Cell autonomous sanctions in legumes target ineffective rhizobia in nodules with mixed infections

Regus, John U.; Quides, Kenjiro W.; O’Neill, Matthew R.; Suzuki, Rina; Savory, Elizabeth A.; Chang, Jeff H.; Sachs, Joel

doi:10.3732/ajb.1700165

Cited by 65 publications

(99 citation statements)

References 90 publications

(182 reference statements)

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“…In this case, the presence of multiple nodules on a plant and/or multiple bacteroids within a nodule could lead to bargaining power asymmetry. This mechanism could be particularly important if bacteroids within nodules bargain independently with the plant; this is consistent with the plant being able to interact differently with different bacteroids within a nodule (Daubech et al ., ; Regus et al ., ). Each of these mechanisms can explain why the plant has more bargaining power than the rhizobia, but alone they do not explain why plant bargaining power appears to be higher when nitrogen is scarce (for example 8 mg l −1 N).…”

Section: Discussionmentioning

confidence: 99%

Unfair trade underground revealed by integrating data with Nash bargaining models

et al. 2019

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Summary Mutually beneficial resource exchange is fundamental to global biogeochemical cycles and plant and animal nutrition. However, there is inherent potential conflict in mutualisms, as each organism benefits more when the exchange ratio (‘price’) minimizes its own costs and maximizes its benefits. Understanding the bargaining power that each partner has in these interactions is key to our ability to predict the exchange ratio and therefore the functionality of the cell, organism, community and ecosystem. We tested whether partners have symmetrical (‘fair’) or asymmetrical (‘unfair’) bargaining power in a legume–rhizobia nitrogen‐fixing symbiosis using measurements of carbon and nitrogen dynamics in a mathematical modeling framework derived from economic theory. A model of symmetric bargaining power was not consistent with our data. Instead, our data indicate that the growth benefit to the plant (Medicago truncatula) has greater weight in determining trade dynamics than the benefit to the bacteria. Quantitative estimates of the relative power of the plant revealed that the plant's influence rises as soil nitrogen availability decreases and trade benefits to both partners increase. Our finding that M. truncatula legumes have more bargaining power than their rhizobial partner at lower nitrogen availabilities highlights the importance of context‐dependence for the evolution of mutualism with increasing nutrient deposition.

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Section: Discussionmentioning

confidence: 99%

Unfair trade underground revealed by integrating data with Nash bargaining models

et al. 2019

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“…Fix À rhizobia can impose important costs on hosts, resulting in a 12-28% reduction of leaf nitrogen content . However, legumes can sanction (Box 1) Fix À rhizobia by causing these nodules to senesce prematurely, significantly reducing fitness of the rhizobia (Sachs et al, 2010b;Oono et al, 2011;Regus et al, 2017a). A key step during nodule senescence is the neutralization of the peribacteroid space (Box 1) that surrounds the symbiosome, an otherwise acidic environment which facilitates import of host resources (Pierre et al, 2013).…”

Section: Control and Conflict Over Nodule Growth And Senescencementioning

confidence: 99%

Legumes versus rhizobia: a model for ongoing conflict in symbiosis

2018

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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.

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“…Flow cytometry data were used to select diploid and neotetraploid plants for confocal microscopy. One to three mature nodules were harvested from each plant 34 days post-infection into 80 mm PIPES buffer and sectioned longitudinally into thin slices using a double-edged razor blade (Haynes et al, 2004;Regus et al, 2017). Nodule sections were stained in 1 μL ml −1 SYTO 13 for 15 min and then mounted onto slides and sealed with coverslips for confocal processing (Haynes et al, 2004).…”

Section: Confocal Microscopymentioning

confidence: 99%

“…Although legume taxa differ in nodule morphology (Sprent, 2007), nodule development can be broadly categorized as determinate or indeterminate. Determinate nodules grow to a certain stage of development and then senesce, whereas indeterminate nodules are defined by continuous growth (Sprent, 2007;Regus et al, 2017). The continual growth of indeterminate nodules results in distinct regions within nodules, including a persistent meristem, interzone, N-fixation zone, and senescence zone (Haynes et al, 2004).…”

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Autopolyploidy alters nodule‐level interactions in the legume–rhizobium mutualism

Forrester

Ashman

2019

American J of Botany

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Premise Polyploidy is a major genetic driver of ecological and evolutionary processes in plants, yet its effects on plant interactions with mutualistic microbes remain unresolved. The legume–rhizobium symbiosis regulates global nutrient cycles and plays a role in the diversification of legume species. In this mutualism, rhizobia bacteria fix nitrogen in exchange for carbon provided by legume hosts. This exchange occurs inside root nodules, which house bacterial cells and represent the interface of legume–rhizobium interactions. Although polyploidy may directly impact the legume–rhizobium mutualism, no studies have explored how it alters the internal structure of nodules. Methods We created synthetic autotetraploids using Medicago sativa subsp. caerulea. Neotetraploid plants and their diploid progenitors were singly inoculated with two strains of rhizobia, Sinorhizobium meliloti and S. medicae. Confocal microscopy was used to quantify internal traits of nodules produced by diploid and neotetraploid plants. Results Autotetraploid plants produced larger nodules with larger nitrogen fixation zones than diploids for both strains of rhizobia, although the significance of these differences was limited by power. Neotetraploid M. sativa subsp. caerulea plants also produced symbiosomes that were significantly larger, nearly twice the size, than those present in diploids. Conclusions This study sheds light on how polyploidy directly affects a plant–bacterium mutualism and uncovers novel mechanisms. Changes in plant–microbe interactions that directly result from polyploidy likely contribute to the increased ability of polyploid legumes to establish in diverse environments.

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Cell autonomous sanctions in legumes target ineffective rhizobia in nodules with mixed infections

Abstract: Our data suggest an elegant cell autonomous mechanism by which legumes can detect and defend against ineffective rhizobia even when nodules harbor a mix of effective and ineffective rhizobial genotypes.

Cited by 65 publications

References 90 publications

Unfair trade underground revealed by integrating data with Nash bargaining models

Unfair trade underground revealed by integrating data with Nash bargaining models

Legumes versus rhizobia: a model for ongoing conflict in symbiosis

Autopolyploidy alters nodule‐level interactions in the legume–rhizobium mutualism

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