Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana

Abstract

Summary• The function of fungal volatiles in fungal-plant interactions is poorly understood. The aim here was to address this lack of knowledge, focusing on truffles, ectomycorrhizal fungi that are highly appreciated for their aroma.• The effect of volatiles released by truffles was tested on Arabidopsis thaliana in a closed chamber bioassay. The volatiles produced by Tuber melanosporum , Tuber indicum and Tuber borchii fruiting bodies inhibited A. thaliana in terms of root length and cotyledon leaf size, and in some cases induced a bleaching of the seedlings, thus indicating toxicity. Ten synthetic volatiles were tested in a similar way. The strongest inhibitory effect was observed with C 8 molecules such as 1-octen-3-ol, an alcohol with a typical 'fungal smell'.• Two of these C 8 compounds were further tested to investigate their mechanism of action. 1-Octen-3-ol and trans -2-octenal induced an oxidative burst (hydrogen peroxide, H 2 O 2 ) in the A. thaliana leaves as well as a strong increase in the activities of three reactive oxygen species (ROS)-scavenging enzymes.• These results demonstrate that fungal volatiles inhibit the development of A. thaliana and modify its oxidative metabolism. Even though limited to laboratory observations, these results indicate the presence of a hitherto unknown function of fungal volatiles as molecules that mediate fungal-plant interactions.New Phytologist (2007) 175 : [417][418][419][420][421][422][423][424]

Arbuscular mycorrhizal fungal diversity in the Tuber melanosporum brûlé

“…A close correlation between infection in herbaceous plant roots and Tubermelanosporum was observed by Plattner & Hall (1995), who demonstrated that T. melanosporum caused necrosis in the root cortices of Anthoxanthum odoratum, and Leontodon taraxacoides, thus suggesting that this fungus is pathogenic to the weeds, and in part responsible for the brûlé, thanks to this apparent pathogenic effect and to the production of toxic volatiles. Since the inhibitory effect of T. melanosporum volatiles on herbaceous plants has been widely acknowledged ( Splivallo et al, 2007, Splivallo et al, 2011and Streiblova et al, 2012, which would seem to indicate that fungal volatiles can mediate fungal-plant interactions, it is possible to imagine that there could also be an effect of T. melanosporum on the AMF that colonize the patchy vegetation. This work clearly shows, for the first time, that the patchy herbaceous plants around a T. melanosporum host tree are colonized by AMF to a great extent, as are the plants outside the brûlé, where the vegetation coverage is regular.…”

“…( Pacioni 1991). Splivallo et al (2007) have demonstrated the inhibitory effect of truffle volatiles on the development of the nonhost plant Arabidopsis thaliana in laboratory conditions, and have indicated that fungal volatiles are molecules that can mediate fungal-plant interactions, thus raising questions about their role in the origin of the brûlé. In addition, truffle mycelia produce ethylene and indole-3-acetic acid (IAA), which, in large quantities, might act as herbicides and thus explain the formation of the brûlé ( Splivallo et al 2011).…”

Dimethyl Disulfide Produced by the Naturally Associated Bacterium Bacillus sp B55 Promotes Nicotiana attenuata Growth by Enhancing Sulfur Nutrition

“…The PGP effects were largely attributed to two volatiles, namely, 3-hydroxybutan-2-one (acetoin) and 2,3-butanediol. Several other studies have examined bacterial bioactive volatile compounds that promote or suppress plant growth (Farag et al, 2006;Splivallo et al, 2007;Vespermann et al, 2007;Kai et al, , 2010Gutiérrez-Luna et al, 2010;Zou et al, 2010;Blom et al, 2011aBlom et al, , 2011bVelazquez-Becerra et al, 2011;Weise et al, 2012;Yu and Lee, 2013), but the underlying mechanisms of these effects remain largely unknown (Wenke et al, 2012b). Profiling studies in Arabidopsis seedlings provided the first insights into changes in the transcriptome and proteome elicited by exposure to bacterial VOCs (Zhang et al, 2007;Kwon et al, 2010) and revealed the importance of hormone signaling, particularly that of indole-3-acetic acid and abscisic acid (Zhang et al, 2007(Zhang et al, , 2008.…”

Truffles Regulate Plant Root Morphogenesis via the Production of Auxin and Ethylene

“…Volatile organic compounds have been implicated in the signaling between truffle and plants. Splivallo et al (2007) discussed the phytotoxic activity of fruiting body volatiles and Menotta et al (2004) highlighted their potential role as mycorrhization signals. Fruiting bodies volatiles shortened primary roots of plants (Splivallo et al, 2007) while the effect of mycelial metabolites has not been addressed.…”