responsible for rice resistance to rice stripe virus infection through a nitric oxide-dependent pathway

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2019

Generation of recombinant MVA-norovirus: a comparison study of bacterial artificial chromosome- and marker-based systems

Disseminated zoster in an adult patient with extensive burns: a case report

NAD-linked mechanisms of gene de-repression and a novel role for CtBP in persistent adenovirus infection of lymphocytes

Full genome sequence analysis and putative host-shifting of Milk vetch dwarf virus infecting tobacco (Nicotiana tabacum) in China

Identification of emerging viral genomes in transcriptomic datasets of alfalfa (Medicago sativa L.)

Effectiveness of ombitasvir/paritaprevir/ritonavir, dasabuvir for HCV in HIV/HCV coinfected subjects: a comprehensive analysis

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page