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Efficacy of Althaea officinalis leaf extract in controlling Alternaria spp. pathogenic on Citrus

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Abstract

In this study, inhibitory effects of the aqueous and ethanolic leaf extracts obtained from marshmallow (A. officinalis) were evaluated against Alternaria spp., pathogenic on Citrus. The marshmallow leaf extracts were added to potato dextrose agar medium at various concentrations and antifungal effect of the extracts against three species of Alternaria pathogenic on citrus was tested in vitro and in vivo. The ethanolic leaf extract revealed significant inhibitory effect on the mycelial growth of all fungal species and complete inhibition on spore germination of the pathogens at 100 mg mL−1 concentration, similar to those of the fungicide tested. Microscopic analysis revealed that the extract caused morphological changes, including abnormal hyphal morphology with a rough surface and shriveled hyphae. The HPLC analysis revealed the presence of phenolic/flavonoid compounds, including chlorogenic acid, quercetin, benzoic acid, apegenin, cinnamic acid, ferulic acid and Kaempferol. Results of enzyme activity assays revealed that the activity of cellulase, amylase, protease and pectinase reduced in the samples treated with the ethanolic extract. The ethanolic leaf extract protected Citrus sinensis (orange) fruits against the pathogens and reduced lesion diameter of Alternaria disease in a concentration dependent manner. The concentrations of 50 and 100 mg mL−1 were the most effective in reducing lesion diameters on citrus fruits campared to the control. Both in vitro and in vivo assays revealed potential of marshmallow ethanolic leaf extract to be used as a safe and eco-friendly protectant of citrus fruits against Alternaria spp. as destructive pre- and post-harvest fungal parhogens. Future research seems to be necessary to investigate antifungal effect of the major components detected in marshmallow leaf extract and determine the best formulation to increase its efficiency against phytopathogens.

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References

  • Abd-El-Khair, H., & El-Gamal, N. G. (2011). Effects of aqueous extracts of some plant species against fusarium solani and Rhizoctonia solani in Phaseolus vulgaris plants. Archives of Phytopathology and Plant Protection, 44(1), 1–16.

    Article  Google Scholar 

  • Abdelkhalek, A., Salem, M. Z., Kordy, A. M., Salem, A. Z., & Behiry, S. I. (2020). Antiviral, antifungal, and insecticidal activities of Eucalyptus bark extract: HPLC analysis of polyphenolic compounds. Microbial Pathogenesis, 147, 104383.

    Article  CAS  Google Scholar 

  • Abdel-Razik, A. A. (1970). The parasitism of white Sclerotium cepivorum Berk, the incitant of white rot of onion. Doctoral thesis: Univ, Fac Agric, Assiut.

    Google Scholar 

  • Akimitsu, K., Peever, T. L., & Timmer, L. W. (2003). Molecular, ecological and evolutionary approaches to understanding Alternaria diseases of citrus. Molecular Plant Pathology, 4(6), 435–446.

    Article  CAS  Google Scholar 

  • Ali, M., Haroon, U., Khizar, M., Chaudhary, H. J., & Munis, M. F. H. (2020). Facile single step preparations of phyto-nanoparticles of iron in Calotropis procera leaf extract to evaluate their antifungal potential against Alternaria alternata. Curr Plant Biol, 100157.

  • Aminnezhad, S., Kermanshahi, R. K., & Ranjbar, R. (2016). Effect of Althaea officinalis extract on growth and biofilm formation in Pseudomonas aeruginosa. J Pure Appl Microbiol, 10(3), 1857–1863.

    CAS  Google Scholar 

  • Armitage, A. D., Barbara, D. J., Harrison, R. J., Lane, C. R., Sreenivasaprasad, S., Woodhall, J. W., & Clarkson, J. P. (2015). Discrete lineages within Alternaria alternata species group: Identification using new highly variable loci and support from morphological characters. Fungal Biology, 119(11), 994–1006.

    Article  Google Scholar 

  • Bianchi, A., Zambonelli, A., D'Aulerio, A. Z., & Bellesia, F. (1997). Ultrastructural studies of the effects of Allium sativum on phytopathogenic fungi in vitro. Plant Disease, 81(11), 1241–1246.

    Article  CAS  Google Scholar 

  • Carvalho, D. D. C., Alves, E., Camargos, R. B., Oliveira, D. F., Scolforo, J. R. S., de Carvalho, D. A., & Batista, T. R. S. (2011). Plant extracts to control Alternaria alternata in Murcott tangor fruits. Revista Iberoamericana de Micología, 28(4), 173–178.

    Article  Google Scholar 

  • Chen, Q., Xu, S., Wu, T., Guo, J., Sha, S., Zheng, X., & Yu, T. (2014). Effect of citronella essential oil on the inhibition of postharvest Alternaria alternata in cherry tomato. Journal of the Science of Food and Agriculture, 94(12), 2441–2447.

    Article  CAS  Google Scholar 

  • De Lima, C. B., Rentschler, L. L. A., Bueno, J. T., & Boaventura, A. C. (2016). Plant extracts and essential oils on the control of Alternaria alternata, Alternaria dauci and on the germination and emergence of carrot seeds (Daucus carota L.). Ciência Rural, 46(5), 764–770.

    Article  Google Scholar 

  • Feng, W., & Zheng, X. (2006). Control of Alternaria alternata by cassia oil in combination with potassium chloride or sodium chloride. J Appl Microbiol, 101(6), 1317–1322 q1.

    Article  CAS  Google Scholar 

  • Feng, W., & Zheng, X. (2007). Essential oils to control Alternaria alternata in vitro and in vivo. Food Control, 18(9), 1126–1130.

    Article  CAS  Google Scholar 

  • Garganese, F., Schena, L., Siciliano, I., Prigigallo, M. I., Spadaro, D., De Grassi, A., & Sanzani, S. M. (2016). Characterization of citrus-associated Alternaria species in mediterranean areas. PLoS One, 11(9), e0163255.

    Article  Google Scholar 

  • Gautam, S. S., Navneet, S. K., & Chauhan, R. (2015). Antimicrobial efficacy of Althaea officinalis Linn seed extracts and essential oil against respiratory tract pathogens. J Appl Pharm Sci, 5(9), 115–119.

    Article  CAS  Google Scholar 

  • Haghgoo, R., Mehran, M., Afshari, E., Zadeh, H. F., & Ahmadvand, M. (2017). Antibacterial effects of different concentrations of Althaea officinalis root extract versus 02% chlorhexidine and penicillin on Streptococcus mutans and Lactobacillus in vitro. J Int Soc Prev Community Dent, 7(4), 180–185.

    PubMed  PubMed Central  Google Scholar 

  • Hamad, Y. K., Abobakr, Y., Salem, M. Z., Ali, H. M., Al-Sarar, A. S., & Al-Zabib, A. A. (2019). Activity of plant extracts/essential oils against three plant pathogenic fungi and mosquito larvae: GC/MS analysis of bioactive compounds. BioResources, 14(2), 4489–4511.

    Article  CAS  Google Scholar 

  • Kadhum H H, Abd A H, Al-Shammari A M, 2019. HPLC analysis and chemical composition identification of isolated flavonoid fraction of Althaea officinalis from Iraq In AIP. Conf on Proceedings, AIP Publishing LLC, Vol 2123, No 1, Jul 17, p 020045.

  • Khaledi, N., Taheri, P., & Tarighi, S. (2015). Antifungal activity of various essential oils against Rhizoctonia solani and Macrophomina phaseolina as major bean pathogens. Journal of Applied Microbiology, 118(3), 704–717.

    Article  CAS  Google Scholar 

  • Korbekandi, H., Asghari, G., Chitsazi, M. R., Bahri Najafi, R., Badii, A., & Iravani, S. (2016). Green biosynthesis of silver nanoparticles using Althaea officinalis radix hydroalcoholic extract. Artif Cells Nanomed Biotechnol, 44(1), 209–215.

    Article  CAS  Google Scholar 

  • Latha, P., Anand, T., Ragupathi, N., Prakasam, V., & Samiyappan, R. (2009). Antimicrobial activity of plant extracts and induction of systemic resistance in tomato plants by mixtures of PGPR strains and Zimmu leaf extract against Alternaria solani. Biological Control, 50(2), 85–93.

    Article  Google Scholar 

  • Lynd, L. R., Weimer, P. J., van Zyl, W. H., & Pretorius, I. S. (2002a). Microbial cellulose utilization: fundamentals and biotechnology. Micro Mol Biol Rev, 66, 506–577.

    Article  CAS  Google Scholar 

  • Lynd, L. R., Weimer, P. J., Van Zyl, W. H., & Pretorius, I. S. (2002b). Microbial cellulose utilization fundamentals and biotechnology. Microbiology and Molecular Biology Reviews, 66(3), 506–577.

    Article  CAS  Google Scholar 

  • Ma, H., Zhang, B., Gai, Y., Sun, X., Chung, K.-R., & Li, H. (2019b). Cell-wall-degrading enzymes required for virulence in the host selective toxin-producing necrotroph Alternaria alternata of citrus. Frontiers in Microbiology, 10, 2514.

    Article  Google Scholar 

  • Ma, Y. N., Xu, F. R., Chen, C. J., Li, Q. Q., Wang, M. Z., Cheng, Y. X., & Dong, X. (2019a). The beneficial use of essential oils from buds and fruit of Syzygium aromaticum to combat pathogenic fungi of Panax notoginseng. Industrial Crops and Products, 133, 185–192.

    Article  CAS  Google Scholar 

  • Martelli, I. B., de Andrade, P. C., Bastianel, M., Schinor, E. H., da Conceição, P. M., & de Azevedo, F. A. (2016). Diagrammatic scale for assessing foliar symptoms of Alternaria brown spot in citrus. Agro Sci Bio, 2(2), 57–57.

    Article  Google Scholar 

  • Mehreen A, Waheed M, Liaqat I, Arshad N, 2016. Phytochemical, antimicrobial, and toxicological evaluation of traditional herbs used to treat sore throat. Biomed Res Int

  • Mugao L G, Muturi P W, Gichimu B M, Njoroge E K, 2020. In vitro control of Phytophthora infestans and Alternaria solani using crude extracts and essential oils from selected plants. Int. J. Agron.

  • Muhsin, T. M., Al-Zubaidy, S. R., & Ali, E. T. (2001). Effect of garlic bulb extract on the growth and enzymatic activities of rhizosphere and rhizoplane fungi. Mycopathologia, 152(3), 143–146.

    Article  CAS  Google Scholar 

  • Muto, M., Mulabagal, V., Huang, H. C., Takahashi, H., Tsay, H. S., & Huang, J. W. (2006). Toxicity of black nightshade Solanum nigrum extracts on Alternaria brassicicola, causal agent of black leaf spot of Chinese cabbage Brassica pekinensis. Journal of Phytopathology, 154(1), 45–50.

    Article  Google Scholar 

  • Ozturk, S., & Ercisli, S. (2007). Antibacterial activity of aqueous and methanol extracts of Althaea officinalis and Althaea cannabina from Turkey. Pharmaceutical Biology, 45(3), 235–240.

    Article  Google Scholar 

  • Peever, T. L., Su, G., Carpenter-Boggs, L., & Timmer, L. W. (2004). Molecular systematics of citrus-associated Alternaria species. Mycologia, 96(1), 119–134.

    Article  CAS  Google Scholar 

  • Perina, F. J., Belan, L. L., Moreira, S. I., Nery, E. M., Alves, E., & Pozza, E. A. (2019). Diagrammatic scale for assessment of Alternaria brown spot severity on tangerine leaves. Journal of Plant Pathology, 101(4), 981–990.

    Article  Google Scholar 

  • Romeo, F. V., Ballistreri, G., Fabroni, S., Pangallo, S., Nicosia, M. G. L. D., Schena, L., & Rapisarda, P. (2015). Chemical characterization of different sumac and pomegranate extracts effective against Botrytis cinerea rots. Molecules, 20(7), 11941–11958.

    Article  CAS  Google Scholar 

  • Scavo, A., Pandino, G., Restuccia, C., Parafati, L., Cirvilleri, G., & Mauromicale, G. (2019). Antimicrobial activity of cultivated cardoon Cynara cardunculus L var. altilis DC leaf extracts against bacterial species of agricultural and food interest. Industrial Crops and Products, 129, 206–211.

    Article  CAS  Google Scholar 

  • Sunitha, V. H., Nirmala Devi, D., & Srinivas, C. (2013). Extracellular enzymatic activity of endophytic fungal strains isolated from medicinal plants. World J Agric Sci, 9(1), 1–9.

    CAS  Google Scholar 

  • Tian, J., Ban, X., Zeng, H., He, J., Huang, B., & Wang, Y. (2011). Chemical composition and antifungal activity of essential oil from Cicuta virosa L var latisecta Celak. International Journal of Food Microbiology, 145(2–3), 464–470.

    Article  CAS  Google Scholar 

  • Timmer, L. W., Peever, T. L., Solel, Z. V. I., & Akimitsu, K. (2003). Alternaria diseases of citrus–novel pathosystems. Phytopathologia Mediterranea, 42(2), 99–112.

    Google Scholar 

  • Vega, B., & Dewdney, M. M. (2014). QoI-resistance stability in relation to pathogenic and saprophytic fitness components of Alternaria alternata from citrus. Plant Disease, 98(10), 1371–1378.

    Article  CAS  Google Scholar 

  • Vicent, A., Armengol, J., & Garcia-Jimenez, J. (2007). Rain fastness and persistence of fungicides for control of Alternaria brown spot of citrus. Plant Disease, 91(4), 393–399.

    Article  CAS  Google Scholar 

  • Wei, X., Zheng, K., Chen, M., Liu, G., Li, J., Lei, Y., & Qu, Y. (2011). Transcription analysis of lignocellulolytic enzymes of Penicillium decumbens 114-2 and its catabolite-repression-resistant mutant. Comptes Rendus Biologies, 334(11), 806–811.

    Article  CAS  Google Scholar 

  • Wery, N., Gerike, U., Sharman, A., Chaudhuri, J. B., Hough, D. W., & Danson, M. J. (2003). Use of a packed-column bioreactor for isolation of diverse protease-producing bacteria from antarctic soil. Applied and Environmental Microbiology, 69(3), 1457–1464.

    Article  Google Scholar 

  • Wood, T. M., & Bhat, K. M. (1988). Methods for measuring cellulase activities. Methods in Enzymology, 160, 87–112.

    Article  CAS  Google Scholar 

  • Zorzi Tomazoni, E., Ribeiro, R. T., Pauletti, G. F., Soares, G. L., & Schwambach, J. (2019). Inhibition of Alternaria stem canker on tomato by essential oils from Baccharis species. Journal of Environmental Science and Health. Part. B, 54(9), 781–790.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Ferdowsi University of Mashhad, Iran, for financial support of this research with project number 3/45524 approved on 26th Dec 2017.

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  1. Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

    Fatemeh Maghsoodi & Parissa Taheri

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  1. Fatemeh Maghsoodi
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Correspondence to Parissa Taheri.

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Maghsoodi, F., Taheri, P. Efficacy of Althaea officinalis leaf extract in controlling Alternaria spp. pathogenic on Citrus. Eur J Plant Pathol 161, 799–813 (2021). https://doi.org/10.1007/s10658-021-02361-1

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