Effects of Glucosinolate-Derived Isothiocyanates on Fungi: A Comprehensive Review on Direct Effects, Mechanisms, Structure-Activity Relationship Data and Possible Agricultural Applications

Abstract

Plants heavily rely on chemical defense systems against a variety of stressors. The glucosinolates in the Brassicaceae and some allies are the core molecules of one of the most researched such pathways. These natural products are enzymatically converted into isothiocyanates (ITCs) and occasionally other defensive volatile organic constituents (VOCs) upon fungal challenge or tissue disruption to protect the host against the stressor. The current review provides a comprehensive insight on the effects of the isothiocyanates on fungi, including, but not limited to mycorrhizal fungi and pathogens of Brassicaceae. In the review, our current knowledge on the following topics are summarized: direct antifungal activity and the proposed mechanisms of antifungal action, QSAR (quantitative structure-activity relationships), synergistic activity of ITCs with other agents, effects of ITCs on soil microbial composition and allelopathic activity. A detailed insight into the possible applications is also provided: the literature of biofumigation studies, inhibition of post-harvest pathogenesis and protection of various products including grains and fruits is also reviewed herein.

Keywords: Cruciferae; QSAR; VOC; antifungal natural products; biofumigation; crop protection; fungi; glucosinolates; grain storage; isothiocyanates; synergistic activity.

Figure 1

Glucosinolates and isothiocyanates mentioned in the current review. The classification is based on [5]. If available, the trivial names for glucosinolates are mentioned in the absence of trivial names, the GSL name is formed from the side chain name. Abbreviations: Ac—acetyl-group, Ara—arabinoside; Glc—glucoside; ITC—isothiocyanate; Rha—rhamnoside; Xyl—xyloside. 1. methyl ITC/Glucocapparin; 2. ethyl ITC/Glucolepidiin; 3. propyl ITC; 4. i-propyl ITC/Glucoputranjivin; 5. butyl ITC; 6. iso-butyl ITC; 7. pentyl ITC; 8. hexyl ITC; 9. octyl ITC; 10. nonyl ITC; 11. 2-propenyl ITC (allyl ITC)/sinigrin; 12. 3-butenyl ITC/Gluconapin; 13. 4-pentenyl ITC/Glucobrassicanapin; 14. 2-hydroxy-3-butenyl ITC/Progoitrin; 15. 4-isothiocyanatobutanoic acid; 16. 4-oxopentyl ITC; 17. phenyl ITC; 18. 4-methoxybenzyl ITC/Glucoaubrietin; 19. 3-methoxybenzyl ITC/Glucolimnanthin; 20. benzyl ITC/Glucotropaeolin; 21. 4-hydroxybenzyl ITC/sinalbin; 22. 3-hydroxybenzyl ITC/Glucolepigramin; 23. phenethyl ITC/Gluconasturtiin; 24. hydroxyphenethyl ITC/Glucobarbarin, 25. 4-hydroxyphenethyl ITC; 26. 3-phenylpropyl ITC; 27. sinapigladioside; 28. 4-phenylbutyl ITC; 29. 5-phenylpentyl ITC; 30. 4-(a-L-rhamnosyloxy)-benzyl ITC; 31. 4-(4′-O-acetyl-a-L-rhamnosyloxy)-benzyl ITC; 32. 3-(methylsulfinyl)propyl ITC; 33. 4-(methylsulfinyl)butyl ITC (sulforaphane)/glucoraphanin; 34. 9-(methylsulfinyl)nonyl ITC/Glucoarabin; 35. 3-(methylsulfonyl)propyl ITC; 36. 4-(methylsulfonyl)butyl ITC; 37. 9-(methylsulfonyl)nonyl ITC; 38. 3-(methylsulfanyl)propyl ITC (iberverin)/Glucoiberverin; 39. 4-(methylthio)butyl ITC (erucin)/Glucoerucin; 40. 4-methylsulfinyl-3-butenyl ITC (sulforaphene)/Glucoraphanin; 41. 5-(methylthio)pentyl ITC (Berteroin); 42. 9-(methylthio)nonyl ITC; 43. indol-3-ylmethyl ITC/Glucobrassicin; 44. 1-methoxyindol-3-ylmethyl ITC/Neoglucobrassicin.

Figure 2

Deglucosylation and subsequent spontaneous rearrangement of glucosinolates into various volatile natural products. Compiled from data in [4,13]. Abbreviations: ESM—epithiospecifier modifier protein; ESP—epithionitrile specifier protein; Glc—glucose; NSP—nitrile specifier protein; PEN2—atypical myrosinase; TGG—beta-thioglucoside glucohydrolase (myrosinase); TFP—thiocyanate-forming protein.

Figure 3

Reaction of isothiocyanates with nucleophiles. Compiled from data in [13].