A great diversity of plants and fungi engage in mycorrhizal associations. In natural habitats, and in an ecologically meaningful time span, these associations have evolved to improve the fitness of both plant and fungal symbionts. In systems managed by humans, mycorrhizal associations often improve plant productivity, but this is not always the case. Mycorrhizal fungi might be considered to be parasitic on plants when net cost of the symbiosis exceeds net benefits. Parasitism can be developmentally induced, environmentally induced, or possibly genotypically induced. Morphological, phenological, and physiological characteristics of the symbionts influence the functioning of mycorrhizas at an individual scale. Biotic and abiotic factors at the rhizosphere, community, and ecosystem scales further mediate mycorrhizal functioning. Despite the complexity of mycorrhizal associations, it might be possible to construct predictive models of mycorrhizal functioning. These models will need to incorporate variables and parameters that account for differences in plant responses to, and control of, mycorrhizal fungi, and differences in fungal effects on, and responses to, the plant. Developing and testing quantitative models of mycorrhizal functioning in the real world requires creative experimental manipulations and measurements. This work will be facilitated by recent advances in molecular and biochemical techniques. A greater understanding of how mycorrhizas function in complex natural systems is a prerequisite to managing them in agriculture, forestry, and restoration.

http://max2.ese.u-psud.fr/epc/conservation/PDFs/HIPE/Johnson1997.pdf

Functioning of mycorrhizal associations along the mutualism–parasitism continuum*

Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability

Each perennial woody plant is a highly integrated system of competing carbohydrate sinks (utilization sites). Internal competition for carbohydrates is shown by changes in rates of carbohydrate movement from sources to sinks and reversals in direction of carbohydrate transport as the relative sink strengths of various organs change. Most carbohydrates are produced in foliage leaves but some are synthesized in cotyledons, hypocotyls, buds, twigs, stems, flowers, fruits, and strobili. Although the bulk of the carbohydrate pool moves to sinks through the phloem, some carbohydrates are obtained by sinks from the xylem sap. Sugars are actively accumulated in the phloem and move passively to sinks along a concentration gradient. The dry weight of a mature woody plant represents only a small proportion of the photosynthate it produced. This discrepancy results not only from consumption of plant tissues by herbivores and shedding of plant parts, but also from depletion of carbohydrates by respiration, leaching, exudation, secretion, translocation to other plants through root grafts and mycorrhizae and losses to parasites. Large spatial and temporal variations occur in the use of reserve- and currently produced carbohydrates in metabolism and growth of shoots, stems, roots, and reproductive structures. A portion of the carbohydrate pool is diverted for production of chemicals involved in defense against fungi, herbivores, and competing plants. Woody plants accumulate carbohydrates during periods of excess production and deplete carbohydrates when the rate of utilization exceeds the rate of production. Stored carbohydrates play an important role in metabolism, growth, defense, cold hardiness, and postponement or prevention of plant mortality.

Carbohydrate sources and sinks in woody plants

There is plenty of evidence for improved nutrient acquisition by ectomycorrhizas in trees; however, their role in water uptake is much less clear. In addition to experiments showing improved performance during drought by mycorrhizal plants, there are several studies showing reduced root hydraulic conductivity and reduced water uptake in mycorrhizal roots. The clearest direct mechanism for increased water uptake is the increased extension growth and absorbing surface area, particularly in fungal species with external mycelium of the long-distance exploration type. Some studies have found increased aquaporin function and, consequently, increased root hydraulic conductivity in ectomycorrhizal plants while other studies showed no effect of ectomycorrhizal associations on root water flow properties. The aquaporin function of the fungal hyphae is also likely to be important for the uptake of water by the ectomycorrhizal plant, but more work needs to be done in this area. The best-known indirect mechanism for mycorrhizal effects on water relations is improved nutrient status of the host. Others include altered carbohydrate assimilation via stomatal function, possibly mediated by changes in growth regulator balance; increased sink strength in mycorrhizal roots; antioxidant metabolism; and changes in osmotic adjustment. None of these possibilities has been sufficiently explored. The mycorrhizal structure may also reduce water movement because of different fine root architecture (thickness), cell wall hydrophobicity or the larger number of membranes that water has to cross on the way from the soil to the xylem. In future studies, pot experiments comparing mycorrhizal and nonmycorrhizal plants will still be useful in studying well-defined physiological details. However, the quantitative importance of ectomycorrhizas for tree water uptake and water relations can only be assessed by field studies using innovative approaches. Hydraulic redistribution can support nutrient uptake during prolonged dry periods. In large trees with deep root systems, it may turn out that the most important function of mycorrhizas during drought is to facilitate nutrient acquisition.

Ectomycorrhizas and water relations of trees: a review.

PLANTS and soils are a critically important element in the global carbon–energy equation. It is estimated that in forest ecosystems over two-thirds of the carbon is contained in soils and peat deposits1. Despite the importance of forest soils in the global car-bon cycle, fluxes of carbon associated with fundamental processes and soil functional groups are inadequately quantified, limiting our understanding of carbon movement and sequestration in soils. We report here the direct measurement of carbon in and through all major pools of a mycorrhizal (fungus-root) coniferous seedling (a complete carbon budget). The mycorrhizal symbiont reduces over-all retention of carbon in the plant–fungus symbiosis by increasing carbon in roots and below-ground respiration and reducing its retention and release above ground. Below ground, mycorrhizal plants shifted allocation of carbon to pools that are rapidly turned over, primarily to fine roots and fungal hyphae, and host root and fungal respiration. Mycorrhizae alter the size of below-ground carbon pools, the quality and, therefore, the retention time of carbon below ground. Our data indicate that if elevated atmos-pheric CO2 and altered climate stressors alter mycorrhizal colonization in forests, the role of forests in sequestering carbon could be altered.

/pdf/mycorrhizae-alter-quality-and-quantity-of-carbon-allocated-24ew8lzax4.pdf

Mycorrhizae alter quality and quantity of carbon allocated below ground

summary
Douglas fir [Pseudotsuga menziesii (Mirb.) Franco] seedlings responded differently regarding rate of photosynthesis when inoculated with three different ectomycorrhizal fungi. Rhizopogon vinicolor FSL788-5 caused a significant increase in net photosynthesis rate compared to non-mycorrhizal controls, while Hebeloma crustuliniforme HeCr2 and Laccaria laccata S238-A had no effect. Colonization by Rhizopogon and Hebeloma caused increased osmotic potential in the leaf symplast compared to controls, while Laccaria did not. Colonization levels for Rhizopogon, Hebeloma and Laccaria were 36, 93 and 73 % of root tips, respectively. Rhizopogon and Hebeloma produced abundant extramatrical hyphae and/or rhizomorphs, while Laccaria was smooth-mantled. Hebeloma-colonized seedlings were significantly smaller than non-mycorrhizal controls; Rhizopogon seedlings were smaller, but significantly so only at P < 0.10. Laccaria did not affect seedling size. Only smaller Hebeloma seedlings exhibited elevated concentrations of N, P, K, and Ca over non-mycorrhizal controls. These data demonstrate a non-nutritional basis for increased rate of photosynthesis caused by some ectomycorrhizal fungi that can be explained by the increased photosynthate sink generated by extensive fungal growth associated with the mycorrhizas.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.1990.tb00452.x

Carbon–sink stimulation of photosynthesis in Douglas fir seedlings by some ectomycorrhizas

summary
Douglas fir [Pseudotsuga menziesii (Mirb.) Franco] seedlings were inoculated with different species of ectomycorrhizal fungi, Rhizopogon vinicolor FSL788-5, Laccaria laccata S238-A, or Hebeloma crustuliniforme HeCr2, to determine how different fungi affect the response of photosynthesis and water relations of seedlings to drying soil. Potted seedlings were grown in a greenhouse for 6 months under well-watered conditions, then transferred to a growth chamber where measurements were made as the soil dried.

Rhizopogon enhanced both net photosynthesis rate and stomatal conductance compared to non-mycorrhizal controls (P < 0.01) over the soil water potential range of −0.05 to −0.50 MPa, despite 0.2 to 0.3 MPa lower leaf water potential. Hebeloma tended to enhance, while Laccaria decreased net photosynthesis rate and stomatal conductance of host seedlings over this range of soil water potential, but neither fungus affected leaf potential. Our observations for Rhizopogon and Laccaria could not be explained by existing hypotheses based on mycorrhizal effects on plant size, nutrition, osmotic adjustment, or water uptake characteristics. Nutrition may have been a factor for Hebeloma.

We propose that in the absence of nutritional and water uptake effects, net photosynthesis rate and stomatal conductance are correlated with rate of export of photosynthate to the mycorrhizal fungus. Strong mycorrhizal demand for photosynthate stimulates photosynthesis, to which stomata respond by opening, notwithstanding water stress. Our results for Rhizopogon are consistent with this hypothesis.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.1991.tb04914.x

Role for the photosynthate demand of ectomycorrhizas in the response of Douglas fir seedlings to drying soil

A growth chamber experiment was conducted to determine if P fertilization to enhance the P nutrition of otherwise N and P deficient Douglas fir [Pseudotsuga menziesii (Mirb.) Franco] seedlings reduces water stress in the seedlings during drought periods. Seedlings were grown in pasteurized mineral soil under well-watered conditions and fertilized periodically with a small amount of nutrient solution containing P at either of three levels: 0, 20, or 50 mg P L-1. By age 6 mo, leaf nutrient analysis indicated that N and P were deficient in control (0 mg P L-1) seedlings. The highest level of P fertilization, which doubled leaf P concentration, did not affect plant biomass, suggesting that N deficiency was limiting growth. When these seedlings were subjected to drought, there was no effect of P fertilization on leaf water potential or osmotic potential. Furthermore, P fertilized seedlings had lower stomatal conductance and net photosynthesis rate. These results indicate that enhanced P nutrition, in the presence of N deficiency, does not reduce water stress in Douglas fir seedlings during drought periods.

Effect of phosphorus fertilization on water stress in Douglas fir seedlings during soil drying

Biomass allocation in 6-month-old ectomycorrhizal Douglas fir seedlings was compared to that in nonmycorrhizal seedlings of the same age, nutrient status and total biomass. Seedlings colonized by Rhizopogon vinicolor had the same distribution of biomass between roots, stems and needles, but only 56% of the total length of roots (including mycorrhizal branches) compared to nonmycorrhizal seedlings. Laccaria laccata had no effect on distribution of biomass or root length of seedlings. The results for Rhizopogon provide direct evidence that the process of ectomycorrhizal colonization can significantly affect plant biomass allocation by one or more mechanisms not directly related to altered nutrition or overall plant size.

M. G. Dosskey

Papers

Carbon–sink stimulation of photosynthesis in Douglas fir seedlings by some ectomycorrhizas

Role for the photosynthate demand of ectomycorrhizas in the response of Douglas fir seedlings to drying soil

Effect of phosphorus fertilization on water stress in Douglas fir seedlings during soil drying

Comparison of biomass allocation in ectomycorrhizal and nonmycorrhizal Douglas fir seedlings of similar nutrition and overall size