Legumes versus rhizobia: a model for ongoing conflict in symbiosis

Abstract

Contents Summary 1199 I. Introduction 1199 II. Selecting beneficial symbionts: one problem, many solutions 1200 III. Control and conflict over legume nodulation 1201 IV. Control and conflict over nodule growth and senescence 1204 V. Conclusion 1204 Acknowledgements 1205 References 1205 SUMMARY: The legume-rhizobia association is a powerful model of the limits of host control over microbes. Legumes regulate the formation of root nodules that house nitrogen-fixing rhizobia and adjust investment into nodule development and growth. However, the range of fitness outcomes in these traits reveals intense conflicts of interest between the partners. New work that we review and synthesize here shows that legumes have evolved varied mechanisms of control over symbionts, but that host control is often subverted by rhizobia. An outcome of this conflict is that both legumes and rhizobia have evolved numerous traits that can improve their own short-term fitness in this interaction, but little evidence exists for any net improvement in the joint trait of nitrogen fixation.

Environmental variation impacts trait expression and selection in the legume–rhizobium symbiosis

“…Different forms of selection on nodulation suggest that the benefit of nodulation is largely environment-dependent. Theoretically, the carbon cost of nodulation may begin to exceed the benefits of N fixation at a critical nodulation threshold (Sachs et al, 2018), and thus, could lead to stabilizing selection on nodulation. However, this critical nodulation threshold is likely contingent on factors that differ among environments, including the availability of N in the soil, the availability of rhizobia and other microbial partners, as well as the other plant species present.…”

“…In addition to influencing trait expression, the environment can have profound effects on selection. Studies often find strong positive selection for nodulation under N-limiting conditions (Simonsen and Stinchcombe, 2014b;Ossler et al, 2015;Batstone et al, 2017), whereas high N availability causes legumes to become less dependent on their rhizobial partners, potentially resulting in an adaptive decrease in nodulation (Sachs et al, 2018) and rhizobial quality (Weese et al, 2015;Klinger et al, 2016).…”

Legacy of prior host and soil selection on rhizobial fitness in planta

“…; Sachs et al. ). Several lines of evidence indicate that evolution in the soil is also important: rhizobia maintain genes necessary for free‐living growth on diverse substrates (Galibert et al.…”

“…In nodules with terminal bacteroid differentiation, such as those formed by Medicago , once inside the nodule, the bacterium divides and forms two subpopulations, a nonreproductive population that fixes nitrogen and a reproductive population that is released into the soil when the nodule senesces (reviewed in Sachs et al. ).…”

Role and exploitation of underground chemical signaling in plants

“…The second well‐studied case is that of the symbiosis between legumes and the Gram‐negative soil bacteria defined as ‘Rhizobia’ that can colonise the roots of legumes and induce the formation of specific structures, called root nodules . Within the nodules, bacteria differentiate into bacteriods and through nitrogen fixation convert atmospheric nitrogen (N 2 ) into a reduced form and make it available to the host .…”