Elsevier

Tetrahedron

Volume 64, Issue 8, 18 February 2008, Pages 1612-1619
Tetrahedron

Phyllostictines A–D, oxazatricycloalkenones produced by Phyllosticta cirsii, a potential mycoherbicide for Cirsium arvense biocontrol

https://doi.org/10.1016/j.tet.2007.12.010Get rights and content

Abstract

Phyllosticta cirsii, a fungal pathogen isolated from Cirsium arvense and proposed as biocontrol agent of this noxious perennial weed, produces in liquid cultures different phytotoxic metabolites with potential herbicidal activity. Four new oxazatricycloalkenones, named phyllostictines A–D, were isolated and characterized using essentially spectroscopic and chemical methods. Tested by leaf-puncture assay on the fungal host plant phyllostictine A proved to be highly toxic. The phytotoxicity decreases when both the dimension and the conformational freedom of the macrocyclic ring change, as in phyllostictines B and D, and it is totally lost when also the functionalization of the same ring is modified, as in phyllostictine C. Beside its phytotoxic properties, phyllostictine A has no antifungal activity, an interesting antibiotic activity only against Gram+ bacteria, and a noticeable zootoxic activity when tested at high concentrations. The integrity of the oxazatricycloalkenone system appears to be an important feature to preserve these activities.

Graphical abstract

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From the liquid culture of Phyllosticta cirsii four new oxazatricycloalkenones, named phyllostictine A–D (14), were isolated, and chemically and biologically characterized. Three of them (1, 2, and 4) proved to have interesting herbicidal activity.

Introduction

Cirsium arvense (L.) Scop. (commonly called Canada thistle) is a persistent perennial weed that grows vigorously, forming dense colonies, and spreading by roots growing horizontally that give rise to aerial shoots. It spreads by seed either by wind or as a contaminant in crop seed. Canada thistle is native to south eastern Europe and the eastern Mediterranean area. It has spread to most temperate parts of the world and is considered an important weed all around the world as it infests many habitats such as cultivated fields, roadsides, pastures and rangeland, railway embankments, and lawns. There is no easy method of control, and all methods require follow-up. Combinations of mechanical, cultural, and chemical methods are more effective than any single method used alone.1 Although there are no effective biological control organisms available at this time, search for efficacious biocontrol microorganisms and natural herbicides is receiving a renewed interest.

Recently, the fungus Phyllosticta cirsii has been evaluated as a possible biocontrol agent of Canada thistle.2 Species belonging to the genus Phyllosticta are known to produce bioactive metabolites, including non-host phytotoxins, e.g., phyllosinol, brefeldin, and PM-toxin isolated by cultures of Phyllosticta sp.,3 Phyllosticta maydis,4 and Phyllosticta medicaginis,5 respectively.

Considering the interest for bioactive metabolites produced by weed pathogens as sources of novel natural herbicides, it seemed interesting to investigate the production of toxins by this species of Phyllosticta.

This paper describes the isolation, structural elucidation, and biological characterization of four new phytotoxic oxazatricycloalkenones produced in liquid culture by P. cirsii, named phyllostictines A–D (14) (Fig. 1). Their structure was determined by extensive use of spectroscopic (essentially NMR and MS techniques) and chemical methods.

Section snippets

Results and discussion

The liquid culture of P. cirsii (7.7 L) was exhaustively extracted as reported in Section 4. The organic extract, having high phytotoxicity, was purified by a combination of CC and TLC as described in Section 4. Four metabolites were obtained as homogeneous oily compounds (11.0, 1.0, 0.9, and 0.5 mg/L, respectively), which were named phyllostictines A–D (14). Preliminary 1H and 13C investigations allowed to demonstrate that these metabolites have closely related structures being, as described

Conclusion

Phyllostictines A–D are the first four fungal metabolites described to belong to a oxazatricycloalkenone group and to occur for the first time as natural compounds with interesting biological activity. In particular, the main fungal metabolite phyllostictine A showed potentially strong herbicidal properties not associated to antifungal or zootoxic activities, while a selective antibiosis was exhibited against Gram+ bacteria. Compounds containing macrocyclic rings as well as furan derivatives

General

Optical rotation was measured in CHCl3 solution on a Jasco P-1010 digital polarimeter and the CD spectrum was recorded on a JASCO J-710 spectropolarimeter in CHCl3 solution. IR spectra were recorded as neat on a Perkin–Elmer Spectrum One FT-IR Spectrometer and UV spectra were taken in MeCN solution on a Perkin–Elmer Lambda 25 UV/vis spectrophotometer. 1H and 13C NMR spectra were recorded at 600, and at 150 and 75 MHz, respectively, in CDCl3 by Bruker spectrometers. The same solvent was used as

Acknowledgements

The authors thank ‘Servizio di Spettrometria di Massa del CNR’, Pozzuoli, Italy and for mass spectra, the assistance of the staff is gratefully acknowledged. The NMR spectra were recorded in the laboratory of the Istituto di Chimica Biomolecolare del CNR, Pozzuoli, Italy. This work was carried out within the project ‘Enhancement and Exploitation of Soil Biocontrol Agents for Bio-Constraint Management in Crops’ (Contract no. FOOD-CT-2003-001687), which is financially supported by the European

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    Has contributed for registration of some HRESIMS spectra.

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