Abstract
Arbuscular mycorrhizas are widespread in land plants including liverworts, some of the closest living relatives of the first plants to colonize land 500 million years ago (MYA). Previous investigations reported near-exclusive colonization of liverworts by the most recently evolved arbuscular mycorrhizal fungi, the Glomeraceae, indicating a recent acquisition from flowering plants at odds with the widely held notion that arbuscular mycorrhizal-like associations in liverworts represent the ancestral symbiotic condition in land plants. We performed an analysis of symbiotic fungi in 674 globally collected liverworts using molecular phylogenetics and electron microscopy. Here, we show every order of arbuscular mycorrhizal fungi colonizes early-diverging liverworts, with non-Glomeraceae being at least 10 times more common than in flowering plants. Arbuscular mycorrhizal fungi in liverworts and other ancient plant lineages (hornworts, lycopods, and ferns) were delimited into 58 taxa and 36 singletons, of which at least 43 are novel and specific to liverworts. The discovery that early plant lineages are colonized by early-diverging fungi supports the hypothesis that arbuscular mycorrhizas are an ancestral symbiosis for all land plants.
Highlights
Arbuscular mycorrhizas (AM) are the most widespread land plant –fungus mutualisms; members of the AM fungal lineage (Glomeromycotina) colonize at least 72% of flowering plant species [1]
Some of the closest living relatives of the first land plants, contrary to previous reports, are more frequently associated with ancient lineages of arbuscular mycorrhizal fungi (AMF) than flowering plants and harbour diverse, newly described and specific symbionts
Our study shows for the first time that liverworts can be colonized by the full diversity of Glomeromycotina and are not limited to a narrow set
Summary
Arbuscular mycorrhizas (AM) are the most widespread land plant –fungus mutualisms; members of the AM fungal lineage (Glomeromycotina) colonize at least 72% of flowering plant species [1]. The exclusive or near-exclusive colonization by Glomeraceae (a family that evolved after plant terrestrialization) reported for earlydiverging plants suggests that liverwort AM-like associations do not represent the symbiotic status of the first land plants and instead symbiosis is derived, having host-shifted from flowering plants [27]. Given the key phylogenetic position of liverworts in the plant tree of life, very few studies have attempted to identify molecularly the AMF associated with this group, and only a handful of species have been analysed [15,16,26] To address this striking paucity of data, we performed a molecular analysis of the AM-like associations of globally collected liverwort samples to test the hypothesis that liverworts exhibit specificity towards Glomeraceae, as suggested by previous studies. Our discovery of a predominance of the more ancient, non-Glomeraceae AMF families in these plants when compared to flowering plants supports 2 the notion that liverwort AM-like associations are not derived but ancient and representative of an ancestral symbiotic condition in land plants
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