Abstract
The pine mushroom (Tricholoma matsutake; Agaricales, Tricholomataceae) is an ectomycorrhizal fungus that produces a commercially valuable, edible mushrooms. Attempts to artificially cultivate T. matsutake has so far been unsuccessful. One method used to induce T. matsutake to produce fruiting bodies of in the wild is shiro (mycelial aggregations of T. matsutake) transplantation. In vitro ectomycorrhization of T. matsutake with seedlings of Pinus densiflora has been successful, but field trials showed limited production of fruiting bodies. Few studies have been done to test what happens after transplantation in the wild, whether T. matsutake persists on the pine seedling roots or gets replaced by other fungi. Here, we investigated the composition and the interaction of the root fungal microbiome of P. densiflora seedlings inoculated with T. matsutake over a 3 year period after field transplantation, using high-throughput sequencing. We found a decline of T. matsutake colonization on pine roots and succession of mycorrhizal fungi as P. densiflora seedlings grew. Early on, roots were colonized by fast-growing, saprotrophic Ascomycota, then later replaced by early stage ectomycorrhiza such as Wilcoxina. At the end, more competitive Suillus species dominated the host roots. Most of the major OTUs had negative or neutral correlation with T. matsutake, but several saprotrophic/plant pathogenic/mycoparasitic species in genera Fusarium, Oidiodendron, and Trichoderma had positive correlation with T. matsutake. Four keystone species were identified during succession; two species (Fusarium oxysporum, and F. trincintum) had a positive correlation with T. matsutake, while the other two had a negative correlation (Suillus granulatus, Cylindrocarpon pauciseptatum). These findings have important implications for further studies on the artificial cultivation of T. matsutake.
Highlights
Ectomycorrhizal fungi are one of the most common forms of plant-fungal root symbioses in woody plants (Brundrett, 2009; Van Der Heijden et al, 2015), and improve nutrition and stress resistance of the host plant (Smith and Read, 2010; Berendsen et al, 2012; Van Der Heijden et al, 2015)
The number of operational taxonomic units (OTUs) significantly increased with the age of P. densiflora seedlings, from 63 OTUs found in M03 to 487 OTUs in M38 (Figure 1)
The relative abundance of T. matsutake drastically decreased after the transplantation to greenhouse (M03 to M10; Figure 2C and Table 1), but T. matsutake was still detected in some samples (15/16 in M10; 8/16 in M17; 4/16 in M24 and M31; 2/16 in M38; Table 1)
Summary
Ectomycorrhizal fungi are one of the most common forms of plant-fungal root symbioses in woody plants (Brundrett, 2009; Van Der Heijden et al, 2015), and improve nutrition and stress resistance of the host plant (Smith and Read, 2010; Berendsen et al, 2012; Van Der Heijden et al, 2015). Succession of the mycorrhizal community was reported in several host plants (Twieg et al, 2007) This phenomenon occurs in mature trees, and in seedlings, where the dominant ectomycorrhizal taxa can change (Matsuda et al, 2009; Obase et al, 2009). Arrival sequence of ectomycorrhizal fungi often influences colonization at early stages, with negative consequences for later colonizers (Alford and Wilbur, 1985; Shorrocks and Bingley, 1994). This phenomenon is called the priority effect, and has been reported in the early stage of interaction between ectomycorrhizal fungi and pine seedlings (Kennedy and Bruns, 2005; Fukumi, 2015)
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