Truffle volatiles: from chemical ecology to aroma biosynthesis

Abstract

Summary Truffles (Tuber spp.) are symbiotic fungi that develop underground in association with plant roots. Food connoisseurs describe their scent as sensual, seductive and unique. These mysterious fungi, however, do not produce their aroma for the mere pleasure of humans. Truffle volatiles act as odorant cues for mammals and insects which are thus able to locate the precious fungi underground and spread their spores. They also freely diffuse in the soil and mediate interactions with microorganisms and plant roots, potentially regulating a complex molecular dialogue among soil fauna and flora. The aim of this review is to synthesize 30 yr of research on truffle volatiles, spanning fields of study from chemical ecology to aroma biosynthesis. Specific aspects of truffle volatile ecology and biology will be discussed, including which species have been studied so far and for what purpose, what ecological role has been demonstrated or speculated to exist for specific truffle volatiles, which volatiles are common or unique to certain species and what their biosynthetic route might be. Future challenges in truffle aroma research will also be addressed, focusing on how high‐throughput post‐genomic technologies may advance our understanding of truffle aroma biosynthesis and chemical ecology.

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.…”

“…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). What actually causes the brûlé is not known precisely, although some studies have recently reported its impact on the microorganisms that live inside this area ( Napoli et al, 2010 andMello et al, 2013;see below).…”

Does the natural “microcosm” created by Tuber aestivum affect soil microarthropods? A new hypothesis based on Collembola in truffle culture

“…are symbiotic fungi that depend closely on other organisms to complete their lifecycle. T. aestivum emits volatile organic compounds (VOCs) to attract animal vectors for spore dispersal and possibly other functions (Pacioni et al, 1991;Splivallo et al, 2011). Bellina-Agostinone et al (1987) found that thiobismethane or dimethyl sulphide is the main VOC compound in T. aestivum.…”

Diversity, population genetics, and evolution of macrofungi associated with animals

“…Similar to other hypogeous macrofungi, Tuber truffles require and recruit mycetophagous mammals to disperse their spores. Generally, mycetophagous animals are attracted by truffle volatiles, which then consume sporocarps and disseminate spores in their fecal pellets (Splivallo et al 2011; Danks 2012). In the case of truffles, the dispersing distance is determined by two factors: (i) the gut-retention time of spores in mycetophagous mammals, which generally might be more than 20 h; and (ii) the travel distance of the mammals within that time span, which may cover dozens of hectares (Danks 2012; Vernes and Jarman 2014).…”