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Dihydroisocoumarins produced by Diaporthe cf. heveae LGMF1631 inhibiting citrus pathogens

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Abstract

Citrus black spot (CBS) and post-bloom fruit drop (PFD), caused by Phyllosticta citricarpa and Colletotrichum abscissum, respectively, are two important citrus diseases worldwide. CBS depreciates the market value and prevents exportation of citrus fruits to Europe. PFD under favorable climatic conditions can cause the abscission of flowers, thereby reducing citrus production by 80%. An ecofriendly alternative to control plant diseases is the use of endophytic microorganisms, or secondary metabolites produced by them. Strain LGMF1631, close related to Diaporthe cf. heveae 1, was isolated from the medicinal plant Stryphnodendron adstringens and showed significant antimicrobial activity, in a previous study. In view of the potential presented by strain LGMF1631, and the absence of chemical data for secondary metabolites produced by D. cf. heveae, we decided to characterize the compounds produced by strain LGMF1631. Based on ITS, TEF1, and TUB phylogenetic analysis, strain LGMF1631 was confirmed to belong to D. cf. heveae 1. Chemical assessment of the fungal strain LGMF1631 revealed one new seco-dihydroisocoumarin [cladosporin B (1)] along with six other related, already known dihydroisocoumarin derivatives and one monoterpene [(−)-(1S,2R,3S,4R)-p-menthane-1,2,3-triol (8)]. Among the isolated metabolites, compound 5 drastically reduced the growth of both phytopathogens in vitro and completely inhibited the development of CBS and PFD in citrus fruits and flowers. In addition, compound 5 did not show toxicity against human cancer cell lines or citrus leaves, at concentrations higher than used for the inhibition of the phytopathogens, suggesting the potential use of (−)-(3R,4R)-cis-4-hydroxy-5-methylmellein (5) to control citrus diseases.

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Acknowledgments

We thank the College of Pharmacy NMR Center (University of Kentucky) for NMR support.

Funding

This work was supported by National Institutes of Health grant R24 OD21479 (JST), the University of Kentucky College of Pharmacy, the University of Kentucky Markey Cancer Center, and the National Center for Advancing Translational Sciences (UL1TR001998 and UL1TR000117). Additional support came from NIH grants CA 91091, GM 105977, and an Endowed University Professorship in Pharmacy to J.R. It was also supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico – Brazil grant 424738/2016-3 and CNPq309971/2016-0 to C.G., and CAPES-Brazil—grant to D.C.S.

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  1. Daiani Cristina Savi, Sandriele Aparecida Noriler and Khaled A. Shaaban contributed equally to this work.

Authors and Affiliations

  1. Department of Genetics, Universidade Federal do Parana, Av. Coronel Francisco Heráclito dos Santos, 210, Curitiba, PR, 81531-970, Brazil

    Daiani Cristina Savi & Chirlei Glienke

  2. Department of Pharmaceutical Sciences, College of Pharmacy, University of Kentuck, Lexington, KY, 40536, USA

    Daiani Cristina Savi, Larissa V. Ponomareva, Jon S. Thorson, Jürgen Rohr & Khaled A. Shaaban

  3. Department of Pathology, Universidade Federal do Parana, Av. Coronel Francisco Heráclito dos Santos, 210, Curitiba, PR, 81531-970, Brazil

    Sandriele Aparecida Noriler

  4. Center for Pharmaceutical Research and Innovation, College of Pharmacy, University of Kentucky, Lexington, KY, 40536, USA

    Larissa V. Ponomareva, Jon S. Thorson & Khaled A. Shaaban

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Savi, D.C., Noriler, S.A., Ponomareva, L.V. et al. Dihydroisocoumarins produced by Diaporthe cf. heveae LGMF1631 inhibiting citrus pathogens. Folia Microbiol 65, 381–392 (2020). https://doi.org/10.1007/s12223-019-00746-8

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