The beneficial effects of mycorrhizae on plant growth have often been related to the increase in the uptake of immobile nutrients, especially phosphorus (P). In this review the mechanisms for the increase in the uptake of P by mycorrhizae and the sources of soil P for mycorrhizal and non-mycorrhizal plants are examined. Various mechanisms have been suggested for the increase in the uptake of P by mycorrhizal plants. These include: exploration of larger soil volume; faster movement of P into mycorrhizal hyphae; and solubilization of soil phosphorus. Exploration of larger soil volume by mycorrhizal plants is achieved by decreasing the distance that P ions must diffuse to plant roots and by increasing the surface area for absorption. Faster movement of P into mycorrhizal hyphae is achieved by increasing the affinity for P ions and by decreasing the threshold concentration required for absorption of P. Solubilization of soil P is achieved by the release of organic acids and phosphatase enzymes. Mycorrhizal plants have been shown to increase the uptake of poorly soluble P sources, such as iron and aluminium phosphate and rock phosphates. However, studies in which the soil P has been labelled with radioactive 32P indicated that both mycorrhizal and non-mycorrhizal plants utilized the similarly labelled P sources in soil.

A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants

The effects of Cd, Cu, Zn, and Pb on soil microorganisms and microbially mediated soil processes are reviewed. The emphasis is placed on temperate forest soils. The sensitivity of different measurements is discussed, and data compiled to compare relative toxicity of different metals. On the whole the relative toxicity of the metals (on a μg g−1 soil basis) decreased in the order Cd > Cu > Zn > Pb, but differences between different investigations were found. The influence of abiotic factors on metal toxicity is briefly discussed and especially examplified by different soil organic matter content. Evidence of tolerance and adaptation in the soil environment and the time scale involved in the evolution of a metal-tolerant microbial community after metal exposure are also considered.

Effects of heavy metals in soil on microbial processes and populations (a review)

The production of organic acids by fungi has profound implications for metal speciation, physiology and biogeochemical cycles. Biosynthesis of oxalic acid from glucose occurs by hydrolysis of oxaloacetate to oxalate and acetate catalysed by cytosolic oxaloacetase, whereas on citric acid, oxalate production occurs by means of glyoxylate oxidation. Citric acid is an intermediate in the tricarboxylic acid cycle, with metals greatly influencing biosynthesis: growth limiting concentrations of Mn, Fe and Zn are important for high yields. The metal-complexing properties of these organic acids assist both essential metal and anionic (e.g. phosphate) nutrition of fungi, other microbes and plants, and determine metal speciation and mobility in the environment, including transfer between terrestrial and aquatic habitats, biocorrosion and weathering. Metal solubilization processes are also of potential for metal recovery and reclamation from contaminated solid wastes, soils and low-grade ores. Such ‘heterotrophic leaching’ can occur by several mechanisms but organic acids occupy a central position in the overall process, supplying both protons and a metal-complexing organic acid anion. Most simple metal oxalates [except those of alkali metals, Fe(III) and Al] are sparingly soluble and precipitate as crystalline or amorphous solids. Calcium oxalate is the most important manifestation of this in the environment and, in a variety of crystalline structures, is ubiquitously associated with free-living, plant symbiotic and pathogenic fungi. The main forms are the monohydrate (whewellite) and the dihydrate (weddelite) and their formation is of significance in biomineralization, since they affect nutritional heterogeneity in soil, especially Ca, P, K and Al cycling. The formation of insoluble toxic metal oxalates, e.g. of Cu, may confer tolerance and ensure survival in contaminated environments. In semiarid environments, calcium oxalate formation is important in the formation and alteration of terrestrial subsurface limestones. Oxalate also plays an important role in lignocellulose degradation and plant pathogenesis, affecting activities of key enzymes and metal oxidoreduction reactions, therefore underpinning one of the most fundamental roles of fungi in carbon cycling in the natural environment. This review discusses the physiology and chemistry of citric and oxalic acid production in fungi, the intimate association of these acids and processes with metal speciation, physiology and mobility, and their importance and involvement in key fungal-mediated processes, including lignocellulose degradation, plant pathogenesis and metal biogeochemistry.

Fungal production of citric and oxalic acid: importance in metal speciation, physiology and biogeochemical processes.

SUMMARY
More than 400 species of vascular plants, in 87 genera, are acholophyllous and heterotrophic, but not directly parasitic upon autotrophs. They are usually, but incorrectly, described as 'saprophytes’since they are in fact nourished by means of specialized mycorrhizal associations. Although distributed world-wide, they are most abundant and show the greatest species-richness in the Neotropics and Palaeotropical regions. Their aerial parts range in size from a few centimetres to extensive liane types up to 40 m long. With few exceptions, their habitats are dense moist forests in which there is a surface accumulation of leaf litter, often in situations which are too shaded for autotrophic growth.

Although the achlorophyllous mycorrhizal mode of life has evolved independently many times and in widely disparate taxonomic groups, such plants show strong convergent evolution in particular adaptations to their peculiar mode of life. Most prominant amongst these are reductions in the size of seed and embryo, and the lack of differentiation of the embryo at maturity. The number of seeds produced by each flower is typically very large and the shape, structure and surface features of seeds involving adaptation for wind dispersal show remarkable parallels in many species. Specific adaptations for zoochory are rare but well developed in a small number of genera, some of which produce scents like fungal fruit bodies or floral parts which mimic fungal sporocarps.

Vegetative parts are often even more conspicuously reduced. Most myco-heterotrophs are entirely subterranean for most of their lives and these stages exhibit adaptations consistent with a change in function from organs of absorption to organs of storage, shown by the almost universal loss of root hairs, decrease in surface area as exhibited in short cylindric‘vermiform’and tuberous roots or, in extreme cases, the complete suppression of roots and the formation of a swollen tuber or rhizome. Increased width of the root cortex often accommodates mycorrhizal infection and stores of carbohydrates and other materials obtained from the fungal symbiont. Mycorrhizal infection is confined to the below-ground parts of the plants but may be found there in modified stems as well as in roots.

In many genera, stems are exceptionally slender and thread-like and their vascular tissues are either reduced to a single narrow cylinder of bicollateral bundles or, minimally, to four or six narrow bundles in the cortex. Secondary thickening is poorly developed in all but a tiny minority of species, lignification being confined to annular or, rarely, a few scalariform xylem vessels. Phloem is present in very small amounts and then mainly as parenchyma with sieve tubes frequently recorded as narrow and possibly with abherent sieve plates.

Leaves are typically reduced to widely spaced achlorophyllous scales on the inflorescence axis. Occasionally, they are present only on underground rhizomes or tubers. The vascular supply to the leaf-scales, normally reduced to a single trace, may be absent. Vestigial stomata are sometimes found on leaves and, in a few species which retain traces of chlorophyll, on shoots but, in most fully heterotrophic species, stomata are absent from aerial parts.

Since their seeds are very small and contain minimal reserve carbohydrates, the germination of myco-heterotrophs in nature would appear to depend upon infection by an appropriate symbiotic fungus at an early stage. The nature of the carbohydrates transferred from the fungus to the plants has not been determined. Once acquired from The fungal partner, most plants store carbon in a variety of forms, the most common of which is starch, although other compounds including glucomannan, fructan and calcium oxalate art important in some specks.

Asexual reproduction is frequently important with root tubers, tubercles and rhizomes providing the means of vegetative spread. Nonetheless, all the angiospermous species recorded to date also reproduce sexually. Floral structures show varying degrees of reduction concomitant with myco-heterotrophy. Inflorescences are typically small, often with a single terminal flower, and the floral parts often show extreme simplification, with the production of unilocular or, more rarely, bilocular and trilocular ovaries. In some of the most highly adapted species, there is reduction of integumentary layers surrounding each ovule from the normal bitegmic condition to unitegmic or, occasionally, ategmic. With the principal exception of the Monotropaceae, placentation is typically trimerous and parietal. Flowers normally appear to be cross-pollinated and are brightly coloured. nectiferous, occasionally scented, and can demonstrate extreme morphological adaptations which attract insects as in the production of lone caudate tepals or fungus-mimicking structures.

Much is still to be learned about the adaptive features and especially about the physiology of these plants and of their early developmental stages during which the essential associations with fungi are established. Similarly, studies of the taxonomy and physiology of most of their fungal partners are still in their infancy.

The biology of myco‐heterotrophic (‘saprophytic’) plants

Oxalate secretion by fungi provides many advantages for their growth and colonization of substrates. The role of oxalic acid in pathogenesis is through acidification of host tissues and sequestrati...

Oxalate production by fungi : its role in pathogenicity and ecology in the soil environment

SUMMARY
Calcium oxalate crystals occur in the mantle of ectomycorrhizal roots of Firms radiata and Eucalyptus marginata. Dense concentrations of these crystals were observed in association with the fungal symbiont of both tree species. It is suggested that oxalate production may enhance nutrient uptake by ectomycorrhizal roots of forest species growing in nutrient impoverished soils. Concentrations of Ca, S, K and P were similar in mycorrhizal root masses of P. radiata and E. marginata.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.1982.tb03411.x

K. Cromack

Papers

Accumulation of calcium oxalate in the mantle of ectomycorrhizal roots of pinus radiata and eucalyptus marginata