Foliar fungi of the enigmatic desert plant Welwitschia mirabilis show little adaptation to their unique host plant

Michael J Wingfield,Don A Cowan,Bernard Slippers,Martin Kemler

doi:10.17159/sajs.2021/7666

Michael J Wingfield, Don A Cowan + Show 2 more

Open Access

https://doi.org/10.17159/sajs.2021/7666

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Abstract

Foliar fungi, especially endophytic fungi, constitute an important part of the microbiome of plants. Yet little is known about the composition of these communities. In this study, we isolated fungi from leaf tissues of the desert plant Welwitschia mirabilis to determine the culturable diversity of the foliar fungal community. The isolated fungal taxa, which grouped into 17 distinct lineages, were identified by sequencing elongation factor 1 alpha, beta-tubulin 1, beta-tubulin 2 and the internal transcribed spacer region. The culturable community was mainly composed of cosmopolitan fungal genera despite the unique taxonomic position of the plant and its geographic isolation. To test for endemism in two of the common fungal genera, Alternaria and Aureobasidium, we built haplotype networks using a global data set. Even this broad data set showed little evidence for specialisation within this unique host or its geographical location. The data suggest that the culturable members of communities of leaf-associated fungi in habitats with little plant coverage, such as the Namib Desert, are mainly established by long-distance aerially distributed fungal inocula and few of these taxa co-evolve with the host within the habitat.Significance:  The culturable members of fungal communities associated with an ecological and evolutionary isolated plant have not co-speciated with their hosts, but to a large extent are composed of globally distributed fungal species. Harsh environmental conditions and the geographic isolation of host plants seem to favour ubiquitous fungal species over more specialist fungal species.  Open data sets*: https://www.ncbi.nlm.nih.gov/genbank *see accession numbers in text

Highlights

Fungi and plants have a long history of co-evolution and plant–fungal interactions are thought to have been essential in the establishment of plants in terrestrial environments
The foliar fungi associated with the leaves of W. mirabilis that could be isolated and grown in culture belonged to either the Ascomycota or Basidiomycota (Supplementary table 1)
Fungal specimens isolated from Welwitschia that fell within the genera Alternaria and Aureobasidium did not cluster according to their origin but were intermingled with sequences from other geographic origins

Summary

Introduction

Fungi and plants have a long history of co-evolution and plant–fungal interactions are thought to have been essential in the establishment of plants in terrestrial environments. Structures of endophytic fungi (i.e. microorganisms that in part or during their whole life cycle colonise plant tissues without visible symptoms3) in prostrate axes have been described from as early as 400 Ma.[4] leaf-associated endophytes are known from the 300 Ma Carboniferous era.[5] These studies show that, despite the unknown interaction type between host and fungus, aboveground organs of plants, the so-called phyllosphere, have served as a suitable habitat for fungi for a long time. Extant phyllosphere-associated fungi including endophytes and epiphytes (i.e. fungi that grow on the surface of plants) mostly show no visible impact on their host under favourable conditions or even enhance plant performance. Most likely similar mechanisms apply for epiphytes.[17,18]

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