Double lives: transfer of fungal endophytes from leaves to woody substrates

Abstract

Fungal endophytes are a ubiquitous feature of plants, yet for many fungi the benefits of endophytism are still unknown. The Foraging Ascomycete (FA) hypothesis proposes that saprotrophic fungi can utilize leaves both as dispersal vehicles and as resource havens during times of scarcity. The presence of saprotrophs in leaf endophyte communities has been previously observed but their ability to transfer to non-foliar saprobic substrates has not been well investigated. To assess this ability, we conducted a culture study by placing surface-sterilized leaves from a single tropical angiosperm tree (Nectandra lineatifolia) directly onto sterile wood fragments and incubating them for 6 weeks. Fungi from the wood were subsequently isolated in culture and identified to the genus level by ITS sequences or morphology. Four-hundred and seventy-seven fungal isolates comprising 24 taxa were cultured from the wood. Of these, 70.8% of taxa (82.3% of isolates) belong to saprotrophic genera according to the FUNGuild database. Furthermore, 27% of OTUs (6% of isolates) were basidiomycetes, an unusually high proportion compared to typical endophyte communities. Xylaria flabelliformis, although absent in our original isolations, formed anamorphic fruiting structures on the woody substrates. We introduce the term viaphyte (literally, “by way of plant”) to refer to fungi that undergo an interim stage as leaf endophytes and, after leaf senescence, colonize other woody substrates via hyphal growth. Our results support the FA hypothesis and suggest that viaphytism may play a significant role in fungal dispersal.

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

“…Moreover, most of the putative endophytic fungi species were basidiomycete woody saprotrophs of the orders Polyporales, Agaricales and Hymenochaetales. Taking together, our findings corroborate the viaphytism hypothesis (Nelson et al, 2020;Thomas, Vandegrift & Roy, 2020), which states that saprotrophic fungi (especially the wood decayers) can utilize leaves both as dispersal vehicles and as resource during times of scarcity (Nelson et al, 2020). Furthermore, as the viaphytism hypothesis have been tested only in trees in humid biomes (rainforests) without any marked seasonal hydric deficiency (Thomas et al, 2016(Thomas et al, , 2019, our study not only corroborate the viaphytism hypothesis but also extended it to a typical and endemic tree in Mediterranean biome, which is characterized by a dry and hot summer season that is very unfavorable to wood-decomposing fungi.…”

“…Therefore, this cycle can really be a very common and still previously ignored ecological process in forests, which may have far-reaching implications for whole forest health ( Thomas, Vandegrift & Roy, 2020 ). Thus, the dominance of basidiomycete woody saprothrophs in the foliar mycoendophytome of Myrtus communis in Southwestern Mediterranean sclerophyllous forest may be 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 viaphytism hypothesis ( Nelson et al, 2020 ; Thomas, Vandegrift & Roy, 2020 ).…”

“…This hypothesis states that, for wood-degrading fungi, endophytism is a life-history strategy to span the scarcity of dead wood substrates and stressful environmental conditions, such as hydric restriction, in both time and space ( Carroll, 1999 ; Thomas et al, 2016 ). Despite this FA hypothesis having been initially suggested for Ascomycota ( Carroll, 1999 ), in fact, it can be applied to any endophytic fungus regardless of its taxonomic assignment, and the term viaphytism has been recently proposed ( Nelson et al, 2020 ). The Viaphytism hypothesis states that many fungi may be in a continuous and cyclical flux between life stages as endophytes in the forest canopy and as wood-decomposing fungi on the forest floor ( Thomas, Vandegrift & Roy, 2020 ).…”

“…Additionally, the Mediterranean Forests, Woodlands and Scrubs, where M. communis is a bioindicator species, is one of understudied biomes of the world for fungal endophytes. Assuming the premises that (i) foliar endophytism may be an efficient strategy for saprotrophic fungi both as dispersal vehicle and as resource source during times of scarcity ( Nelson et al, 2020 ) and (ii) a significant proportion of fungal endophytes of trees are saprotrophs ( Parfitt et al, 2010 ), we hypothesize that, in biomes seasonally subjected to hydric deficiency, such as the Mediterranean biome, a high relative incidence and abundance of saprotrophic fungi will be inhabiting tree hosts when compared to pathotrophic and symbiothrophic guilds. Thus, in the current work, we performed, for the first time, a study on the spatial variation of fungal community structure in the foliar endophytome of this endemic plant of the Mediterranean biome, and their probable ecological functions in distinct individuals of M. communis , using bipartite network analysis as a model.…”

Seed Banks as Incidental Fungi Banks: Fungal Endophyte Diversity in Stored Seeds of Banana Wild Relatives

“…Despite their ubiquity, the endophytic lifestyle remains somewhat of a mystery. While there are aforementioned examples of mutualistic endophytes found only to benefit the plant host, other fungi described as endophytes are found to be latent pathogens or decomposers (saprotrophs) ( Slippers and Wingfield, 2007 ; Promputtha et al, 2010 ; Delaye et al, 2013 ; Nelson et al, 2020 ). This concept–that the term endophyte represents a range of functional roles within the plant host–has been referred to as the endophytic continuum ( Schulz and Boyle, 2005 ).…”