New
Phytologist 154(2): 275 (May 2002)
Coevolution
of roots and mycorrhizas of land plants
Mark C. Brundrett
Summary
Here, the coevolution of mycorrhizal fungi and roots is assessed in the light of evidence now available, from palaeobotanical and morphological studies and the analysis of DNA-based phylogenies. The first bryophyte-like land plants, in the early Devonian (400 million years ago), had endophytic associations resembling vesicular–arbuscular mycorrhizas (VAM) even before roots evolved. Mycorrhizal evolution would have progressed from endophytic hyphae towards balanced associations where partners were interdependent due to the exchange of limiting energy and nutrient resources. Most mycorrhizas are mutualistic, but in some cases the trend for increasing plant control of fungi culminates in the exploitative mycorrhizas of achlorophyllous, mycoheterotrophic plants. Ectomycorrhizal, ericoid and orchid mycorrhizas, as well as nonmycorrhizal roots, evolved during the period of rapid angiosperm radiation in the Cretaceous. It is hypothesised that roots gradually evolved from rhizomes to provide more suitable habitats for mycorrhizal fungi and provide plants with complex branching and leaves with water and nutrients. Selection pressures have caused the morphological divergence of roots with different types of mycorrizas. Root cortex thickness and exodermis suberization are greatest in obligately mycorrhizal plants, while nonmycorrhizal plants tend to have fine roots, with more roots hairs and relatively advanced chemical defences. Major coevolutionary trends and the relative success of plants with different root types are discussed.
II. Mycorrhizal fungi
There is only limited fossil evidence of Paleozoic fungi (Taylor & Osborn, 1996), but molecular evidence suggests they diverged from other living organisms deep in the Proterozoic (Wang et al., 1999). Thus, it is probable that the first terrestrial fungi colonised land long before plants did. Soil surface microbial communities containing fungi and algae were probably the first terrestrial associations between fungi and photosynthetic organisms (Gehrig et al., 1996; Evans & Johansen, 1999; Schü̈ßler & Kluge, 2000). Most Paleozoic fossils of fungi resemble oomycetes, chytrids or zygomycetes, protoctistan organisms that are not directly related to any mycorrhizal fungus lineages (Taylor & Taylor, 1997). These fossils provide examples of putative parasitic plant–fungus associations (similar fungi probably were long established parasites of aquatic algae), but evidence of saprophytism is rare until much later (Taylor & Osborn, 1996). There is scant fossil evidence of lichens in the Paleozoic (Taylor & Osborn, 1996), except for a Devonian fossil that may be a zygomycete lichen (Taylor et al., 1997).
III. The dawn of mycorrhizas
IV. Mycorrhizal associations of living and extinct plants
The first land plants were thought to be bryophytes, similar to liverworts or hornworts, with a horizontally spreading thallus and separate sporophyte and gametophyte generations (Kenrick & Crane, 1997; Renzaglia et al., 2000). Fossil evidence of these plants first appeared in the Mid Ordovician to Early Silurian periods (476–432 myr old), but earlier spore tetrads that may be from land plants are known (Table 4). The first land plants most likely evolved from freshwater charophycean algae and probably required wet habitats (Kenrick & Crane, 1997). There are no structurally preserved specimens of these plants to show if they were mycorrhizal. These plants had no roots (Section V).
1. Bryophytes
Mosses, the largest living group of bryophytes, are generally not mycorrhizal, but often contain endophytic hyphae of VAM fungi (Rabatin, 1980; Turnau et al., 1999). Liverworts and hornworts have VAM–like associations with glomalean fungi that form arbuscules in their thalli (Table 4). Fine endophytes (glomalean fungi with very narrow hyphae forming VAM with arbuscules) are common in bryophytes, but other VAM fungi, such as Glomus species, are also present (Johnson, 1977; Turnau et al., 1999; Schüßler, 2000). Fine endophytes have much narrower hyphae than other VAM fungi and may have specifically evolved to grow within the narrow rhizoids and confined spaces of bryophytes. Fine endophytes also colonise roots of vascular plants in many habitats (e.g. Hall, 1977; Brundrett et al., 1999).
Liverwort rhizoids are also colonised by the fungi of ericoid mycorrhizas in some ecosystems (Duckett & Read, 1995; Chambers et al., 1999; Read et al., 2000). It is not known how common liverwort colonisation by VAM or ericoid mycorrhizal fungi is, or if they provide benefits to the plants. These may be the oldest forms of balanced mycorrhizal association, or endophytic activity by mycorrhizal fungi. Evidence for the former is provided by the presence of arbuscules, the confinement of hyphae to specific tissues and the expression of different hyphal morphologies in different tissues (Ligrone & Lopes, 1989; Turnau et al., 1999). These morphological adaptations by the host are only likely to evolve if associations are beneficial (Section III). Several species of subterranean achlorophyllous bryophytes apparently have exploitative mycorrhizas (Leake, 1994; Read et al., 2000).
2. Primitive plants
The oldest fossil evidence of mycorrhizas is in the rhizomes of early vascular plants, but it is quite likely that these associations started in the thallus of their bryophyte-like precursors. There are VAM-like hyphae, vesicles and arbuscules in fossil rhizomes from the Devonian period onwards and spores from the Ordovician onwards (Tables 1 and 3). These fungal structures show a remarkable resemblance to modern VAM associations (Stubblefield & Taylor, 1988; Taylor & Osborn, 1996). Taylor et al. (1995) and Phipps & Taylor (1996) provide the most detailed studies of mycorrhizas in rhizome fossils. The consistency and intensity of these associations is typical of obligate VAM in living plants (Section VI). The rhizomes of Aglaophyton major, an Early Devonian land plant of uncertain affinities, contained arbuscules that were restricted to a specialised cortical zone, with a meristem that apparently extended the zone containing cells occupied by fungi. This meristem probably evolved to increase the capacity of Aglaophyton to control mycorrhizal fungi. However, it is not possible conclusively to prove that early VAM–like associations were mycorrhizal (Section II).
Sphenophytes, lycopodophytes and pteridophytes were the first plants with roots, and arose in the Mid Devonian (Table 1). Their surviving descendants include Lycopodium, Selaginella and Isoetes. These plants have a separate gametophyte phase without roots and a sporophyte with roots and leaves (Foster & Gifford, 1974). Schmid & Oberwinkler (1993) found an unusual association in the subterranean gametophyte of a Lycopodium species with some characteristics of VAM, but without arbuscules and with very fine coiled hyphae that were digested in cells. Gametophytes of another species of Lycopodium are similar, but have arbuscule-like structures in cells (Duckett & Ligrone, 1992). The hyphae within these gametophytes have similar ultrastructural features to VAM fungi, but are extremely narrow, so are most likely to be a fine endophyte (Read et al., 2000). These gametophytes probably have exploitative VAM (Leake, 1994). Adult Lycopodium and Selaginella sporophytes have normal VAM associations (Harley & Harley, 1987; Gemma et al., 1992). Isoetes often has VAM, even when growing as a submerged aquatic plant (Beck-Nielsen & Madsen, 2001).