Abstract
Like the majority of land plants, liverworts regularly form intimate symbioses with arbuscular mycorrhizal fungi (Glomeromycotina). Recent phylogenetic and physiological studies report that they also form intimate symbioses with Mucoromycotina fungi and that some of these, like those involving Glomeromycotina, represent nutritional mutualisms. To compare these symbioses, we carried out a global analysis of Mucoromycotina fungi in liverworts and other plants using species delimitation, ancestral reconstruction, and network analyses. We found that Mucoromycotina are more common and diverse symbionts of liverworts than previously thought, globally distributed, ancestral, and often co-occur with Glomeromycotina within plants. However, our results also suggest that the associations formed by Mucoromycotina fungi are fundamentally different because, unlike Glomeromycotina, they may have evolved multiple times and their symbiotic networks are un-nested (i.e., not forming nested subsets of species). We infer that the global Mucoromycotina symbiosis is evolutionarily and ecologically distinctive.
Highlights
To what extent did fungi influence the conquest of land and greening of the planet by plants some 500 million years ago? This remains one of the most critical questions in land plant evolution ever since the idea of fungal-assisted plant terrestrialization was first proposed over 40 years ago Electronic supplementary material The online version of this article contains supplementary material, which is available to authorized users.(Pirozynski and Malloch 1975)
Mucoromycotina were detected in 24% of the 674 liverwort samples and were found in sixteen countries and all six continents investigated
Comparing our results with those of a worldwide analysis of Glomeromycotina in these plants (Rimington et al 2018) indicates that many liverwort species can be colonized by both fungal lineages (Table 1), often simultaneously within the same plant individual
Summary
The fungi provided early rootless plants with nutrients and water in exchange for photosynthesis-derived carbohydrates. Following terrestrialization, this relationship evolved into mycorrhizal symbioses, present in more than 85% of plants (Brundrett and Tedersoo 2018). Though the order of divergence of these groups remains under active debate (Puttick et al 2018; Rensing 2018; de Sousa et al 2019), bryophytes are generally regarded as some of the earliest terrestrial plants (Renzaglia et al 2018) and have provided invaluable insights into the origin and evolution of key land plant innovations including mycorrhizas (e.g., Wang et al 2010; Field et al 2015a, b, 2016, 2019). Glomeromycotina colonization in liverworts (Ligrone et al 2007), together with the dominance of AM in extant land plant lineages, and their putative occurrence in fossils (Taylor et al 1995) have long supported the paradigm that
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