Skip to main content
SpringerLink
Log in

Mycorrhiza-induced plant defence responses in trifoliate orange infected by Phytophthora parasitica

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Arbuscular mycorrhizal fungi (AMF) reduce disease incidence of host plants through the competition of carbon sources and direct inhibition of pathogens, as well as through induction of biochemical and molecular responses. However, it is not known whether AMF enhance the resistance to Phytophthora parasitica-induced root rot in citrus and what the underlying mechanisms are. This study was carried out to analyze roles of Funneliformis mosseae (a mycorrhizal fungus) in plant defence responses of Poncirus trifoliata infected by P. parasitica. A week after the pathogen infection, mycorrhizal seedlings possessed higher expression of root mitogen-activated protein kinase 3 (PtMAPK3) regardless of P. parasitica infection. F. mosseae induced higher root salicylic acid (SA) concentrations, accompanied with up-regulation of SA synthesis genes (PtPAL1 and PtEPS1), regardless of being infected with P. parasitica or not. Jasmonic acid (JA) synthesis genes were down-regulated by mycorrhization in the absence of P. parasitica and up-regulated (except for PtAOC) by mycorrhization under P. parasitica infection. Moreover, F. mosseae stimulated higher expression of pathogenesis-related protein gene 1 (PtPR1), PtPR4, and PtPR5, especially under P. parasitica infection. F. mosseae inoculation increased levels of root lignin, calmodulin, and total soluble phenol and activities of root chitinase, phenylalanine ammonialyase, and β-1,3-glucanase, and decreased concentrations of root nitric oxide with or without P. parasitica infection. These results implied that F. mosseae elicited MAPKs cascades as well as SA- and calmodulin-mediated signal pathways to activate disease-defence genes, proteins, and compounds to early-warn P. parasitica infection for enhancing tolerance of root rot in trifoliate orange.

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

Similar content being viewed by others

References

  • Aguilar E, del Toro FJ, Canto T, Tenllado F (2017) Identification of MAPKs as signal transduction components required for the cell death response during compatible infection by the synergistic pair potato virus X-potato virus Y. Virology 509:178–184

    Article  CAS  PubMed  Google Scholar 

  • Alvarez ME (2000) Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol Biol 44:429–442

    Article  CAS  PubMed  Google Scholar 

  • Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983

    Article  CAS  PubMed  Google Scholar 

  • Ballhorn DJ, Younginger BS, Kautz S (2014) An aboveground pathogen inhibits belowground rhizobia and arbuscular mycorrhizal fungi in Phaseplus vulgaris. BMC Plant Biol 14:321

    Article  PubMed  PubMed Central  Google Scholar 

  • Cahill DM, Mccomb JA (1992) A comparison of changes in phenylalanine ammonia-lyase activity, lignin and phenolic synthesis in the roots of Eucalyptus calophylla (field resistant) and E. marginata (susceptible) when infected with Phytophthora cinnamomi. Physiol Mol Plant Pathol 40:315–332

    Article  CAS  Google Scholar 

  • Chen ZZ, Wang JG, Li Y, Zhong Y, Liao LG, Lu SG, Wang L, Wang XW, Chen SY (2018) Dry mycelium of Penicillum chrysogenum activates defense via gene regulation of salicylic acid and jasmonic acid signaling in Arabidopsis. Physiol Mol Plant Pathol 103:54–61

    Article  CAS  Google Scholar 

  • Cheng S, Tian L, Zou YN, Wu QS, Kuča K, Bora P (2020) Molecular responses of arbuscular mycorrhizal fungi in tolerating root rot of trifoliate orange. Not Bot Hortic Agrobot 48:558–571

    Article  CAS  Google Scholar 

  • Dóczi R, Brader G, Pettkószandtner A, Rajh I, Djamei A, Pitzschke A, Teige M, Hirt H (2007) The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19:3266–3279

    Article  PubMed  PubMed Central  Google Scholar 

  • Du XY (2016) Progress of phenylalanine ammoniase. J Mod Agric 7:24–26 (In Chinese)

    Google Scholar 

  • Esquerré-Tugayé MT, Boudart G, Dumas B (2000) Cell wall degrading enzymes, inhibitory proteins, and oligosaccharides participate in the molecular dialogue between plants and pathogens. Plant Physiol Biochem 38:157–163

    Article  Google Scholar 

  • Farivar RS, Brecher P (1996) Salicylate is a transcriptional in hibitor of the inducible nitric oxide synthase in cultured cardiacfib rob lasts. Biol Chem 271:31585–31592

    Article  CAS  Google Scholar 

  • Ferrol N, Azcon-Aguilar C, Perez-Tienda J (2019) Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: an overview on the mechanisms involved. Plant Sci 280:441–447

    Article  CAS  Google Scholar 

  • Gao WQ, Lu LH, Srivastava AK, Wu QS, Kuča K (2020) Effects of mycorrhizae on physiological responses and relevant gene expression of peach affected by replant disease. Agronomy 10:186

    Article  CAS  Google Scholar 

  • Giovannetti M, Tosi L, Torre GD (1991) Histological, physiological and biochemical interactions between vesicular-arbuscular mycorrhizae and Thielaviopsis basicola in tobacco plants. J Phytopathol 131:265–274

    Article  CAS  Google Scholar 

  • He JD, Chi GG, Zou YN, Shu B, Wu QS, Srivastava AK, Kuča K (2020a) Contribution of glomalin-related soil proteins to soil organic carbon in trifoliate orange. Appl Soil Ecol 154:103592

    Article  Google Scholar 

  • He JD, Zou YN, Wu QS, Kuča K (2020b) Mycorrhizas enhance drought tolerance of trifoliate orange by enhancing activities and gene expression of antioxidant enzymes. Sci Hortic 262:108745

    Article  CAS  Google Scholar 

  • Hu N, Tu XR, Li KT, Ding H, Li H, Zhang HW, Tu GQ, Huang L (2017) Changes in protein content and chitinase and β-1,3-glucanase activities of rice with blast resistance induced by Ag-antibiotic 702. Plant Dis Pests 8:33–36

    Google Scholar 

  • Huang YM, Srivastava AK, Zou YN, Ni QD, Han Y, Wu QS (2014) Mycorrhizal-induced calmodulin mediated changes in antioxidant enzymes and growth response of drought-stressed trifoliate orange. Front Microbiol 5:682–688

    Article  PubMed  PubMed Central  Google Scholar 

  • Jongedijk E, Tigelaar H, van Roekel JSC, Bres-Vloemans SA, Dekker I, van den Elzen PJM, Cornelissen BJC, Melchers LS (1995) Synergistic activity of chitinases and β-1,3-glucanases enhances fungal resistance in transgenic tomato plants. Euphytica 85:173–180

    Article  CAS  Google Scholar 

  • Kenneth JL, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and 2−ΔΔCt method. Methods 25:402–408

    Article  Google Scholar 

  • Kim DS, Hwang BK (2014) An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. J Exp Bot 65:2295–2306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kofalvi SA, Nassuth A (1995) Influence of wheat streak mosaic virus infection on phenylpropanoid metabolism and the accumulation of phenolics and lignin in wheat. Physiol Mol Plant Pathol 47:365–377

    Article  CAS  Google Scholar 

  • Lahlali R, McGregor L, Song T, Gossen BD, Narisawa K, Peng G (2014) Heteroconium chaetospira induces resistance to clubroot via upregulation of host genes involved in jasmonic acid, ethylene, and auxin biosynthesis. PLoS ONE 9:e94144

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Liu QP, Tang YM, Ding W (2019) NtPR1a regulates resistance to Ralstonia solanacearum in Nicotiana tabacum via activating the defense-related genes. Biochem Biophys Res Commun 508:940–945

    Article  CAS  PubMed  Google Scholar 

  • Mehari ZH, Elad Y, Rav-David D, Graber ER, Harel YM (2015) Induced systemic resistance in tomato (Solanum lycopersicum) against Botrytis cinerea by biochae amendment involves jasmonic acid signaling. Plant Soil 395:31–44

    Article  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 

  • Monteiro S, Barakat M, Piçarra-Pereira MA, Teixeira AR, Ferreira RB (2003) Osmotin and thaumatin from grape: a putative general defense mechanism against pathogenic fungi. Phytopathology 93:1505–1512

    Article  CAS  PubMed  Google Scholar 

  • Nagai A, Torres PB, Duarte LML, Chaves ALR, Macedo AF, Floh ELS, de Oliveira LF, Zuccarelli R, dos Santos DYAC (2020) Signaling pathway played by salicylic acid, gentisic acid, nitric oxide, polyamines and non-enzymatic antioxidants in compatible and incompatible Solanum-tomato mottle mosaic virus interactions. Plant Sci 290:110274

    Article  CAS  PubMed  Google Scholar 

  • O’Connell RJ, Panstruga R (2006) Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 171:699–718

    Article  PubMed  Google Scholar 

  • Park JY, Jin J, Lee YW, Kang S, Lee YH (2009) Rice blast fungus (Magnaporthe oryzae) infects Arabidopsis via a mechanism distinct from that required for the infection of rice. Plant Physiol 149:474–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421–426

    Article  CAS  PubMed  Google Scholar 

  • Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343

    Article  CAS  PubMed  Google Scholar 

  • Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW, Goldberg RB (2000) The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12:1041–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarfir GE (1968) The infiuence of vesicular arbuscular mycorrhiza on the resistance of onion to Phyrenochacta terreation. Thesis for M.S., University of Illinois, Urbaba

  • Slezack S, Dumas-Gaudot E, Rosendahl S, Kjoller R, Paynot MJ, Gianinazzi S (1999) Endoproteolytic activities in pea roots inoculated with the arbuscular mycorrhizal fungus Glomus mosseae and/or Aphanomyces euteiches in relation to bioprotection. New Phytol 142:517–529

    Article  Google Scholar 

  • Vos CM, Yang Y, De Cininck B, Cammue BPA (2014) Fungal (-like) biocontrol organisms in tomato disease control. Biol Control 74:65–81

    Article  Google Scholar 

  • Wang Y, Li J, Hou S, Wang X, Li Y, Ren D, Chen S, Tang X, Zhou JM (2010) A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22:2033–2044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu QS, He JD, Srivastava AK, Zou YN, Kuča K (2019) Mycorrhizas enhance drought tolerance of citrus by altering root fatty acid compositions and their saturation levels. Tree Physiol 39:1149–1158

    Article  CAS  Google Scholar 

  • Xie MM, Zhang YC, Liu LP, Zou YN, Wu QS, Kuča K (2019) Mycorrhiza regulates signal substance levels and pathogen defense gene expression to resist citrus canker. Not Bot Hortic Agrobot 47:1161–1167

    Article  CAS  Google Scholar 

  • Xie MM, Zou YN, Wu QS, Zhang ZZ, Kuča K (2020) Single or dual inoculation of arbuscular mycorrhizal fungi and rhizobia regulates plant growth and nitrogen acquisition in white clover. Plant Soil Environ 66:287–294

    Article  CAS  Google Scholar 

  • Yang L, Zou YN, Tian ZH, Wu QS, Kuča K (2021) Effects of beneficial endophytic fungal inoculants on plant growth and nutrient absorption of trifoliate orange seedlings. Sci Hortic 277:109815

    Article  CAS  Google Scholar 

  • Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13:1527–1540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang RQ, Zhu HH, Zhao HQ, Yao Q (2013) Arbuscular mycorrhizal fungi inoculation increases phenolic synthesis in clover roots via hydrogen peroxide salicylic acid and nitric oxide signaling pathways. J Plant Physiol 170:74–79

    Article  CAS  PubMed  Google Scholar 

  • Zhang YC, Liu CY, Wu QS (2017) Mycorrhiza and common mycorrhizal network regulate the production of signal substances in trifoliate orange (Poncirus trifoliata). Not Bot Hortic Agrobot 45:43–49

    Article  Google Scholar 

  • Zhang YC, Zou YN, Liu LP, Wu QS (2019) Common mycorrhizal networks activate salicylic acid defense responses of trifoliate orange (Poncirus trifoliata). J Integr Plant Biol 61:1099–1111

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Zou YN, Wu QS, Kuča K (2020) Arbuscular mycorrhizas modulate root polyamine metabolism to enhance drought tolerance of trifoliate orange. Environ Exp Bot 171:103962

    Article  Google Scholar 

  • Zhu WS, Lan XY, Chen H, Su YC, Shen CR (1993) Study on citrus root rot. Acta Phytopathol Sin 2:7–8 (In Chinese with English abstract)

    Google Scholar 

  • Zou YN, Zhang F, Srivastava AK, Wu QS, Kuča K (2021) Arbuscular mycorrhizal fungi regulate polyamine homeostasis in roots of trifoliate orange for improved adaptation to soil moisture deficit stress. Front Plant Sci 11:600792

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by the Hubei Provincial Department of Education (T201604).

Author information

Authors and Affiliations

  1. College of Horticulture and Gardening, Yangtze University, Jingzhou, 434025, Hubei, China

    Li Tian, Ying-Ning Zou & Qiang-Sheng Wu

  2. Department of Chemistry, Faculty of Science, University of Hradec Kralove, Hradec Kralove, 50003, Czech Republic

    Qiang-Sheng Wu & Kamil Kuča

Authors
  1. Li Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ying-Ning Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qiang-Sheng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kamil Kuča
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qiang-Sheng Wu.

Additional information

Communicated by E. Kuzniak-Gebarowska.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tian, L., Zou, YN., Wu, QS. et al. Mycorrhiza-induced plant defence responses in trifoliate orange infected by Phytophthora parasitica. Acta Physiol Plant 43, 45 (2021). https://doi.org/10.1007/s11738-021-03216-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-021-03216-2

Keywords

Search

Navigation