Mycorrhiza (2020) 30:23–49 https://doi.org/10.1007/s00572-020-00938-y REVIEW The distribution and evolution of fungal symbioses in ancient lineages of land plants William R. Rimington1,2,3 & Jeffrey G. Duckett2 & Katie J. Field4 & Martin I. Bidartondo1,3 & Silvia Pressel2 Received: 15 November 2019 /Accepted: 5 February 2020 /Published online: 4 March 2020 # The Author(s) 2020 Abstract An accurate understanding of the diversity and distribution of fungal symbioses in land plants is essential for mycorrhizal research. Here we update the seminal work of Wang and Qiu (Mycorrhiza 16:299-363, 2006) with a long-overdue focus on early-diverging land plant lineages, which were considerably under-represented in their survey, by examining the published literature to compile data on the status of fungal symbioses in liverworts, hornworts and lycophytes. Our survey combines data from 84 publications, including recent, post-2006, reports of Mucoromycotina associations in these lineages, to produce a list of at least 591 species with known fungal symbiosis status, 180 of which were included in Wang and Qiu (Mycorrhiza 16:299-363, 2006). Using this up-to-date compilation, we estimate that fewer than 30% of liverwort species engage in symbiosis with fungi belonging to all three mycorrhizal phyla, Mucoromycota, Basidiomycota and Ascomycota, with the last being the most wide- spread (17%). Fungal symbioses in hornworts (78%) and lycophytes (up to 100%) appear to be more common but involve only members of the two Mucoromycota subphyla Mucoromycotina and Glomeromycotina, with Glomeromycotina prevailing in both plant groups. Our fungal symbiosis occurrence estimates are considerably more conservative than those published previ- ously, but they too may represent overestimates due to currently unavoidable assumptions. Keywords Arbuscular mycorrhizas . Ericoid mycorrhizas . Mucoromycota . Hornworts . Liverworts . Lycophytes Introduction termed mycorrhizas, with soil fungi (Brundrett and Tedersoo 2018). This percentage is only an estimate because investigat- Fungi colonize plants and interact with their living tissues in a ing every plant species is neither practical nor currently pos- variety of ways; these interactions can be detrimental (parasit- sible given that not all species are known and ca. 2000 new ic), neutral (symptomless) or beneficial (mutualistic) to the vascular plants species are described each year (Pimm and host plant. More than 85% of vascular plant species are con- Raven 2017). For the most part, fungal symbiosis occurrence sidered to form mutually beneficial symbioses in their roots, rate estimates are lacking for early-diverging plant lineages as little effort has been directed towards compiling the data re- Electronic supplementary material The online version of this article quired to allow these estimations to be made. This also reflects (https://doi.org/10.1007/s00572-020-00938-y) contains supplementary an overall paucity of data available on these groups, including material, which is available to authorized users. information on the type of interaction formed, i.e. whether the interaction is mycorrhizal or mycorrhizal-like in plants such as * Silvia Pressel liverworts and hornworts that lack true roots. However, in the [email protected] last decade, there has been an increased research focus on the 1 Department of Life Sciences, Imperial College London, diversity and distribution of fungal associations in liverworts, London SW7 2AZ, UK hornworts and lycophytes, largely driven by the discovery of 2 Department of Life Sciences, Algae, Fungi and Plants Division, Mucoromycotina fungi in association with these plants Natural History Museum, London, London SW7 5BD, UK (Bidartondo et al. 2011;Desiròetal.2013; Rimington et al. 3 Comparative Plant and Fungal Biology, Royal Botanic Gardens, 2015) and the demonstration that at least some of these asso- Kew, Richmond TW9 3DS, UK ciations are mycorrhizal or mycorrhizal-like—i.e. those be- 4 Centre for Plant Sciences, Faculty of Biological Sciences, University tween lycophytes and Mucoromycotina (Hoysted et al. of Leeds, Leeds LS2 9JT, UK 2019); between liverworts and Glomeromycotina (Field 24 Mycorrhiza (2020) 30:23–49 et al. 2012), Mucoromycotina (Field et al. 2015)and epiphytic or endophytic in the dead hyaline cells in Glomeromycotina and Mucoromycotina together (Field Sphagnum leaves (Kostka et al. 2016; Warshan et al. 2017). et al. 2016b); and between liverworts and Ascomycota Recently, it has been shown that lycophytes also form as- (Kowal et al. 2018). We address this lacuna by compiling sociations with Mucoromycotina and Glomeromycotina fungi published fungal symbiosis status for these early-diverging (Rimington et al. 2015), with emerging evidence of carbon- plant lineages with the caveat that some of the reported sym- for-nutrient exchanges between these early-diverging vascular bioses, e.g. those in hornworts, are considered such on the plants and their Mucoromycotina symbionts (Hoysted et al. basis of morphology and/or involvement of fungi known to 2019). A better understanding of fungal associations in be mycorrhizal with other plant lineages but are yet to be lycophytes is important when considering the early evolution confirmed experimentally. A comprehensive list of which of land plant-fungus symbiosis. Lycophytes, which comprise plant species enter into fungal symbioses and with which fun- ca. 1360 species (Hassler and Schmitt 2018), are the earliest gi not only serves as a useful resource for future studies but branching lineage of vascular plants (tracheophytes) and rep- also provides insight into the origins and distribution of these resent the transition from non-vascular to seed plants (Kenrick relationships and how they evolved across plant lineages and Crane 1997). They are of particular importance because (Wang and Qiu 2006). This is particularly pertinent today as putative transitional ‘pre-vascular’ plants, including Rhynie recent studies are finally providing much improved resolution Chert fossils such as Aglaophyton, are all extinct (Remy on the phylogenetic relationships among the earliest-diverging et al. 1994). As such, extant lycophytes are considered the bryophytes (liverworts, mosses and hornworts) and vascular best modern analogues for the first vascular plants (Kenrick plants, which have been contested for decades (e.g. Puttick and Crane 1997). et al. 2018; de Sousa et al. 2019). Within bryophytes, mosses Lists detailing the fungal symbiosis status of plants have are the only group not known to harbour symbiotic fungi in been published for many years; for example, the first list of their living cells (Pressel et al. 2010). On the other hand, fungal symbiosis in liverworts was produced 70 years ago liverworts engage in remarkably diverse symbioses with (Stahl 1949). Such lists require regular updating as the number Mucoromycotina, Glomeromycotina, Ascomycota or of studies increases and so does our knowledge of the diver- Basidiomycota fungi (Pressel et al. 2010; Bidartondo et al. sity of symbioses within and across plant clades. Earlier com- 2011). Hornworts appear intermediate between liverworts pilations usually focused on a local scale and only on certain, and mosses by forming associations with Mucoromycotina almost invariably vascular, plant groups (Harley and Harley and Glomeromycotina but not with members of the Dikarya 1987). It was not until 2006 that a worldwide literature survey (Desirò et al. 2013). Both liverworts and hornworts can also of fungal symbioses across all land plant groups was per- be fungus-free (non-symbiotic). Liverworts have undergone a formed (Wang and Qiu 2006). This landmark publication by number of gains and losses of symbiosis during their evolu- Wang and Qiu (2006) captured the status of over 3000 species tion; the early-diverging groups Haplomitriopsida, (143 of which were bryophytes) and, unsurprisingly, has been Marchantiopsida and Pelliidae are symbiotic with highly influential ever since. In the 13 years since its publica- Mucoromycotina and/or Glomeromycotina (Rimington et al. tion, this paper has been one of the most cited on mycorrhizas 2019) while more derived lineages associate with (over 1500 citations as of January 2020) and has provided Basidiomycota (Metzgeriidae, Jungermanniidae) and important insights on the evolution of mycorrhizas; for exam- Ascomycota (Jungermanniidae) (Pressel et al. 2010). ple, evidence that arbuscular mycorrhizas (AM) are found Ascomycota and Basidiomycota are both members of the sub- throughout the land plant phylogeny has been used as a key kingdom Dikarya, the latest diverging fungal lineage (Hibbett argument for Glomeromycotina symbiosis being an ancestral et al. 2007). Molecular analysis has indicated that the trait of land plants (Rimington et al. 2018). However, Wang Basidiomycota symbionts of liverworts are members of the and Qiu’ssurvey(WangandQiu2006) is now considerably genera Serendipita (Sebacina)andTulasnella (Bidartondo outdated, especially with regard to early-diverging plant line- and Duckett 2010), while Ascomycota symbioses are formed ages. Since its publication there has been much interest in the by Hyaloscypha (Pezoloma or Rhizoscyphus) ericae (Upson diverse fungal symbioses of early-diverging plants (e.g. et al. 2007;Fehreretal.2019). Ligrone et al. 2007;DuckettandLigrone2008;Bidartondo Hornworts and some liverworts also form endosymbioses and Duckett 2010; Pressel et al. 2010; Desirò et al. 2013; with cyanobacteria (Nostoc sp.) (Adams and Duggan