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.

Coevolution of roots and mycorrhizas of land plants

A comprehensive appraisal of the mycorrhizal literature provides data for 336 plant families representing 99% of flowering plants, with regard to mycorrhizas and other nutritional adaptations. In total, arbuscular (AM), orchid, ectomycorrhizas (EM) and ericoid mycorrhizas and nonmycorrhizal (NM) roots occur in 74%, 9%, 2%, 1% and 6% of Angiosperm species respectively. Many families of NM plants have alternative nutritional strategies such as parasitism, carnivory, or cluster roots. The remaining angiosperms (8%) belong to families reported to have both AM and NM species. These are designated as NM-AM families here and tend to occur in habitats considered non-conducive to mycorrhizal fungi, such as epiphytic, aquatic, extremely cold, dry, disturbed, or saline habitats. Estimated numbers of species in each category of mycorrhizas is presented with lists of NM and EM families. Evolutionary trends are also summarised by providing data on all clades and orders of flowering and non-flowering vascular plants on a global scale. A case study of Western Australian plants revealed that plants with specialised nutritional modes such as carnivory, cluster roots, or EM were much more diverse in this ancient landscape with infertile soils than elsewhere. Detailed information on the mycorrhizal diversity of plants presented here is linked to a website (mycorrhizas.info) to allow data to remain current. Over a century of research effort has resulted in data on mycorrhizal associations of >10,000 plant species that are of great value, but also somewhat of a liability due to conflicting information about some families and genera. It is likely that these conflicts result in part from misdiagnosis of mycorrhizal associations resulting from a lack of standardisation in criteria used to define them. Families that contain both NM and AM species provide a second major source of inconsistency, but even when these are excluded there is a ∼10% apparent error rate in published lists of mycorrhizal plants. Arbuscules are linked to AM misdiagnosis since they are used less often than vesicles to recognise AM associations in roots and apparently occur sporadically in NM plants. Key issues with the diagnosis of mycorrhizal plants are discussed using the Cyperaceae as a case study. Detailed protocols designed to consistently distinguish AM from endophytic Glomeromycotan Fungus Colonisation (GFC) are provided. This review aims to stimulate debate and provide advice to researchers delving into root biology.

Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis

Most terrestrial plants associate with root-colonising mycorrhizal fungi, which improve the fitness of both the fungal and plant associates. However, exceptions exist both between and within plant families failing to associate with mycorrhizal fungi or in the incidence and the extent of mycotrophy, which may vary greatly. Sedges are important pioneers of disturbed habitats and often dominate vegetations like wetlands, and arctic and alpine vegetations, in which the mycorrhizal inoculum in the soil is often low or absent. In the past, sedges were often designated as non-mycorrhizal, though limited reports indicated the presence of mycorrhiza in certain species. However, studies since 1987 indicate widespread occurrence of mycorrhiza in sedges. Based on these studies, the family Cyperaceae is no longer a non-mycorrhizal family, but the mycorrhizal status of its members is greatly influenced by environmental conditions. Further, sedges appear to have several morphological adaptations to thrive in the absence of mycorrhizal association. Though mycorrhizal associations have been noted in many sedge species, the ecological role of this association is not well documented and no clear generalisation can be drawn. Similarly, the role of mycorrhizal fungi on sedge growth and nutrient uptake or non-nutritional benefits has yet to be fully ascertained. This paper reviews the current information available on the incidence of mycorrhiza in sedges and the possible reasons for low mycotrophy observed in this family.

Mycorrhiza in sedges—an overview

The Cyperaceae have generally been considered nonmycorrhizal, although recent evidence suggests that mycotrophy may be considerably more widespread among sedges than was previously realized. This study surveyed 23 species of Carex occurring in upland and wetland habitats in northeastern Illinois. Mycorrhizal infection by arbuscular fungi was found in the roots of 16 species of Carex and appears to occur in response to many factors, both environmental and phylogenetic. While some species appear to be obligately nonmycorrhizal, edaphic influences may be responsible for infection in others. In five of the seven Carex species that were nonmycorrhizal, a novel root character, the presence of bulbous-based root hairs, was identified. The taxonomically patchy distribution of the distinctive root hair trait suggests that these structures may have evolved several times within the genus. Evidence of multiple independent origins of the root hair trait lends support to the hypothesis that root hairs represent an adaptation to nonmycotrophy. Although taxonomic position does seem to be of importance in determining the mycorrhizal dependence of sedges, the pattern may be a patchwork of both mycorrhizal clades and clades that have adapted to the nonmycorrhizal state.

https://bsapubs.onlinelibrary.wiley.com/doi/pdf/10.2307/2656816

Mycorrhizal status of the genus Carex (Cyperaceae).

When grown in nutrient solutions of extremely low [P] (<or=1.0 microm), the sedge Schoenus unispiculatus Benth. (Cyperaceae) develops dauciform roots, which are short and carrot shaped, and produce dense numbers of long root hairs. It has been suggested that dauciform roots of monocotyledonous sedges function to acquire P from nutrient-poor, P-fixing soils in a manner similar to that of cluster (proteoid) roots developed by some dicotyledonous species, but without evidence to substantiate this claim. To elucidate the ecophysiological role of dauciform roots, we assessed carboxylate exudation, internal carboxylate and P concentrations and O(2) uptake rates during dauciform root development. We showed that O(2) consumption was fastest [9 nmol O(2) g(-1) fresh mass (FM) s(-1)] and root [P] greatest (0.4 mg P g(-1) FM) when dauciform roots were young and rapidly developing. Citrate was the most abundant carboxylate in root tissues at all developmental stages, and was most concentrated (22.2 micromol citrate g(-1) FM) in young dauciform roots, decreasing by more than half in mature dauciform roots. Peak citrate-exudation rates (1.7 nmol citrate g(-1) FM s(-1)) occurred from mature dauciform roots, and were approximately an order of magnitude faster than those from roots of species without root clusters, and similar to those of mature proteoid (cluster) roots of Proteaceae. Both developing and mature dauciform roots had the capacity to acidify (but not alkalinize) the rhizosphere. Anatomical studies showed that epidermal cells in dauciform roots were greatly elongated in the transverse plane; epidermal cells of parent roots were unmodified. Although structurally distinct, the physiology of dauciform roots in sedges appears to be analogous to that of proteoid roots of Proteaceae and Fabaceae, and hence, dauciform roots would facilitate access to sorbed P and micronutrients from soils of low fertility.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-3040.2006.01574.x

Specialized 'dauciform' roots of Cyperaceae are structurally distinct, but functionally analogous with 'cluster' roots

Species of Cyperaceae and Restionaceae were examined for presence of vesicular-arbuscular (VA) mycorrhizal fungi in natural habitat in south-west Western Australia. VA mycorrhizal fungi were detected in roots of two species of Cyperaceae (Lepidosperma gracile and Tetraria capillaris), and two species of Restionaceae (Alexgeorgea nitens and Lyginia barbata), all representing the first records for these genera. Results indicated a very short seasonal period of infection, with VA mycorrhizal fungi representing the genera Acaulospora, Glomus, Scutellospora and Gigaspora identified in roots. VA mycorrhizal fungi were prominent from late autumn to early winter (April-June) and in up to 30% of the young, new season's roots as they penetrated the upper 10 cm region of the soil profile. Mycorrhizal infection was not evident during the dry summer months. This study suggests that mycorrhizas may be important for nutrition of these hosts in these environments but their activity is restricted to a brief period of the growing season.

Occurrence of Vesicular Mycorrhizal Fungi in Dryland Species of Restionaceae and Cyperaceae From South-West Western Australia

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Occurrence of Vesicular Mycorrhizal Fungi in Dryland Species of Restionaceae and Cyperaceae From South-West Western Australia