Germination of Penicillium paneum Conidia Is Regulated by 1-Octen-3-ol, a Volatile Self-Inhibitor

Abstract

Penicillium paneum is an important contaminant of cereal grains which is able to grow at low temperature, low pH, high levels of carbon dioxide, and under acid conditions. P. paneum produces mycotoxins, which may be harmful to animals and humans. We found that conidia in dense suspensions showed poor germination, suggesting the presence of a self-inhibitor. A volatile compound(s) produced by these high-density conditions also inhibited mycelial growth of different species of fungi belonging to a variety of genera, suggesting a broad action range. The heat-stable compound was isolated by successive centrifugation of the supernatant obtained from spore suspensions with a density of 10 9 conidia ml ؊1 . By using static headspace analyses, two major peaks were distinguished, with the highest production of these metabolites after 22 h of incubation at 25°C and shaking at 140 rpm. Gas chromatography coupled with mass spectra analysis revealed the compounds to be 3-octanone and 1-octen-3-ol. Notably, only the latter compound appeared to block the germination process at different developmental stages of the conidia (swelling and germ tube formation). In this study, 1-octen-3-ol influenced different developmental processes during the P. paneum life cycle, including induction of microcycle conidiation and inhibition of spore germination. Therefore, the compound can be considered a fungal hormone during fungal development.The spore is an important vehicle for distribution or longterm survival of fungi. Conidia are nonmotile asexual spores, which can be produced in very large numbers by fungi belonging to the order Eurotiales. This order, which includes the genera Aspergillus and Penicillium (14), contains many species of food-related fungi. Conidia are dispersed into the air but do not germinate before they reach a suitable substrate. Invariably, germination is inhibited when spores are present in high densities, an effect observed for example in Aspergillus niger and the zygomycete Syncephalastrum racemosum (3,19). This is designated as the crowding effect. Also, in the formation of an adhesive bud on spores of the nematophagous fungus Drechmeria coniospora, there is a clear crowding effect (35). These observations suggest that intercellular signaling prevents premature germination.Acervuli of Colletotrichum spp. form large numbers of conidia embedded in mucilage but not germinating there. From the mucilage that surrounds the conidia of this fungus, a self-inhibitor of germination named mycosporine-alanine has been identified and characterized (26). Germination is also retarded in pustules of rust fungi (Basidiomycetes) where cisferulic acid methyl ester and cis-3,4-dimethoxycinnamic acid methyl ester have been identified (28, 36).Self-inhibitors have been characterized in Puccinia, Uromyces, Colletotrichum, Dictyostelium, Fusarium oxysporum, and Aspergillus and can be volatile or nonvolatile (2,3,16,24,28).They also can influence other fungal processes, for example, mycosporine-alanine produced by Colletotrichum graminic...

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