The colonization of land by plants relied on fundamental biological innovations, among which was symbiosis with fungi to enhance nutrient uptake. Here we present evidence that several species representing the earliest groups of land plants are symbiotic with fungi of the Mucoromycotina. This finding brings up the possibility that terrestrialization was facilitated by these fungi rather than, as conventionally proposed, by members of the Glomeromycota. Since the 1970s it has been assumed, largely from the observation that vascular plant fossils of the early Devonian (400 Ma) show arbuscule-like structures, that fungi of the Glomeromycota were the earliest to form mycorrhizas, and evolutionary trees have, until now, placed Glomeromycota as the oldest known lineage of endomycorrhizal fungi. Our observation that Endogone -like fungi are widely associated with the earliest branching land plants, and give way to glomeromycotan fungi in later lineages, raises the new hypothesis that members of the Mucoromycotina rather than the Glomeromycota enabled the establishment and growth of early land colonists.
An analysis of the current state of knowledge of symbiotic fungal associations in 'lower' plants is provided. Three fungal phyla, the Zygomycota, Ascomycota and Basidiomycota, are involved in forming these associations, each producing a distinctive suite of structural features in well-defined groups of 'lower' plants. Among the 'lower' plants only mosses and Equisetum appear to lack one or other of these types of association. The salient features of the symbioses produced by each fungal group are described and the relationships between these associations and those formed by the same or related fungi in 'higher' plants are discussed. Particular consideration is given to the question of the extent to which root fungus associations in 'lower' plants are analogous to 'mycorrhizas' of 'higher' plants and the need for analysis of the functional attributes of these symbioses is stressed. Zygomycetous fungi colonize a wide range of extant lower land plants (hornworts, many hepatics, lycopods, Ophioglossales, Psilotales and Gleicheniaceae), where they often produce structures analogous to those seen in the vesicular-arbuscular (VA) mycorrhizas of higher plants, which are formed by members of the order Glomales. A preponderance of associations of this kind is in accordance with palaeohbotanical and molecular evidence indicating that glomalean fungi produced the archetypal symbioses with the first plants to emerge on to land. It is shown, probably for the first time, that glomalean fungi forming typical VA mycorrhiza with a higher plant (Plantago lanceolata) can colonize a thalloid liverwort (Pellia epiphylla), producing arbuscules and vesicles in the hepatic. The extent to which these associations, which are structurally analogous to mycorrhizas, have similar functions remains to be evaluated. Ascomycetous associations are found in a relatively small number of families of leafy liverworts. The structural features of the fungal colonization of rhizoids and underground axes of these plants are similar to those seen in mycorrhizal associations of ericaceous plants like Vaccinium. Cross inoculation experiments have confirmed that a typical mycorrhizal endophyte of ericaceous plants, Hymenoscyphus ericae, will form associations in liverworts which are structurally identical to those seen in nature. Again, the functional significance of these associations remains to be examined. Some members of the Jungermanniales and Metzgeriales form associations with basidiomycetous fungi. These produce intracellular coils of hyphae, which are similar to the pelotons seen in orchid mycorrhizas, which also involve basidiomycetes. The fungal associates of the autotrophic Aneura and of its heterotrophic relative Cryptothallus mirabilis have been isolated. In the latter case it has been shown that the fungal symbiont is an ectomycorrhizal associate of Betula, suggesting that the apparently obligate nature of the association between the hepatic and Betula in nature is based upon requirement for this particular heterotroph.
Background Molecular phylogeny has resolved the liverworts as the earliest-divergent clade of land plants and mosses as the sister group to hornworts plus tracheophytes, with alternative topologies resolving the hornworts as sister to mosses plus tracheophytes less well supported. The tracheophytes plus fossil plants putatively lacking lignified vascular tissue form the polysporangiophyte clade. Scope This paper reviews phylogenetic, developmental, anatomical, genetic and paleontological data with the aim of reconstructing the succession of events that shaped major land plant lineages. Conclusions Fundamental land plant characters primarily evolved in the bryophyte grade, and hence the key to a better understanding of the early evolution of land plants is in bryophytes. The last common ancestor of land plants was probably a leafless axial gametophyte bearing simple unisporangiate sporophytes. Water-conducting tissue, if present, was restricted to the gametophyte and presumably consisted of perforate cells similar to those in the early-divergent bryophytes Haplomitrium and Takakia. Stomata were a sporophyte innovation with the possible ancestral functions of producing a transpiration-driven flow of water and solutes from the parental gametophyte and facilitating spore separation before release. Stomata in mosses, hornworts and polysporangiophytes are viewed as homologous, and hence these three lineages are collectively referred to as the 'stomatophytes'. An indeterminate sporophyte body (the sporophyte shoot) developing from an apical meristem was the key innovation in polysporangiophytes. Poikilohydry is the ancestral condition in land plants; homoiohydry evolved in the sporophyte of polysporangiophytes. Fungal symbiotic associations ancestral to modern arbuscular mycorrhizas evolved in the gametophytic generation before the separation of major present-living lineages. Hydroids are imperforate water-conducting cells specific to advanced mosses. Xylem vascular cells in polysporangiophytes arose either from perforate cells or de novo. Food-conducting cells were a very early innovation in land plant evolution. The inferences presented here await testing by molecular genetics.
Internal specialized conducting tissues, if present, are restricted to the gametophytic generation in liverworts while they may occur in both generations in mosses. Conducting tissues are unknown in the anthocerotes. Water-conducting cells (WCCs) with walls perforated by plasmodesma-derived pores occur in the Calobryales and Pallaviciniaceae (Metzgeriales) among liverworts and in Takakia among mosses. Imperforate WCCs (hydroids) are present in bryoid mosses. A polarized cytoplasmic organization and a distinctive axial system of microtubules is present in the highly specialized food-conducting cells of polytrichaceous mosses (leptoids) and in less specialized parenchyma cells of the leafy stem and seta in other mosses including Sphagnum. A similar organization, suggested to re£ect specialization in long-distance symplasmic transport of nutrients, also occurs in other parts of the plant in mosses, including rhizoids and caulonemata, and may be observed in thallus parenchyma cells of liverworts. Perforate WCCs in the Calobryales, Metzgeriales and Takakia, and hydroids in bryoid mosses, probably evolved independently. Because of fundamental di¡erences in developmental design, homology of any of these cells with tracheids is highly unlikely. Likewise, putative food-conducting of bryophytes present highly distinctive characteristics and cannot be considered homologous with the sieve cells of tracheophytes.
Liverworts form endophytic associations with fungi that mirror mycorrhizal associations in tracheophytes. Here we report a worldwide survey of liverwort associations with glomeromycotean fungi (GAs), together with a comparative molecular and cellular analysis in representative species. Liverwort GAs are circumscribed by a basal assemblage embracing the Haplomitriopsida, the Marchantiopsida (except a few mostly derived clades), and part of the Metzgeriidae. Fungal endophytes from Haplomitrium, Conocephalum, Fossombronia, and Pellia were related to Glomus Group A, while the endophyte from Monoclea was related to Acaulospora. An isolate of G. mosseae colonized axenic thalli of Conocephalum, producing an association similar to that in the wild. Fungal colonization in marchantialean liverworts suppressed cell wall autofluorescence and elicited the deposition of a new wall layer that specifically bound the monoclonal antibody CCRC-M1 against fucosylated side groups associated with xyloglucan and rhamnogalacturonan I. The interfacial material covering the intracellular fungus contained the same epitopes present in host cell walls. The taxonomic distribution and cytology of liverwort GAs suggest an ancient origin and multiple more recent losses, but the occurence in widely separated liverwort taxa of fungi related to glomeromycotean lineages that form arbuscular mycorrhizas in tracheophytes, notably the Glomus Group A, is better explained by host shifting from tracheophytes to liverworts.
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