Abstract
Rising concentrations of carbon dioxide (CO2) is likely to have important effects on growth and development of plants and on their relationship with symbiotic microbes. A rise in CO2 could increase demand by plant hosts for nutrient resources, which may increase host investments in beneficial symbionts. In the legume-rhizobia mutualism, while elevated CO2 is often associated with increased nodule growth and investment in N2-fixing rhizobia, it is yet unclear if this response depends on the mutualistic quality of the rhizobia. To test if host carbon allocation towards more-beneficial nodules are similar to less-beneficial (but still effective) nodules when plant N demand changes, we manipulated plant C and N status with elevated CO2 and additional nitrate. We used two isogenic Rhizobium etli strains that differ in their ability to synthesize an energy reserve compound, poly-beta-hydroxybutyrate (PHB), as well as their efficiencies for nitrogen fixation and nodulation rates, resulting in two Phaseolus vulgaris host groups with either large number of small nodules or small number of large nodules. The addition of nitrate negatively affected carbon allocation towards nodules, and elevated CO2 reversed this effect, as expected. However, this alleviation of nodule inhibition was greater on plants that started with greater numbers of smaller nodules. If smaller nodules indicate less-efficient or low-fixing rhizobia, this study suggests that increased demand for nitrogen in the face of elevated CO2 has the potential to disproportionately favor less-beneficial strains and increase variation of nitrogen fixation quality among rhizobia.
Highlights
Nitrogen fixation is one of the most important metabolic reactions for life on Earth (Canfield et al 2010)
When plants are infected by multiple strains (Kiers et al 2013) or have alternative sources of nitrogen (Streeter and Wong 1988) or when rhizobia can manipulate host carbon allocation (Ratcliff and Denison 2009), the fitnesses of host and symbiont may not align and the mutualistic traits may no longer be under strong selection for either species (Heath and Stinchcombe 2014)
Plants appear to “loosen their hold” of their carbon in the face of elevated CO2, as exemplified by the increase in nodule weights without detectable increases in fixed nitrogen in plants that were inoculated with the less-efficient strain (Fig. 5)
Summary
Nitrogen fixation is one of the most important metabolic reactions for life on Earth (Canfield et al 2010) This chemical reaction is performed solely by prokaryotic microbes and is further selected by macro-hosts, such as plants or termites, that depend on the symbiotic associations with these microbes for nitrogen (Mylona et al 1995). A product of this host selection, or “host sanctions” (sensu West et al 2002), is the positive alignment (i.e., correlation) between legume and rhizobial fitness during singlestrain inoculation because plants with highly-beneficial nodules grow more (i.e., have higher fitness) themselves and allocate more carbon to their nodules (i.e., increasing fitness of the rhizobia; Friesen 2012; Kiers et al 2013). When plants are infected by multiple strains (Kiers et al 2013) or have alternative sources of nitrogen (Streeter and Wong 1988) or when rhizobia can manipulate host carbon allocation (Ratcliff and Denison 2009), the fitnesses of host and symbiont may not align (i.e., a more fit plant does not necessarily have uniformly larger nodules than a less fit plant; Sachs and Simms 2006) and the mutualistic traits may no longer be under strong selection for either species (Heath and Stinchcombe 2014)
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