Reciprocal exchange of limiting resources as a mechanism for the maintenance of mycorrhizal mutualism

Background/Question/Methods

The majority of land plants form symbiotic associations with arbuscular mycorrhizal (AM) fungi, but mechanisms underlying the persistence of this ancient symbiosis remain obscure.  Recent evidence demonstrates that host plant is able to allocate more carbon toward the most effective mutualist and preferential allocation has therefore been suggested as a mechanism for the maintenance of mutualism.  It is unclear how preferential allocation is triggered and regulated.  We hypothesized that the strength of preferential allocation is tightly aligned with the differential benefits (e.g. phosphorus) provided by co-existing fungal partners.  In greenhouse, we quantitatively evaluated the relationship between carbon allocation and phosphorus uptake across a gradient of soil phosphorus availability.  We used a split root system in which roots of Allium vineale were divided into two pots with different AM fungal species: a beneficial Glomus candidum and a non-beneficial Gigaspora decipiens.  Soil phosphorus in both pots was manipulated to 1X, 2X, or 4X of background level.  Each side of the pots was labeled with either P-32 or P-33, and plant shoot was labeled with C-14. Carbon allocation and phosphorus uptake were quantified based on the radioactivities of P-32 and P-33 in shoot and C-14 in roots measured upon harvest.

Results/Conclusions

With the split root design and the three way radioactive labeling, we were able to simultaneously measure the bidirectional exchange of resources between a single host plant and two different fungal partners across a soil nutrient gradient.  Our data showed that the beneficial AM fungus Gl. candidum delivered an average of 39.98 times more phosphorus to the plants than the non-beneficial Gi. decipiens did, and host plant A. vineale allocated  3.09 times more carbon to Gl. candidum than to Gi. decipiens.  There was a weak but significant correlation between the differential carbon allocation from the plant and the differential phosphorus delivery to the plant.  We also found that the increase in soil P availability negatively impacted both carbon allocation and phosphorus uptake.  When soil phosphorus availability was elevated from 1X to 2X and 4X, preferential allocation of carbon disappeared; the difference in phosphorus uptake between beneficial and non-beneficial fungi reduced significantly.  Our findings suggest that plant carbon allocation is in reciprocity with mycorrhizal phosphorus uptake.  It is unknown whether carbon allocation triggers phosphorus uptake, or vice versa, but the direction of this reciprocal exchange of resources between plants and symbiotic fungi in a phosphorus limiting environment clearly favors more beneficial mutualists.