The Périgord black truffle (Tuber melanosporum Vittad.) and the Piedmont white truffle dominate today's truffle market. The hypogeous fruiting body of T. melanosporum is a gastronomic delicacy produced by an ectomycorrhizal symbiont 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'. This feature may however reflect evolution of this particular taxon and not a general trait shared by all ectomycorrhizal species. 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 approximately 125 megabases is the largest and most complex fungal genome sequenced so far. This expansion results from a proliferation of transposable elements accounting for approximately 58% of the genome. In contrast, this genome only contains approximately 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.
Blots were performed against DDR (p53 pSer15, histone 2AX pSer139), cell survival/ cell death (AKT pThr308, cleaved PARP), and cell signaling (ERK1/2 pThr202/Tyr204) markers and controls. Actin and GAPDH served as loading controls.
Mycorrhizal fungi are a heterogeneous group of diverse fungal taxa, associated with the roots of over 90 % of all plant species. Recently, state-of-the-art molecular and genetic tools, coupled to high-throughput sequencing and advanced microscopy, have led to the genome and transcriptome analysis of several symbionts. Signalling pathways between plants and fungi have now been described and the identifi cation of several novel nutrient transporters has revealed some of the cellular processes that underlie symbiosis. Thus, the contributions of each partner in a mycorrhizal association are starting to be unravelled. This new knowledge is now available for use in agricultural practices.O wing to their fi lamentous organization, fungi exploit very diverse substrates on the basis of their nutritional strategy. Saprobes thrive in soil, water and on decaying animal and plant tissues. A smaller group of fungi, the parasitic and mutualistic symbionts, feed on living organisms 1 . Such a classifi cation cannot easily be applied to mycorrhizal fungi, a heterogeneous group of species spread over diverse fungal taxa. Although they can spend part of their life cycle as free-living organisms, mycorrhizal fungi always associate with the roots of higher plants, indeed over 90 % of plant species, including forest trees, wild grasses and many crops. Both partners benefi t from the relationship: mycorrhizal fungi improve the nutrient status of their host plants, infl uencing mineral nutrition, water absorption, growth and disease resistance, whereas in exchange, the host plant is necessary for fungal growth and reproduction 2 .Mycorrhizal fungi colonize environments such as alpine and boreal zones, tropical forests, grasslands and croplands. Th ey have a major role in nutrient cycling through the specifi c activity of their mycelium in absorbing soil nutrients and supplying them to the plant, although their role in carbon fl ux is less well defi ned 3 .Th e term mycorrhiza is derived from the Greek words for ' fungus ' and ' root ' . Mycorrhizal fungi develop an extensive hyphal network in the soil, the aptly named wood-wide web 4 , which can connect whole plant communities off ering effi cient horizontal transfer of nutrients. Mycorrhizas develop specialized areas, called symbiotic interfaces, to interact with the host plant 5 -7 . Mycorrhizal fungi can be divided into two major groups: aseptate endophytes such as Glomeromycota, or septate Asco-and Basidiomycota (see Box 1 Glossary) 2 . More commonly, mycorrhiza classifi cations refl ect anatomical aspects and identify two broad categories 2 , referred to as ectomycorrhizas (EMs) and endomycorrhizas, depending on whether the fungus colonizes the root intercellular spaces or develops inside cells ( Fig. 1 ). Endomycorrhizas are further divided into orchid, ericoid and arbuscular mycorrhizas (AMs).A descriptive approach has dominated the investigation of mycorrhizas for at least 50 years until the advent of molecular biology, and the ' omics ' era provided insight into their mechanis...
This review focuses on interactions among plants, mycorrhizal fungi, and bacteria, testing the hypothesis whether mycorrhizas can be defined as tripartite associations. After summarizing the main biological features of mycorrhizas, we illustrate the different types of interaction occurring between mycorrhizal fungi and bacteria, from loosely associated microbes to endobacteria. We then discuss, in the context of nutritional strategies, the mechanisms that operate among members of the consortium and that often promote plant growth. Release of active molecules, including volatiles, and physical contact among the partners seem important for the establishment of the bacteria/mycorrhizal fungus/plant network. The potential involvement of quorum sensing and Type III secretion systems is discussed, even if the exact nature of the complex interspecies/interphylum interactions remains unclear.
SummaryThe primary objective of this study was to identify the molecular signals present in arbuscular mycorrhizal (AM) germinated spore exudates (GSEs) responsible for activating nuclear Ca 2+ spiking in the Medicago truncatula root epidermis.Medicago truncatula root organ cultures (ROCs) expressing a nuclear-localized cameleon reporter were used as a bioassay to detect AM-associated Ca 2+ spiking responses and LC-MS to characterize targeted molecules in GSEs. This approach has revealed that short-chain chitin oligomers (COs) can mimic AM GSE-elicited Ca 2+ spiking, with maximum activity observed for CO4 and CO5. This spiking response is dependent on genes of the common SYM signalling pathway (DMI1/DMI2) but not on NFP, the putative Sinorhizobium meliloti Nod factor receptor. A major increase in the CO4/5 concentration in fungal exudates is observed when Rhizophagus irregularis spores are germinated in the presence of the synthetic strigolactone analogue GR24. By comparison with COs, both sulphated and nonsulphated Myc lipochito-oligosaccharides (LCOs) are less efficient elicitors of Ca 2+ spiking in M. truncatula ROCs. We propose that short-chain COs secreted by AM fungi are part of a molecular exchange with the host plant and that their perception in the epidermis leads to the activation of a SYM-dependent signalling pathway involved in the initial stages of fungal root colonization.
The penetration of arbuscular mycorrhizal (AM) fungi through the outermost root tissues of the host plant is a critical step in root colonization, ultimately leading to the establishment of this ecologically important endosymbiotic association. To evaluate the role played by the host plant during AM infection, we have studied in vivo cellular dynamics within Medicago truncatula root epidermal cells using green fluorescent protein labeling of both the plant cytoskeleton and the endoplasmic reticulum. Targeting roots with Gigaspora hyphae has revealed that, before infection, the epidermal cell assembles a transient intracellular structure with a novel cytoskeletal organization. Real-time monitoring suggests that this structure, designated the prepenetration apparatus (PPA), plays a central role in the elaboration of the apoplastic interface compartment through which the fungus grows when it penetrates the cell lumen. The importance of the PPA is underlined by the fact that M. truncatula dmi (for doesn't make infections) mutants fail to assemble this structure. Furthermore, PPA formation in the epidermis can be correlated with DMI-dependent transcriptional activation of the Medicago early nodulin gene ENOD11. These findings demonstrate how the host plant prepares and organizes AM infection of the root, and both the plant-fungal signaling mechanisms involved and the mechanistic parallels with Rhizobium infection in legume root hairs are discussed.Arbuscular mycorrhizae (AM) are highly specialized endosymbiotic associations formed between a restricted group of biotrophic soil fungi (the Glomeromycota) and the large majority of vascular land plants, including most angiosperm and gymnosperm families. Fossil evidence shows that AM symbiosis has existed for >450 million years (Remy et al., 1994), and this unique beneficial fungal-plant association is believed to have played a major role in the early colonization of land plants. AM fungi penetrate and colonize the root, forming highly differentiated symbiotic structures known as arbuscules, which are the principal sites of metabolic exchange between the two organisms (reviewed in Harrison, 2005). Concomitant extraradical hyphal development allows the fungus to supply important nutrients, including phosphate, to the host, while in return receiving carbohydrates from the plant. The AM symbiosis also confers resistance to the plant against biotic and abiotic stresses.Despite the agronomic and ecological importance of the AM symbiosis, the molecular and cellular events associated with the establishment of the association are poorly understood. This is primarily attributable to the difficulty in culturing these obligate fungi, coupled with the low frequency and lack of synchrony of host infection. Nevertheless, it is now clearly established that, before infection, germinated AM fungi respond to host root exudates by switching to an active presymbiotic growth phase, which leads to intense hyphal ramification (or branching) in the vicinity of the root (Giovannetti et al., 1993;B...
Summary• The arbuscular mycorrhizal symbiosis is arguably the most ecologically important eukaryotic symbiosis, yet it is poorly understood at the molecular level. To provide novel insights into the molecular basis of symbiosis-associated traits, we report the first genome-wide analysis of the transcriptome from Glomus intraradices DAOM 197198.• We generated a set of 25 906 nonredundant virtual transcripts (NRVTs) transcribed in germinated spores, extraradical mycelium and symbiotic roots using Sanger and 454 sequencing. NRVTs were used to construct an oligoarray for investigating gene expression.• We identified transcripts coding for the meiotic recombination machinery, as well as meiosis-specific proteins, suggesting that the lack of a known sexual cycle in G. intraradices is not a result of major deletions of genes essential for sexual reproduction and meiosis. Induced expression of genes encoding membrane transporters and small secreted proteins in intraradical mycelium, together with the lack of expression of hydrolytic enzymes acting on plant cell wall polysaccharides, are all features of G. intraradices that are shared with ectomycorrhizal symbionts and obligate biotrophic pathogens.• Our results illuminate the genetic basis of symbiosis-related traits of the most ancient lineage of plant biotrophs, advancing future research on these agriculturally and ecologically important symbionts.*These authors contributed equally to this work.
Summary Arbuscular mycorrhizas (AMs) contribute significantly to soil nutrient uptake in plants. As a consequence of the fungal colonization and of the deep reorganization shown by arbusculated cells, important impacts on root transcriptome are expected. An Affymetrix GeneChip with 50 000 probe‐sets and real‐time RT‐PCR allowed us to detect transcriptional changes triggered in Lotus japonicus by the AM fungus Gigaspora margarita, when arbuscules are at their maximum (28 d postinoculation (dpi)). An early time (4 dpi) was selected to differentiate genes potentially involved in signaling and/or in colonization of outer tissues. A large number (75 out of 558) of mycorrhiza‐induced genes code for proteins involved in protein turnover, membrane dynamics and cell wall synthesis, while many others are involved in transport (47) or transcription (24). Induction of a subset (24 genes) of these was tested and confirmed by qRT‐PCR, and transcript location in arbusculated cells was demonstrated for seven genes using laser‐dissected cells. When compared with previously published papers, the transcript profiles indicate the presence of a core set of responsive genes (25) that seem to be conserved irrespective of the symbiotic partner identity.
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