The Périgord black truffle (Tuber melanosporum Vittad.) and the Piedmont white truffle dominate today’s truffle market^1,2. The hypogeous fruiting body of T. melanosporum is a gastronomic delicacy produced by an ectomycorrhizal symbiont³ endemic to calcareous soils in southern Europe. The worldwide demand for this truffle has fuelled intense efforts at cultivation. Identification of processes that condition and trigger fruit body and symbiosis formation, ultimately leading to efficient crop production, will be facilitated by a thorough analysis of truffle genomic traits. In the ectomycorrhizal Laccaria bicolor, the expansion of gene families may have acted as a ‘symbiosis toolbox’⁴. This feature may however reflect evolution of this particular taxon and not a general trait shared by all ectomycorrhizal species⁵. To get a better understanding of the biology and evolution of the ectomycorrhizal symbiosis, we report here the sequence of the haploid genome of T. melanosporum, which at ∼ 125 megabases is the largest and most complex fungal genome sequenced so far. This expansion results from a proliferation of transposable elements accounting for ∼ 58% of the genome. In contrast, this genome only contains ∼ 7,500 protein-coding genes with very rare multigene families. It lacks large sets of carbohydrate cleaving enzymes, but a few of them involved in degradation of plant cell walls are induced in symbiotic tissues. The latter feature and the upregulation of genes encoding for lipases and multicopper oxidases suggest that T. melanosporum degrades its host cell walls during colonization. Symbiosis induces an increased expression of carbohydrate and amino acid transporters in both L. bicolor and T. melanosporum, but the comparison of genomic traits in the two ectomycorrhizal fungi showed that genetic predispositions for symbiosis—‘the symbiosis toolbox’—evolved along different ways in ascomycetes and basidiomycetes.

For some truffle species of the Tuber genus, the symbiotic phase is often associated with the presence of an area of scant vegetation, commonly known as the brûlé, around the host tree. Previous metagenomics studies have identified the microorganisms present inside and outside the brûlé of a Tuber melanosporum truffle-ground, but the molecular mechanisms that operate in this ecological niche remain to be clarified. To elucidate the metabolic pathways present in the brûlé, we conducted a metaproteomics analysis on the soil of a characterized truffle-ground and cross-referenced the resulting proteins with a database we constructed, incorporating the metagenomics data for the organisms previously identified in this soil. The soil inside the brûlé contained a larger number of proteins and, surprisingly, more proteins from plants, compared with the soil outside the brûlé. In addition, Fisher’s Exact Tests detected more biological processes inside the brûlé; these processes were related to responses to multiple types of stress. Thus, although the brûlé has a reduced diversity of plant and microbial species, the organisms in the brûlé show strong metabolic activity. Also, the combination of metagenomics and metaproteomics provides a powerful tool to reveal soil functioning.

Nowadays, the worldwide agriculture is experiencing a transition process toward more sustainable production, which requires the reduction of chemical inputs and the preservation of microbiomes’ richness and biodiversity. Plants are no longer considered as standalone entities, and the future of agriculture should be grounded on the study of plant-associated microorganisms and all their potentiality. Moreover, due to the climate change scenario and the resulting rising incidence of abiotic stresses, an innovative and environmentally friendly technique in agroecosystem management is required to support plants in facing hostile environments. Plant-associated microorganisms have shown a great attitude as a promising tool to improve agriculture sustainability and to deal with harsh environments. Several studies were carried out in recent years looking for some beneficial plant-associated microbes and, on the basis of them, it is evident that Actinomycetes and arbuscular mycorrhizal fungi (AMF) have shown a considerable number of positive effects on plants’ fitness and health. Given the potential of these microorganisms and the effects of climate change, this review will be focused on their ability to support the plant during the interaction with abiotic stresses and on multi-omics techniques which can support researchers in unearthing the hidden world of plant–microbiome interactions. These associated microorganisms can increase plants’ endurance of abiotic stresses through several mechanisms, such as growth-promoting traits or priming-mediated stress tolerance. Using a multi-omics approach, it will be possible to deepen these mechanisms and the dynamic of belowground microbiomes, gaining fundamental information to exploit them as staunch allies and innovative weapons against crop abiotic enemies threatening crops in the ongoing global climate change context.

Truffles are hypogeous ectomycorrhizal fungi. They belong to the genus Tuber and are currently considered a hot spot in fungal biology due to their e

Plant specialized metabolites (SMs) play an important role in the interaction with the environment and are part of the plant defense response. These natural products are volatile, semi-volatile and non-volatile compounds produced from common building blocks deriving from primary metabolic pathways and rapidly evolved to allow a better adaptation of plants to environmental cues. Specialized metabolites include terpenes, flavonoids, alkaloids, glucosinolates, tannins, resins, etc. that can be used as phytochemicals, food additives, flavoring agents and pharmaceutical compounds. This review will be focused on Mediterranean crop plants as a source of SMs, with a special attention on the strategies that can be used to modulate their production, including abiotic stresses, interaction with beneficial soil microorganisms and novel genetic approaches.