Abstract
In legume-Rhizobium symbioses, specialised soil bacteria fix atmospheric nitrogen in return for carbon. However, ineffective strains can arise, making discrimination essential. Discrimination can occur via partner choice, where legumes prevent ineffective strains from entering, or via sanctioning, where plants provide fewer resources. Several studies have inferred that legumes exercise partner choice, but the rhizobia compared were not otherwise isogenic. To test when and how plants discriminate ineffective strains we developed sets of fixing and non-fixing strains that differed only in the expression of nifH – essential for nitrogen fixation – and could be visualised using marker genes. We show that the plant is unable to select against the non-fixing strain at the point of entry, but that non-fixing nodules are sanctioned. We also used the technique to characterise mixed nodules (containing both a fixing and a non-fixing strain), whose frequency could be predicted using a simple diffusion model. We discuss that sanctioning is likely to evolve in preference to partner choice in any symbiosis where partner quality cannot be adequately assessed until goods or services are actively exchanged.
Highlights
Across the globe primary productivity is nitrogen limited[1]
In the legume-Rhizobium symbiosis, nitrogen fixation does not begin until the bacteria have entered the roots and nodule formation is sufficiently advanced for rhizobia to have differentiated into nitrogen-fixing bacteroids[8]
We created a non-fixing but otherwise isogenic mutant to mimic a process that might occur in nature, where a mutation arises in a fixing rhizobial strain, rendering it ineffective
Summary
Across the globe primary productivity is nitrogen limited[1]. This limitation has been overcome for plants in the family Fabaceae (commonly known as legumes) through a mutualistic association with nitrogen-fixing bacteria collectively called rhizobia[2]. Plants acquire rhizobia from the soil through an intricate signalling process in which bacteria enter specialized root nodules, where they fix nitrogen in return for plant-derived carbon[8] This horizontal transmission means that rhizobial fitness is not perfectly aligned with the fitness of the host plant[7]. A range of traits affects competitiveness: examples include motility[22], production of antibiotics[23] and the secretion of proteins and polysaccharides involved in biofilm formation and root attachment[24] Such differences in competitiveness explain why poorly-fixing strains can end up occupying a higher proportion of nodules – a problem that is often encountered when developing effective strains for use in agricultural settings[4, 25, 26]. Comparing the nodulation success of naturally occurring strains is difficult to interpret as a test of partner choice
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