Evolutionary history of mycorrhizal symbioses and global host plant diversity

I. Introduction

There are four main types of mycorrhizas based on the criteria of morphological differentiation of root tissues and host plant lineages: arbuscular mycorrhizas (AM), ectomycorrhizas (EcM), ericoid mycorrhiza (ErM) and orchid mycorrhizas (OrM) (see descriptions in Box 1). Mycorrhizal associations have key roles in maintaining plant productivity in natural and agricultural habitats, and are the key sources of energy for many fungal taxonomic groups, yet there are major gaps in knowledge about the evolutionary history of these partnerships. Here we summarize the global diversity of mycorrhizal and nonmycorrhizal (NM) plants, provide regional host plant summaries and briefly address data quality issues in mycorrhizal lists and their consequences. Finally, we provide a brief update on the evolutionary history of mycorrhizal associations, based on information published in the book ‘Biogeography of mycorrhizal symbioses’ (Tedersoo, 2017a) and other sources.

II. Mycorrhizal plant diversity at global and local scales

A phylogenetic approach for summarizing mycorrhizal host plant diversity works well because the majority of plant species belong to genera, families or orders with consistent mycorrhizal status, indicating strong phylogenetic conservatism of the mycorrhizal trait (Brundrett, 2009; Maherali et al., 2016). However, some families are more complex due to specialized or multifunctional roots (e.g. AM and EcM). Fig. 1 illustrates revised estimates of the diversity of mycorrhizal and NM plants, based on 135 years of published information and recently available large-scale plant phylogeny (Zanne et al., 2014) and mycorrhizal data, which includes extensive coverage of both temperate and tropical ecosystems (Brundrett, 2009; Tedersoo, 2017a). This analysis confirms the overall importance of AM, which occurs in 72% of flowering plant species, with ≥2% EcM, 1.5% ErM, 10% OrM and 7% inconsistent AM (NM–AM); 8% remain NM. These numbers are similar for all vascular plants, with 71% species being AM and 2.2% EcM (Brundrett, 2017b). In ferns, c. 67% of species are AM (Lehnert et al., 2017) and c. 25% of bryophytes are mycorrhizal, mostly with AM; however, mosses, the largest group of bryophytes, are normally NM (Davey & Currah, 2006; Pressel et al., 2010).

The general consistency in mycorrhiza development within most plant families allows phylogenetic information about mycorrhizal status to be extended to produce regional-scale estimates of host and nonhost plant diversity (Fig. 2). These comparisons reveal that most plant communities are dominated by mycorrhizal plants in most ecosystems, EcM plants are rare or absent in many tropical habitats, whereas NM plants are more common and diverse in some arid and degraded habitats, as well as arctic and alpine regions (Brundrett, 2009; Gerz et al., 2016; Swaty et al., 2016; Soudzilovskaia et al., 2017). In particular, plants with NM cluster roots have centres of diversity in extremely poor soils in Mediterranean habitats of Western Australia and South Africa (Lambers et al., 2010). It is also remarkable that Australia is a global centre of diversity for plants with EcM roots, NM roots or carnivorous nutrition, with c. 33%, c. 15% and c. 25% of global species, respectively (Brundrett, 2017a). Furthermore, Australia contributes to 17% of diversity of ErM plant species and 10% of plant parasites.

Ectomycorrhizas are the most frequently acquired mycorrhizal associations due to multiple independent gains and some losses of symbiosis (Tedersoo & Brundrett, 2017). We resolved conflicting information and missing data for many EcM plant taxa, resulting in a revised estimate of 6000–7000 EcM plant species, with a further 1500–2500 species that belong to Australian groups with complex roots in which EcM occurs in some species but not others, such as Myrtoideae (Myrtaceae) Acacia (Fabaceae), Mirbelieae (Fabaceae) and Casuarinaceae (Brundrett, 2017b; Tedersoo & Brundrett, 2017). These groups include many species with both EcM and AM roots and require further investigation (Fig. 3). Our maximum estimate includes 335 ectomycorrhizal plant genera (8500 species) in 30 monophyletic lineages. We also identified a further 22 plant genera (76 species) that may also be EcM due to phylogenetic sister relationships to known EcM hosts, but require further investigation (Tedersoo & Brundrett, 2017).

Rapid phylogenetic radiation has occurred in some NM plant groups that have secondarily lost their mycorrhiza-forming capacity permanently, or intermittently depending on habitat and co-occurring plants (NM–AM). We estimate that there are 30–50 separate evolutionary origins of NM or NM–AM plants, including several occasions within some families (Brundrett, 2017b). Many NM and NM–AM plants are habitat specialists that grow in environments where plant productivity is limited by soil or climatic conditions, or nutritional specialists such as carnivores, parasites and cluster-rooted species, where mycorrhizas are redundant (Fig. 1). There also is an over-representation of NM plants in waterlogged, cold and saline soils, as well as in epiphytic, freshwater, marine and disturbed habitats (Fig. 1). For example, 15 of the top 17 weed plant families listed by Daehler (1998) have NM roots. By contrast, mycorrhizal plants usually dominate most mid- and late-successional habitats (Fig. 2).

III. Mycorrhizal evolution in plants: a brief update

Switching from AM to NM or AM to EcM roots and reversal of carbon flow in mycoheterotrophic associations are the three most common trends in mycorrhizal evolution (Box 1; Fig. 3). Additionally, potential losses of EcM associations occur in the Fagales, Fabales, Asterales and Myrtales that may be attributed to the evolution of association with nitrogen-fixing bacteria, of shrubby or herbaceous life forms or following the shift to wetland habitats (Tedersoo & Brundrett, 2017).

Taking the accumulated information together, we recognize three waves of mycorrhizal evolution which resulted in new nutritional mechanisms in plants (Fig. 4). The second and third waves consist of multiple origins of mycorrhizal (especially EcM) and NM plant lineages and extend over a considerable time period.

The first wave represents the origin of AM associations in early terrestrial plants over 450 Myr ago (Ma) (Taylor & Osborn, 1996; Brundrett, 2002). The fossil record for land plants starts in the Ordovician at c. 470 Ma, but interpreting these early clues is complicated due to major gaps in the fossil record and difficulties in linking early cryptosporic land plants to modern lineages (Wellman, 2014). The first well-preserved fossils of mycorrhizal rhizomes originate from the Devonian Rhynie chert (407 Ma) and show remarkably similar mycorrhizal and spore morphology to modern equivalents (Taylor & Osborn, 1996; Krings et al., 2007), but the first AM fungus-like spores have been detected in substrates 50 Myr earlier from the Ordovician (Pirozynski & Dalpé, 1989; Redecker et al., 2000). Due to limited evidence from the first 60 Myr of life on land, it is unclear if mycorrhizal fungi arrived with the first plants or when plant complexity rapidly increased in the Silurian. This is further complicated by the fact that some plant symbiosis genes pre-date land plants (Delaux et al., 2015; Martin et al., 2017). Both fossil evidence and molecular studies support a single origin for AM (Brundrett, 2002; Bravo et al., 2016). For example, genomic studies have revealed common mechanisms for signalling and regulation of mycorrhizal associations that are shared with nitrogen-fixing associations and the common loss of symbiotic genes in NM plants (Delaux et al., 2015; Bravo et al., 2016; Kamel et al., 2017).

Reduced mycorrhizal dependency may have evolved in some ferns and Equisetales (horsetails) with fine roots with long root hairs. However, reduced AM colonization in ferns is primarily correlated with their occupation of epiphytic habitats during their rapid radiation in the Cenozoic (Schuettpelz & Pryer, 2009; Lehnert et al., 2017). The NM bryophyte lineages are also ancient, but some modern bryophytes have relationships with AM or more recently evolved fungi (Box 1).

As shown in Fig. 4, the second major wave of mycorrhizal evolution occurred in the Cretaceous with the origins of the Orchidaceae, Ericaceae and multiple families with EcM or NM roots, as well as parasitic plants carnivorous plants and nitrogen-fixing symbioses (Brundrett, 2002, 2017b; Raven & Andrews, 2010; Li et al., 2015). Although the EcM Pinaceae evolved in the Late Triassic or Jurassic (Zanne et al., 2014; Falcon-Lang et al., 2016; Smith et al., 2017), most of the remaining independent origins of nutrition strategies that are consistent within families date from the Cretaceous. Evolution of EcM and nitrogen-fixing bacterial associations was particularly common in the eurosid group of angiosperms in the Late Cretaceous and early Cenozoic (Werner et al., 2014; Li et al., 2015; Tedersoo & Brundrett, 2017). This plant group may have specific genetic preconditions for entering microbial symbioses (Werner et al., 2014). Late Cretaceous angiosperm radiation has been linked to lower atmospheric CO₂, increasing aridity and fires, as well as plant colonization of aquatic, cold or disturbed habitats (Wing & Boucher, 1998; Gomez et al., 2015; Cardinal-McTeague et al., 2016; Carpenter et al., 2017).

The third wave of root diversification commenced in the Palaeogene c. 65 Ma and is still underway (Fig. 4). It includes lineages of plants with recently acquired root traits that are often inconsistent within families called ‘New Complex Root clades’ (NCR; Brundrett, 2017a,b). This wave, which peaked over the past 30 Myr, is linked to a very high diversity of both EcM and NM plants in certain plant families (Brundrett, 2017a; Tedersoo, 2017b). This is a global phenomenon, but NCR clade plants are most common in Australia, which provides a preview of future soil conditions elsewhere. Australian soils are very old, deep and highly leached (Henderson & Johnson, 2016). Outside Australia, examples of NCR clades include EcM of sedges in the genus Kobresia (Cyperaceae) and EcM or NM cluster roots in some members the Fabaceae, such as Lupinus spp. (Brundrett, 2017b; Tedersoo & Brundrett, 2017). Other less common trends found in one or more plant lineages include switching from NM to EcM (Freudenstein et al., 2016), Ericoid to EcM, and from balanced to myco-heterotrophic associations in plants (Box 1; Brundrett, 2002). Because the third wave of mycorrhizal evolution is linked to climate and soil conditions, it may be being accelerated by the Anthropocene epoch, with the increasing importance of disturbed habitats, as well as aridification and warming of most global ecosystems that can cause shifts in dominant mycorrhizal types in vegetation (Swaty et al., 2016; Tedersoo, 2017b). It is also expected that invasive plants (including many NCR species) will continue to be spread globally along with their co-introduced soil microorganisms, where they will also interact with novel symbiotic partners (Tedersoo, 2017b).

Both the second and third waves of mycorrhizal evolution are linked to climate change as well as increasing habitat and soil complexity, which presumably resulted in a competitive advantage for more specialized root types (Brundrett, 2017b). Mycorrhizal evolution tends to be a staged process starting from AM roots and progressing forward to specialized, NM or EcM roots with some reversions. Fig. 3 illustrates how plants that acquire a new nutrition strategy maintain the old one, at least initially (Brundrett, 2017a,b). The majority of lineages where plants transition from AM to EcM reach an endpoint with fully EcM roots, but others have retained multifunctional roots (EcM–AM). In the case of Allocasuarina spp. (Casuarinaceae), plants have EcM and AM as well as nitrogen fixation and cluster roots. Other examples of EcM–AM include many members of the Australian Myrtaceae and as well as the panglobal Fabaceae, in which mycorrhizal status varies within some genera (Brundrett, 2017a,b; Tedersoo & Brundrett, 2017). Contradictory published information is common for plants bearing multifunctional roots such as Australian Melaleuca and Acacia species, where individual species, in addition to AM, have abundant EcM, occasional EcM or no EcM (Fig. 3). Some plants which predominantly have EcM associations, such as Alnus, Eucalyptus and Salix also have AM as seedlings, or when growing in extreme habitats (Lodge, 1989; Chen et al., 2000; Põlme et al., 2016). This variability becomes problematic if researchers focus on one type of mycorrhiza, only examine seedlings or use a relaxed definition of EcM (Brundrett, 2017b).

Plants that appear to remain in an intermediate evolutionary state such as dual EcM–AM associations have multifunctional roots that may provide them with greater ecological flexibility, but overlapping functional roles would also come at a greater cost. However, these plants are often highly competitive suggesting that soil fertility is the most important factor limiting plant productivity in their habitats (Brundrett, 2009). For example, Australian eucalypts and acacias with multifunctional roots are important in plantation forestry and some are highly invasive weeds (Hui et al., 2014). Despite the success of families that acquired new root trait changes in the second and third wave of mycorrhizal evolution, the majority of vascular plants (72–80%) have retained AM associations throughout their evolutionary history on land.

IV. Conclusions and perspectives

Transitions between nutrition strategies, especially gains or losses of EcM and NM strategies, are more common than previously thought, but completely new mycorrhizal types emerge very rarely. The plant groups undergoing frequent shifts in biotic associations with mycorrhizal fungi and nitrogen-fixing bacteria include the fabids clade of eurosids. Genomics and transcriptomics tools offer high-resolution insights into changes in genetic structure and gene expression profiles related to initiation and loss of symbioses (Garcia et al., 2015; Delaux, 2017). These may include polyploidization events leading to functional shifts in gene paralogues, (e.g. MADS-box genes) which facilitate adaptive morphological radiation and diversification in plants (Van de Peer et al., 2017). It is highly likely that similar processes occur during the acquisition of symbiotic associations with fungi and nitrogen-fixing bacteria through mechanisms that may involve phytohormones, defence suppressor and transportation factors (Delaux et al., 2015; Garcia et al., 2015).

We recognize three waves of mycorrhizal evolution, starting with the origin of AM in early land plants and continuing with a period of major root diversification in the Late Cretaceous, when EcM (except Pinaceae) and NM roots appeared, and ericoid and orchid mycorrhizas evolved. The third ongoing wave of mycorrhizal evolution is related to substantial climate change since the Palaeocene, which is linked to development of specialized nutrition strategies and multifunctional (e.g. EcM and AM) roots in a few plant families. Plants with such multifunctional roots are subject to rapid morphological and taxonomic diversification, especially on nutrient-impoverished soils in seasonally dry habitats. It is likely that plant lineages with newly acquired mycorrhizas do not function in the same way as ancient mycorrhizal lineages and may be regulated by a different suite of symbiotic genes (Delaux et al., 2015; Maherali et al., 2016). In particular, the southwest Australian biodiversity hotspot provides the opportunity to compare association ages and intensity for EcM, as a tool to better understand the evolution, physiology and genomics of mycorrhizas.