Foliar mycoendophytome of an endemic plant of the Mediterranean biome (Myrtus communis) reveals the dominance of basidiomycete woody saprotrophs

Abstract

The true myrtle, Myrtus communis, is a small perennial evergreen tree that occurs in Europe, Africa, and Asia with a circum-Mediterranean geographic distribution. Unfortunately, the Mediterranean Forests, where M. communis occurs, are critically endangered and are currently restricted to small fragmented areas in protected conservation units. In the present work, we performed, for the first time, a metabarcoding study on the spatial variation of fungal community structure in the foliar endophytome of this endemic plant of the Mediterranean biome, using bipartite network analysis as a model. The local bipartite network of Myrtus communis individuals and their foliar endophytic fungi is very low connected, with low nestedness, and moderately high specialization and modularity. Similar network patterns were also retrieved in both culture-dependent and amplicon metagenomics of foliar endophytes in distinct arboreal hosts in varied biomes. Furthermore, the majority of putative fungal endophytes species were basidiomycete woody saprotrophs of the orders Polyporales, Agaricales, and Hymenochaetales. Altogether, these findings suggest a possible adaptation of these wood-decaying fungi to cope with moisture limitation and spatial scarcity of their primary substrate (dead wood), which are totally consistent with the predictions of the viaphytism hypothesis that wood-decomposing fungi inhabit the internal leaf tissue of forest trees in order to enhance dispersal to substrates on the forest floor, by using leaves as vectors and as refugia, during periods of environmental stress.

Why Are There So Few Basidiomycota and Basal Fungi as Endophytes? A Review

“…Abdel-Wahab et al [40] also used metagenomics to determine the fungal diversity from five decaying leaf samples of Halophila stipulacea and found that the percentage occurrence of Basidiomycota ranged from 37.2 to 51.6%. Interestingly, the highest percentage of basidiomycetous endophytes was reported from leaves of Myrtus communis by Vas et al [45]: out of 44 OTUs generated by sequencing, 37 OTUs belonged to 12 orders of Basidiomycota (84% occurrence). Note: ND = No data.…”

“…Table 2 documents endophytic Basidiomycota from a review of 25 selected publications from a wide range of host plants and plant parts, and from temperate to tropical geographical locations, with identifications based on morphology or a combination of morphology and sequence data, yielding 85 species in 46 genera. Two publications document the detection of endophytes in Myrtus communis and decaying leaves of Halophila stipulacea by high-throughput sequencing (metagenomics) (culture-independent method, CID) [40,45], while 23 publications identify the endophytes by isolation and morphological procedures (culture-dependent method, CD).…”

“…Basidiomycetous endophytes numbers are expressed as a percentage of the total number isolated and varied from 0.4 to 84% depending on the host plant: leaves of Vitis vinifera yielded few basidiomycetous endophytes (0.4%) [49], while the highest number was from leaves of Myrtus communis (84%) [45]. Generally, basidiomycetous endophytes were low at 2.1%, in comparison to those of Ascomycota, in leaves, stems and roots of Nicotiana benthamiana, N. occidentalis, and N. simulans [56].…”

“…Schizophyllum commune was the most recurring species, occurring on four host plants, while the genera Ceratobasidium and Trametes were listed three times in various host plants. Ceratobasidium species were recorded from the root of Anacamptis morio [44], the leaf of Myrtus communis [45], and the grass Holcus lanatus [51], with Trametes species reported from M. communis [45], Hevea brasilienesis [50], and Colobanthus quitensis [29]. Seven Basidiomycota genera were listed twice as endophytes: Bjerkandera adusta [28,43], Ganoderma sp.…”

Applying molecular and genetic methods to trees and their fungal communities

“…In a broader interpretation of a lifestyle that has recently been termed viaphytism (Nelson et al 2020 ), certain decomposing fungi can use as endophytes organs of the plant host as a refuge to overcome periods of own environmental stress. For example, such species may exist as temporary foliar endophytes to then enhance their own spread by leaf and needle fall to the forest floor providing more versatile woody substrates to them for saprotrophic hyphal growth (Nelson et al 2020 ; Vaz et al 2020 ). Functions of still other endophytes remain elusive (Gehring et al 2020 ; Rodriguez et al 2009 ), or may they simply be commensals nurtured by a host without recognizable impacts on their feeder (Langer et al 2021 ; Terhonen et al 2019 ; Zanne et al 2020 )?…”