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Plants punish cheaters' relatives

This week's paper is the fourth from Ryoko Oono's PhD thesis. "Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates" was just published on-line in Proceedings of the Royal Society.
Rhizobia are bacteria that can live either in soil or in root nodules, like those shown above. Legume plants (alfalfa, soybean, the lupines loved by Monty Python and many wild species) let rhizobia in because the rhizobia (usually) convert atmospheric nitrogen into forms the plant can use.

But what if the rhizobia don't deliver? What if, once established inside a nodule, they use plant resources only for their own reproduction? In my most-cited paper, Toby Kiers showed that soybean plants impose fitness-reducing "sanctions" on rhizobia that fail to fix nitrogen. Ellen Simms' lab found similar results with wild lupines. But Ryoko had three good reasons to question whether certain legumes, including alfalfa and pea, impose sanctions similar to soybean's.

A key difference is that, in alfalfa and pea nodules, rhizobia lose the ability to reproduce when they become the nitrogen-fixing, bacteroid form. Earlier, Ryoko showed that legumes have repeatedly evolved the ability to suppress bacteroid reproduction, apparently because it increases the efficiency with which bacteroids use plant carbon to fix nitrogen from the atmosphere. If a soybean plant cuts off resources to a bacteroid that isn't fixing nitrogen, that bacteroid is less likely to survive and reproduce. But bacteroids in alfalfa nodules can't reproduce anyway.

One obvious question is, why do rhizobia infect alfalfa roots, if they'll lose the ability to reproduce? The answer is that rhizobia that can infect alfalfa don't usually have the option of infecting soybeanm where bacteroids remain reproductive, instead. They could just stay in the soil, but they reproduce much more inside nodules -- often a million-fold or more, even after subtracting those that lose the ability to reproduce by becoming bacteroids.

Given this difference, why did sanctions seem somewhat less likely in alfalfa nodules (hosting nonreproductive bacteroids) than in soybean nodules (hosting reproductive bacteroids)?

First, because reproductive bacteroids, like those in soybean nodules, might be more likely to "cheat." They can cheat simply by hoarding plant resources for their own reproduction, rather than using those resources to power the nitrogen fixation that benefits their plant host. But why would a nonreproductive bacteroid hoard resources? They can't take it with them when they die. If rhizobia that cheat alfalfa are rare, would natural selection in alfalfa populations still maintain the ability to impose sanctions? Maybe. Nonreproductive bacteroids do still have some cheating options, such as diverting plant resources to their reproductive clonemates in the same nodule, perhaps via chemicals called rhizopines. Also, some nonfixing rhizobia could just be defective mutants rather than strains whose cheating strategies have been honed by natural selection. Defective mutants might be just as common in species with nonreproductive bacteroids.

Second, cutting off resources to nonfixing bacteroids wouldn't necessarily reduce the fitness of their reproductive clonemates in the same nodule. To qualify as sanctions, by our definition, plants would also have to cut off resources to those clonemates, like a tyrannical government punishing the relatives of insurgents. Of course, the plants are just reducing their losses, with fitness effects on the rhizobia as a side-effect.

Third, two published studies of Medicago truncatula, a wild relative of alfalfa, concluded that it doesn't impose sanctions.

Nonetheless, Ryoko found that nodules prevented from fixing nitrogen -- she used a nitrogen-free, argon/oxygen atmosphere -- grew less (lower two panels in photo) and contained less than half as many rhizobia, relative to the same strain allowed to fix nitrogen. So alfalfa does impose sanctions after all, perhaps cutting off resources to an entire nodule when it fails to fix nitrogen. She got similar results with pea, which also hosts nonreproductive bacteroids.

What about those published results that didn't find sanctions? Heath and Tiffin (2009) compared three strains, but maybe none of them performed poorly enough to trigger sanctions. (Earlier, Toby Kiers found that minor cheating doesn't necessarily trigger sanctions.) Gubry-Rangin found less nodule growth with a nonfixing strain (consistent with our results, inconsistent with Heath and Tiffin) but no difference in the number of rhizobia inside (inconsistent with our results). It seems odd that a smaller nodule would have just as many rhizobia inside, but maybe there's something interesting going on. I expect there will be more to this story.

Our research on cooperation and conflict in the symbiosis between legumes and rhizobia has been supported by the National Science Foundation, most recently by grant NSF/IOS-0918986.

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