Skip to main content
Log in

Thiamine induces resistance in tobacco against black shank

  • Original Research Article
  • Published:
Australasian Plant Pathology Aims and scope Submit manuscript

Abstract

Induced resistance by elicitors is considered to be an eco-friendly strategy to stimulate plant defence against pathogen attack. Thiamine (vitamin B1, VB1) can act as a plant defence trigger or priming agent, leading to a rapid counterattack on pathogen invasion, but the underlying molecular mechanisms have not yet been fully elucidated. In the present study, the priming effect of thiamine on tobacco against the disease Phytophthora nicotianae and its biochemical and molecular impact on plant defence mechanisms, as well as the in vitro inhibitory effect of thiamine on P. nicotianae, were evaluated. The results showed that the mycelial growth and sporangium production of P. nicotianae were inhibited by thiamine in a dose-dependent manner. After thiamine pretreatment, the resistance of tobacco plants to P. nicotianae was enhanced, and the severity of tobacco related disease was significantly reduced. In tobacco plants stimulated by thiamine, H2O2 accumulation and catalase (CAT) and peroxidase (POD) and phenylalanine ammonia lyase (PAL) activity levels were enhanced, and seven defence-related genes were upregulated in the plant leaves in order to avoid anthropomorphising plant responses to pathogen attack. Overall, this study demonstrates that thiamine effectively induces resistance against P. nicotianae in tobacco under greenhouse-controlled conditions through a dual mode of action involving direct antifungal activity and induction of host defence mechanisms. It is suggested that thiamine may be an attractive alternative to chemical fungicides in tobacco plant disease management.

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

References

  • Aguiar TR, Bortolozo FR, Filho EF, Parron LM, Luz LD, Brito AG, Ferreira MT (2017) Fate of selected agrochemicals in a tropical karst aquifer: A five-year study. Groundw Sustain Dev 5:187–192

    Article  Google Scholar 

  • Ahn IP, Kim S, Lee YH (2005) Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol 138(3):1505–1515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahn IP, Kim S, Lee YH, Suh SC (2007) Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiol 143(2):838–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asensi-Fabado MA, Munné-Bosch S (2010) Vitamins in plants: occurrence, biosynthesis and antioxidant function. Trends Plant Sci 15(10):582–592

    Article  CAS  PubMed  Google Scholar 

  • Aćimović SG, Zeng Q, McGhee GC, Sundin GW, Wise JC (2015) Control of fire blight (Erwinia amylovora) on apple trees with trunk-injected plant resistance inducers and antibiotics and assessment of induction of athogenesis-related protein genes. Front Plant Sci 6:16

    PubMed  PubMed Central  Google Scholar 

  • Bahuguna RN, Joshi R, Shukla A, Pandey M, Kumar J (2012) Thiamine primed defense provides reliable alternative to systemic fungicide carbendazim against sheath blight disease in rice (Oryza sativa L.). Plant Physiol Biochem 57:159-167

  • Balmer A, Pastor V, Gamir J, Flors V, Mauch-Mani B (2015) The “prime-ome”: towards a holistic approach to priming. Trends Plant Sci 20(7):443–452

    Article  CAS  PubMed  Google Scholar 

  • Barilli E, Sillero JC, Rubiales D (2010) Induction of systemic acquired resistance in pea against rust (Uromyces pisi) by exogenous application of biotic and abiotic inducers. J Phytopathol 158(1):30–34

    Article  CAS  Google Scholar 

  • Bastas KK (2014) Importance of reactive oxygen species in plants-pathogens interactions. Selcuk J Agric Food Sci 28(1):11–21

    Google Scholar 

  • Burrows RJ, Byrne KL, Meacock PA (2000) Isolation and characterization of Saccharomyces cerevisiae mutants with derepressed thiamine gene expression. Yeast (chichester, England) 16(16):1497–1508

    Article  CAS  Google Scholar 

  • Blainski A, Lopes GC, de Mello JC (2013) Application and analysis of the folin ciocalteu method for the determination of the total phenolic content from Limonium brasiliense L. Molecules 18(6):6852–6865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boubakri H, Wahab MA, Chong J, Bertsch C, Mliki A, Soustre-Gacougnolle I (2012) Thiamine induced resistance to Plasmopara viticola in grapevine and elicited host-defense responses, including HR like-cell death. Plant Physiol Biochem 57:120–133

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: Roles in stress, senescence and signal transducation in plants. Curr Sci 89:1113–1121

    CAS  Google Scholar 

  • Bigeard J, Colcombet J, Hirt H (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8(4):521–539

    Article  CAS  PubMed  Google Scholar 

  • Bittel P, Robatzek S (2007) Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr Opin Plant Biol 10(4):335–341

    Article  CAS  PubMed  Google Scholar 

  • Csinos AS (1999) Stem and Root Resistance to Tobacco Black Shank. Plant Dis 83(8):777–780

    Article  CAS  PubMed  Google Scholar 

  • Conrath U, Beckers GJ, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CM, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Molec Plant-Microbe Interact: MPMI 19(10):1062–1071

    Article  CAS  PubMed  Google Scholar 

  • Conrath U, Pieterse CM, Mauch-Mani B (2002) Priming in plant-pathogen interactions. Trends Plant Sci 7(5):210–216

    Article  CAS  PubMed  Google Scholar 

  • Chen N, Goodwin PH, Hsiang T (2003) The role of ethylene during the infection of Nicotiana tabacum by Colletotrichum destructivum. J Exp Bot 54(392):2449–2456

    Article  CAS  PubMed  Google Scholar 

  • Dempsey DA, Shah J, Klessig DF (1997) Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18(4):547–575

    Article  Google Scholar 

  • De Kesel J, Conrath U, Flors V, Luna E, Mageroy MH, Mauch-Mani B, Pastor V, Pozo MJ, Pieterse C, Ton J, Kyndt T (2021) The Induced Resistance Lexicon: Do’s and Don’ts. Trends Plant Sci 26(7):685–691

    Article  PubMed  Google Scholar 

  • Dalio RJ, Fleischmann F, Humez M, Osswald W (2014) Phosphite protects Fagus sylvatica seedlings towards Phytophthora plurivora via local toxicity, priming and facilitation of pathogen recognition. PloS One 9(1):e87860

  • Deenamo N, Kuyyogsuy A, Khompatara K, Chanwun T, Ekchaweng K, Churngchow N (2018) Salicylic Acid Induces Resistance in Rubber Tree against Phytophthora palmivora. Int J Mol Sci 19(7):1883

  • Drzewiecka K, Borowiak K, Bandurska H, Golinski P (2012) Salicylic acid-a potential biomarker of tobacco Bel-W3 cell death developed as a response to ground level ozone under ambient conditions. Acta Biol Hung 63(2):231–249

    Article  CAS  PubMed  Google Scholar 

  • De Gara L, de Pinto MC, Tommasi F (2003) The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol Biochem 41(10):863–870

    Article  Google Scholar 

  • Frąckowiak P, Pospieszny H, Smiglak M, Obrępalska-Stęplowska A (2019) Assessment of the Efficacy and Mode of Action of Benzo(1,2,3)-Thiadiazole-7-Carbothioic Acid S-Methyl Ester (BTH) and Its Derivatives in Plant Protection Against Viral Disease. Int J Mol Sci 20(7):1598

  • Gallup CA, McCorkle KL, Ivors KL, Shew D (2018) Characterization of the Black Shank Pathogen, Phytophthora nicotianae, Across North Carolina Tobacco Production Areas. Plant Dis 102(6):1108–1114

    Article  CAS  PubMed  Google Scholar 

  • Guo W, Yan H, Ren X, Tang R, Sun Y, Wang Y, Feng J (2020) Berberine induces resistance against tobacco mosaic virus in tobacco. Pest Manag Sci 76(5):1804–1813

    Article  CAS  PubMed  Google Scholar 

  • Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3(4):307–319

    Article  CAS  PubMed  Google Scholar 

  • Huang WK, Ji HL, Gheysen G, Kyndt T (2016) Thiamine-induced priming against root-knot nematode infection in rice involves lignification and hydrogen peroxide generation. Mol Plant Pathol 17(4):614–624

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Ma L, Fang DH, Xi JQ, Zhu ML, Mo MH, Zhang KQ, Ji YP (2015) Isolation and characterisation of rhizosphere bacteria active against Meloidogyne incognita, Phytophthora nicotianae and the root knot-black shank complex in tobacco. Pest Manag Sci 71(3):415–422

    Article  CAS  PubMed  Google Scholar 

  • Hong JK, Kim HJ, Jung H, Yang HJ, Kim DH, Sung CH, Park CJ, Chang SW (2016) Differential Control Efficacies of Vitamin Treatments against Bacterial Wilt and Grey Mould Diseases in Tomato Plants. Plant Pathol J 32(5):469–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson AO, Taylor CB (1996) Plant-microbe interactions: life and death at the interface. Plant Cell 8(10):1651–1668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung IL, Kim IG (2003) Thiamine protects against paraquat-induced damage: scavenging activity of reactive oxygen species. Environ Toxicol Pharmacol 15(1):19–26

    Article  CAS  PubMed  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5(4):325–331

    Article  CAS  PubMed  Google Scholar 

  • Kolahi M, Jonoubi P, Majd A, Tabandeh MR, Hashemitabar M (2013) Differential expression of phenylalanine ammonia-lyase in different tissues of sugarcane (Saccharum officinarum L.) during development. Bioresources 8(4):4912–4922

  • Lerat S, Babana AH, El Oirdi M, El Hadrami A, Daayf F, Beaudoin N, Bouarab K, Beaulieu C (2009) Streptomyces scabiei and its toxin thaxtomin A induce scopoletin biosynthesis in tobacco and Arabidopsis thaliana. Plant Cell Rep 28(12):1895–1903

    Article  CAS  PubMed  Google Scholar 

  • Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant 24(2):183–193

    CAS  Google Scholar 

  • Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–266

    Article  CAS  PubMed  Google Scholar 

  • Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense Priming: An Adaptive Part of Induced Resistance. Annu Rev Plant Biol 68:485–512

    Article  CAS  PubMed  Google Scholar 

  • Malamy J, Sanchez-Casas P, Hennig J, Guo A, Klessig DF (1996) Dissection of the salicylic acid signaling pathway in tobacco. Mole Plant-Microbe Interact: MPMI (USA) 9:474–482

    Article  CAS  Google Scholar 

  • Moreira-Vilar FC, Siqueira-Soares Rde C, Finger-Teixeira A et al (2014) The acetyl bromide method is faster, simpler and presents best recovery of lignin in different herbaceous tissues than Klason and thioglycolic acid methods. PLoS One 9(10):e110000

  • Mach J (2015) Phosphorylation and Nuclear Localization of NPR1 in Systemic Acquired Resistance. Plant Cell 27(12):3291

    Article  CAS  PubMed  Google Scholar 

  • Pauwels L, Morreel K, De Witte E, Lammertyn F, Van Montagu M, Boerjan W, Inzé D, Goossens A (2008) Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc Natl Acad Sci USA 105(4):1380–1385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic Acquired Resistance Plant Cell 8(10):1809

    CAS  PubMed  Google Scholar 

  • Sullivan MJ, Melton TA, Shew HD (2005) Fitness of Races 0 and 1 of Phytophthora parasitica var. nicotianae. Plant Dis 89(11):1220–1228

  • Thomma BP, Eggermont K, Penninckx IA, Mauch-Mani B, Vogelsang R, Cammue BP, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci 95(25):15107–15111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vontimitta V, Lewis RS (2012) Mapping of quantitative trait loci affecting resistance to Phytophthora nicotianae in tobacco (Nicotiana tabacum L.) line Beinhart-1000. Mol Breed 29(1):89–98

  • Van Hulten M, Pelser M, van Loon LC, Pieterse CM, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103(14):5602–5607

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang K, Liao Y, Kan J, Han L, Zheng Y (2015) Response of direct or priming defense against Botrytis cinerea to methyl jasmonate treatment at different concentrations in grape berries. Int J Food Microbiol 194:32–39

    Article  CAS  PubMed  Google Scholar 

  • Wen D, Li C, Di H, Liao Y, Liu H (2005) A universal HPLC method for the determination of phenolic acids in compound herbal medicines. J Agric Food Chem 53(17):6624–6629

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson SW, Magerøy MH, López Sánchez A, Smith LM, Furci L, Cotton T, Krokene P,  Ton J (2019) Surviving in a Hostile World: Plant Strategies to Resist Pests and Diseases. Annual review of phytopathology 57:505–529

  • Wu G, Shortt BJ, Lawrence EB, Leon J, Fitzsimmons KC, Levine EB, Raskin I, Shah DM (1997) Activation of Host Defense Mechanisms by Elevated Production of H2O2 in Transgenic Plants. Plant Physiol 115(2):427–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322(Pt 3):681–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu C, Zeng LZ, Sheng K, Chen FX, Zhou T, Zheng XD, Yu T (2014) γ-Aminobutyric acid induces resistance against Penicillium expansum by priming of defence responses in pear fruit. Food Chem 159:29–37

    Article  CAS  PubMed  Google Scholar 

  • Yang G, Tang L, Gong Y, Xie J, Fu Y, Jiang D, Li G, Collinge DB, Chen W, Cheng J (2018) A cerato-platanin protein SsCP1 targets plant PR1 and contributes to virulence of Sclerotinia sclerotiorum. New Phytol 217(2):739–755

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Liu S, Zhang J, Reiter R, Wang Y, Qiu D, Luo X, Khalid A, Wang H, Feng L, Lin Z, Ren M (2018) Synergistic anti-oomycete effect of melatonin with a biofungicide against oomycetic black shank disease. J Pineal Res 65(2):e12492

  • Zhang C, Feng C, Zheng Y, Wang J, Wang F (2020) Root Exudates Metabolic Profiling Suggests Distinct Defense Mechanisms Between Resistant and Susceptible Tobacco Cultivars Against Black Shank Disease. Front Plant Sci 11:559775

Download references

Acknowledgements

This work was supported by Yunnan Tobacco Company Science and Technology Plan Project (Number: 2020530000242026).

Author information

Authors and Affiliations

Authors

Contributions

Tao Liu and Jun Liu conceived and designed the experiments. Tian Suohui and Chen Yanping performed the experiments. Zi Shuhui and Li Zhihua analysed the data. Jin Honggang revised the paper. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Tian Suohui or Liu Tao.

Ethics declarations

Conflicts of interest

The authors declare no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suohui, T., Yanping, C., Shuhui, Z. et al. Thiamine induces resistance in tobacco against black shank. Australasian Plant Pathol. 51, 231–243 (2022). https://doi.org/10.1007/s13313-021-00848-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13313-021-00848-3

Keywords

Navigation