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Phytotoxins Produced by Lasiodiplodia Phytopathologia Mediterranea Firenze University Press The international journal of the www.fupress.com/pm Mediterranean Phytopathological Union Short Notes Phytotoxins produced by Lasiodiplodia laeliocattleyae involved in Botryosphaeria Citation: Reveglia P., Masi M., Cim- mino A., Michereff S., Cinelli T., Mugnai dieback of grapevines in Brazil L., Evidente A. (2019) Phytotoxins pro- duced by Lasiodiplodia laeliocattleyae involved in Botryosphaeria dieback of grapevines in Brazil. Phytopatholo- Pierluigi REVEGLIA1,2,*, Marco MASI2, Alessio CIMMINO2, Sami gia Mediterranea 58(1): 207-211. doi: MICHEREFF3, Tamara CINELLI3, Laura MUGNAI3, Antonio EVIDENTE2 10.14601/Phytopathol_Mediterr-24647 1 National Wine and Grape Industry Centre, School of Agricultural and Wine Sciences, Accepted: March 20, 2019 Charles Sturt University, Locked Bag 588 Wagga Wagga NSW 2678, Australia 2 University of Naples Federico II, Department of Chemical Sciences Complesso Universi- Published: May 15, 2019 tario Montesant’Angelo, Via Cintia 4, 80126, Naples, Italy 3 Copyright: © 2019 Reveglia P., Masi Dipartimento di Scienze delle Produzioni Agroalimentari e dell’Ambiente, Sez. Patologia M., Cimmino A., Michereff S., Cinelli T., vegetale ed entomologia, Università di Firenze, Piazzale delle Cascine 28, 50144 Firenze, Mugnai L., Evidente A. This is an open Italy access, peer-reviewed article published Corresponding author: [email protected] by Firenze University Press (http:// www.fupress.com/pm) and distributed under the terms of the Creative Com- Abstract. Botryosphaeria dieback (BD) is an important trunk disease affecting grape- mons Attribution License, which per- vines. Several Lasiodiplodia species have been shown to be involved in BD affecting mits unrestricted use, distribution, and the perennial organs of grapevine, mainly causing cankers. (R)-(-)-mellein and tyrosol, reproduction in any medium, provided two well-known fungal phytotoxins, were isolated from the organic extract of culture the original author and source are credited. filtrate of Lasiodiplodia laeliocattleyae (syn. egyptiacae), which had been isolated from grapevines affected by BD in Brazil. This increases knowledge of the secondary metab- Data Availability Statement: All rel- olites produced by Lasiodiplodia species, confirming that (R)-(-)-mellein is a toxin typ- evant data are within the paper and its ically produced by Botryosphaericeae species. Supporting Information files. Keywords. Grapevine wood disease, phytotoxins, (R)-(-)-mellein, tyrosol. Competing Interests: The Author(s) declare(s) no conflict of interest. Editor: E. Paplomatas, Agricultural University of Athens, Greece. INTRODUCTION Botryosphaeria dieback (BD) is a grapevine trunk disease that causes serious problems for grape production, including emerging wine-producing countries such as Brazil. The economic impacts of grapevine trunk diseases result from significant yield reductions from diseased vines and increased production costs for application of control measures. Many efforts have been made to find new and effective management practices for the disease (Mon- dello et al., 2018). BD also affects many fruit tree crops, including mango, olive, walnut and almond (de Oliveira Costa et al., 2010; Olmo et al., 2016; Rodríguez-Gálvez et al., 2017). BD of grapevine is caused by several Botryosphaeriaceae species, associ- ated with decline symptoms including dieback, wood canker and spur die- back (Úrbez-Torres, 2011; Billones-Baijens and Savocchia 2018; Gramaje et al., 2018; Mondello et al., 2018). Phytopathologia Mediterranea 58(1): 207-211, 2019 ISSN 0031-9465 (print) | ISSN 1593-2095 (online) | DOI: 10.14601/Phytopathol_Mediterr-24647 208 P. RevegliaS. Arif et alii Like other trunk disease pathogens, Botryospha- inoculated and grown in stationary culture, as reported eriaceous species can produce toxic metabolites belong- for other strains of Lasiodiplodia (Cimmino et al., 2017), ing to different compound classes including aromatic in modified Difco Czapek Dox medium (Benton), with compounds, isocoumarins, jasmonates, naphthalenones, 0.5% yeast and 0.5% malt extract (Difco). The cultures polyketides, and phenols (Martos et al., 2008; Masi et al., were grown for 21 d at 25 °C in the dark. The mycelium 2018). In particular, Lasiodiplodia species were investi- was removed and the liquid cultures were lyophilized gated for production of phytotoxic metabolites and other prior to the extraction procedure. substances (including jasmonic acid, mellein, lasiodiplo- din, theobroxide, butyrolactones, botryosphaeran, bot- ryorodines, lasiodiplodan) are produced in vitro by dif- Extraction of low molecular weight phytotoxic metabolites ferent isolates of L. theobromae and other Lasiodiplodia spp. such as L. mediterranea. These toxic metabolites The lyophilized residues of the culture filtrates (2.85 have also been purified from in vitro cultures of strains L) were dissolved in 300 mL of water and extracted with isolated from host pants other than grapevine, and test- EtOAc (3 × 300 mL) at the same pH as the original cul- ed for their toxic activity (Aldridge et al. 1971, Husan et ture (pH 8). The organic extracts were then combined, al. 1993, Matsuura et al., 1998, He et al., 2004, Miranda dried (Na2SO4), filtered, and evaporated under low pres- et al., 2008, Kitoaka et al., 2009, Andolfi et al., 2014). sure. The organic residue (264.0 mg) was purified by silica In a recent study, phytotoxic metabolites produced in gel column chromatography using CHCl3-i-PrOH (95:5, liquid cultures by six species of Lasiodiplodia isolated in v/v), and six fractions of homogenous groups were collect- Brazil, and causing Botryosphaeria dieback of grapevine, ed. The residue (21.9 mg) of fraction #1 was purified by were chemically identified. As determined by LC-MS, L. preparative TLC on silica gel using CHCl3 as eluent. This brasiliense, L. crassispora., L. iraniensis, L. pseudothe- yielded a white solid, which was identified as R(-)- mel- obromae produced jasmonic acid, while L. brasiliense lein (1, Figure 1, 13.7 mg). The residue of fraction #3 was synthesized jasmonic acid and (3R,4S)-4-hydroxymellein. purified on preparative TLC on silica gel, using CHCl3-i- Lasiodiplodia euphorbiaceicola and L. hormozganensis PrOH (97:3, v/v) as eluent, yielding a white solid, which produced some low molecular weight lipophilic toxins, was identified as tyrosol 2( , Figure 1, 12.4 mg). that were isolated and identified (Cimminoet al., 2017). In particular, from culture filtrate of L. euphorbiaceicola, Chemical analyses and characterization (R)-(-)-mellein, (3R,4R)-(-)- and (3R,4S)-(-)-4-hydroxymel- lein, and tyrosol were isolated, and identified. Tyrosol and Optical rotations were measured in MeOH on a Jas- p-hydroxybenzoic acid were also isolated from culture fil- co P-1010 digital polarimeter (Jasco). 1H NMR spectra trates of L. hormozganensis (Cimmino et al., 2017). were recorded at 400 or 500 MHz in CDCl3 on Bruker Knowledge of the non-specific phytotoxins produced and Varian instruments, with MeOH as an internal by Botryosphaeriaceous species is increasing (Masi et al., standard. ESI MS and LC/MS analyses were performed 2018), and it is increasingly important to determine the using the LC/MS TOF system AGILENT (Agilent Tech- full spectrum of these metabolites to understand their nologies) 6230B, HPLC 1260 Infinity. Analytical and roles in disease and symptom development (Meh et al., preparative TLC was carried out on silica gel plates (Kie- 2013). This note reports the isolation of phytotoxins pro- selgel 60, F254, 0.25 mm and 0.5 mm) (Merck). TLC duced in vitro from L. laeliocattleyae (syn. egyptiacae) spots were visualized by exposure to UV radiation, or (Jayawardena et al., 2018), a pathogen of grapevine (Cor- by spraying first with 10% H2SO4 in MeOH, and then reia et al., 2016) and agent of mango dieback and fruit with 5% phosphomolybdic acid in EtOH, followed by rot (Rosado et al., 2016). To our knowledge this is the heating at 110°C for 10 min. Column chromatography first report of phytotoxic metabolites isolated from L. was performed using silica gel (Kieselgel 60, 0.063-0.200 laeliocattleyae. mm) (Merck). Standard sample of (R)-(-)-mellein was obtained from the culture filtrates of Sardiniella urbana (Cimmino et al., 2018), and of tyrosol from Lasiodiplo- MATERIALS AND METHODS dia euphorbiaceicola (Cimmino et al., 2017). Fungal isolates and culture conditions Phytotoxicity bioassay The strain of L. laeliocattleyae (CMM0206) used in this study was obtained from the collection of Universi- The phytotoxic activity of chromatographic organic dade Federal Rural de Pernambuco, Recife, Brazil. It was extract fractions was assayed on lemon fruit, using pre- LeafLasiodiplodia rot of pak laeliocattleyae choy phytotoxins 209 viously reported protocol (Andolfi et al., 2014b; Cimmi- by several different species of Botryosphaeriaceae such us no et al., 2017). Diplodia mutila, Neofusicoccum parvum, Neofusiccoum australe, Neofusicoccum luteum isolated from grapevine in different grape-growing areas in the world, posing RESULTS questions about its involvement in the virulence of Botry- osphaeria dieback pathogens (Reveglia et al., 2018). The culture filtrates of L. laeliocattleyae were Melleins are isocoumarins, and together with jas- exhaustively extracted with ethyl acetate. The organic monic acid, its esters, dihydrofuranones and closely extract and the resulting aqueous phases were assayed related compounds, these are specifically related to
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