Cost efficiency of nutrient acquisition and the advantage of mycorrhizal symbiosis for the host plant

Abstract

Mycorrhizal symbiosis involves reciprocal transfer of carbon and nutrients between shoots on the one hand and roots colonized by symbiotic fungi on the other. Mycorrhizas may improve the mineral nutrient acquisition rates, but simultaneously increase the belowground demand for carbon. Mycorrhizal plants will have a selective advantage over non‐mycorrhizal ones if they are more cost‐efficient in terms of carbon cost per unit of acquired mineral nutrient. However, we demonstrate here in a simple model system that this is not a necessary condition. Mycorrhizas may evolve even when they are less cost‐efficient, provided that photosynthesis and/or growth are strongly nutrient‐limited. This result implies a unique hypothesis for the evolution of mycorrhizal associations which may be inherently cost‐inefficient as compared to plant roots. Such symbioses may have evolved when the superior nutrient acquisition rate of fungi combines with the relatively high photosynthetic nutrient use efficiency of the host plant. Consequently, provided that mycorrhizas are really cost‐inefficient, the selective advantage of mycorrhizal plants will disappear when an increase in the nutrient acquisition rate is not associated with a sufficiently high nutrient use efficiency of photosynthesis, as at high soil nutrient levels or due to a loss of leaf area, shading or low temperatures.

Mycorrhizal benefit in two low arctic herbs increases with increasing temperature

“…This is evident also in the present work. Decreasing PNUE is predicted to reduce plant C allocation to root symbionts and result in lower mycorrhizal colonization (Tuomi et al, 2001). Thus, the lower mycorrhizal colonization intensity at 128C could theoretically be explained by the lower PNUE at 128C.…”

A model for optimal mycorrhizal colonization along altitudinal gradients

“…Consequently, plants are predicted to be mycorrhizal only if the net carbon gain of mycorrhizal plants is expected to be higher than that of non-mycorrhizal plants. This is a plausible assumption in conditions where mycorrhizas represent mutualistic symbiosis and mycorrhizal fungi hence do not function as parasitic symbionts (for a discussion, see Johnson et al 1997, Tuomi et al 2001. However, this may be a simplifi ed assumption because mycorrhizal plants have not always been found to derive any benefi t from mycorrhizal associations (e.g.…”

“…If α assumes smaller values, C will decrease as a function of p. In other words, in terms of the net carbon gain, the nutrient use effi ciency of photosynthesis determines whether a mycorrhizal condition (p = 1) or a completely non-mycorrhizal condition (p = 0) would be most economical for the carbon balance of the plant (see also Fitter 1991, Tuomi et al 2001. We used the kinetics of nutrient uptake at different soil nutrient concentrations to determine the nutritional benefi ts, i.e.…”

“…is the total nutrient gain of the whole plant, and the last term R (p C m + (1 -p) C nm ) represents the carbon loss to the root system (Tuomi et al 2001). The two main terms on the right-hand side of Eq.…”

Defoliation negatively affects plant growth and the ectomycorrhizal community of Pinus pinaster in Spain

“…Actually, loss of foliage may increase or decrease the relative advantage of symbiosis depending on the cost efficiency (i.e. the ratio between carbon expended belowground/nutrient acquired) of nutrient acquisition and the value of the acquired nutrients for the net primary production of the tree (Tuomi et al 2001). Defoliation of mature needles during the growing season usually strongly affects conifer growth, because it involves the loss of a great part of carbon and nitrogen resources (Saravesi et al 2008).…”