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Reciprocity maintains cooperation between plants and mycorrhizal fungi

Mycorrhizal fungi attach to plant roots and trade phosphorus (and sometimes other benefits) for photosynthates. But is it really "trade"? In other words, if one partner defects, will the other continue its contribution? A recent paper in Science, by Toby Kiers and colleagues, shows that the term, "trade" is justified.(Kiers et al. 2011)

Earlier, as my first PhD student, Toby showed that symbiotic rhizobia, living inside soybean root nodules, can't stop supplying the plant with nitrogen without suffering a decrease in their own fitness.(Kiers et al. 2003) We called the plant response "sanctions", although this could be misinterpreted as an attempt by the plant to improve the behavior of the rhizobia. We assume that the behavior of a given rhizobial genotype is programmed by its DNA, but sanctions against less-beneficial strains will decrease their frequency in subsequent generations. More recently, Ryoko Oono demonstrated a subtler form of sanctions against potentially reproductive rhizobia when their nonreproductive clonemates stop fixing nitrogen.(Oono et al. 2011)

Different strains of rhizobia on the same plant are (mostly) segregated in different root nodules, so "shutting down" one nodule preferentially hurts a single strain of rhizobia. But multiple strains of mycorrhizal fungus typically infect the same root. Can plants preferentially allocate resources to the most-beneficial fungi? Jim Bever and colleagues showed that they can, when different strains are attached to different parts of the root, but apparently not when the strains are more mixed.(Bever et al. 2009) Results from Kiers' group, however, suggest that mixing is not a problem.

They grew Medicago truncatula (a model species related to alfalfa) with mixtures of mycorrhizal fungi that they classified as more- or less-beneficial. To track photosynthate allocation, they let plant photosynthesis take up carbon dioxide containing the heavier 13C isotope of carbon. To see which fungi got more of this carbon, they used a clever technique.

They extracted RNA from the fungi and separated it into lighter and heavier (more-recent-plant-carbon) fractions, using a centrifuge. Then they used difference in the RNA base sequences of their different fungi to measure their relative representation in the light and heavy fractions. Fungi with greater representation in the heavy fraction were getting more recently supplied carbon from the plant, so they were benefiting more from symbiosis. A more-beneficial fungal species got more carbon than either of two less-beneficial species. This result is consistent with host sanctions (or, since each fungus interacts with multiple plants, with a "biological market" where individuals trade more with those that offer the best deal).

It's hard to measure all of the benefits a mycorrhizal fungus provides, however, so they also manipulated the exchange of specific resources. The species they classified as more beneficial got more carbon when it had access to more phosphorus, and presumably supplied it to the plant. A less-beneficial species didn't get more carbon when it had access to more phosphorus, perhaps because it didn't give much of the phosphorus to the plant. Similarly, the cooperative strain apparently responded to differences in carbon supply from the plant, allocating more phosphorus to where it was getting more carbon. So sanctions appear to go both ways.

LITERATURE CITED

Bever J. D., S. C. Richardson, B. M. Lawrence, J. Holmes, and M. Watson. 2009. Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecology Letters 12:13-21.

Kiers E. T., M. Duhamel, Y. Yugandgar, J. A. Mensah, O. Franken, E. Verbruggen, C. R. Felbaum, G. A. Kowalchuk, M. M. Hart, A. Bago, T. M. Palmer, S. A. West, P. Vandenkoornhuyse, J. Jansa, and H. B├╝cking. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880-882.

Kiers E. T., R. A. Rousseau, S. A. West, and R. F. Denison. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.

Oono R., C. G. Anderson, and R. F. Denison. 2011. Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proceedings of the Royal Society B 278:2698-2703.

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