Abstract
The costs and benefits that define gain from trade in resource mutualisms depend on resource availability. Optimal partitioning theory predicts that allocation to direct uptake versus trade will be determined by both the relative benefit of the resource acquired through trade and the relative cost of the resource being traded away. While the costs and benefits of carbon:nitrogen exchange in the legume–rhizobia symbiosis have been examined in depth with regards to mineral nitrogen availability, the effects of varying carbon costs are rarely considered. Using a growth chamber experiment, we measured plant growth and symbiosis investment in the model legume Medicago truncatula and its symbiont Ensifer medicae across varying nitrogen and light environments. We demonstrate that plants modulate their allocation to roots and nodules as their return on investment varies according to external nitrogen and carbon availabilities. We find empirical evidence that plant allocation to nodules responds to carbon availability, but that this depends upon the nitrogen environment. In particular, at low nitrogen—where rhizobia provided the majority of nitrogen for plant growth—relative nodule allocation increased when carbon limitation was alleviated with high light levels. Legumes’ context-dependent modulation of resource allocation to rhizobia thus prevents this interaction from becoming parasitic even in low-light, high-nitrogen environments where carbon is costly and nitrogen is readily available.
Highlights
Interactions between plants and microbial symbionts are major drivers of global nutrient cycles and play vital roles in the productivity of natural and agricultural ecosystems (van der Heijden et al, 2008)
Cheap Carbon Increases Symbiosis Investment as mutualistic, with the symbiosis increasing fitness for both partners (Bronstein, 2015), theory predicts that symbioses exist along a gradient from mutualism to parasitism depending on the environmental context (Bronstein, 1994; Johnson et al, 1997; Bronstein, 2001; Neuhauser and Fargione, 2004)
One key factor that may shift an interaction along the mutualism–parasitism continuum is the availability of the traded resources in the environment
Summary
Interactions between plants and microbial symbionts are major drivers of global nutrient cycles and play vital roles in the productivity of natural and agricultural ecosystems (van der Heijden et al, 2008). Soil bacteria known as rhizobia can colonize plant roots and induce the formation of nodules, inside of which the rhizobia fix an estimated 40 million tons of plant-inaccessible nitrogen from the atmosphere in exchange for photosynthetic carbon and other nutrients required for growth and metabolism (Udvardi and Poole, 2013). In the presence of externally supplied nitrogen, the plant may be able to minimize the costs associated with less beneficial rhizobia by reducing or eliminating its allocation of resources to the microbes
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