Plants and their arbuscular mycorrhizal fungal symbionts interact in complex underground networks involving multiple partners. This increases the potential for exploitation and defection by individuals, raising the question of how partners maintain a fair, two-way transfer of resources. We manipulated cooperation in plants and fungal partners to show that plants can detect, discriminate, and reward the best fungal partners with more carbohydrates. In turn, their fungal partners enforce cooperation by increasing nutrient transfer only to those roots providing more carbohydrates. On the basis of these observations we conclude that, unlike many other mutualisms, the symbiont cannot be "enslaved." Rather, the mutualism is evolutionarily stable because control is bidirectional, and partners offering the best rate of exchange are rewarded.
The arbuscular mycorrhizal (AM) symbiosis, formed between the majority of land plants and ubiquitous soil fungi of the phylum Glomeromycota, is responsible for massive nutrient transfer and global carbon sequestration. AM fungi take up nutrients from the soil and exchange them against photosynthetically fixed carbon (C) from the host. Recent studies have demonstrated that reciprocal reward strategies by plant and fungal partners guarantee a "fair trade" of phosphorus against C between partners [Kiers ET, et al. (2011) Science 333:880-882], but whether a similar reward mechanism also controls nitrogen (N) flux in the AM symbiosis is not known. Using mycorrhizal root organ cultures, we manipulated the C supply to the host and fungus and followed the uptake and transport of N sources in the AM symbiosis, the enzymatic activities of arginase and urease, and fungal gene expression in the extraradical and intraradical mycelium. We found that the C supply of the host plant triggers the uptake and transport of N in the symbiosis, and that the increase in N transport is orchestrated by changes in fungal gene expression. N transport in the symbiosis is stimulated only when the C is delivered by the host across the mycorrhizal interface, not when C is supplied directly to the fungal extraradical mycelium in the form of acetate. These findings support the importance of C flux from the root to the fungus as a key trigger for N uptake and transport and provide insight into the N transport regulation in the AM symbiosis.arbuscular mycorrhiza | arginine catabolism | carbon transport | Glomus intraradices | urea cycle T he arbuscular mycorrhizal (AM) symbiosis plays a key role in nutrient uptake in the majority of land plants, including such important crop species as corn, soybean, and rice. The AM symbiosis can increase the uptake of phosphate (P) and nitrogen (N), as well as of trace elements such as copper and zinc, and improves the abiotic and biotic stress resistance of the host (2). Previous work has focused primarily on the transport of P in AM symbiosis, but more recent work has highlighted the potential importance of N uptake by fungal symbionts (3, 4). The extraradical mycelium (ERM) of the fungus is able to take up NH 4 + (5, 6), NO 3 − (5-7), and organic N resources (3-5) from the soil and to transfer N to the host. The high mobility of N in the soil has raised the question of whether AM fungi can contribute significantly to the N nutrition of the host (8). It has been suggested that an improved N status of mycorrhizal plants may be simply a consequence of an improved P nutrition (9); however, other studies have demonstrated that AM fungi can deliver substantial amounts of N to the host, with an estimated 21% of total N taken up by the fungal ERM in root organ cultures (10) and 74% of the total N in the leaves of Zea mays coming from the fungal ERM with access to urea (11).Current models of N transport in the AM symbiosis involve uptake of inorganic N from the soil and N assimilation via the anabolic arm of the urea...
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