Parasponia: a novel system for studying mutualism stability

Behm, Jocelyn E.; Geurts, René; Kiers, E. Toby

doi:10.1016/j.tplants.2014.08.007

Cited by 53 publications

(39 citation statements)

References 61 publications

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“…An open question is whether Parasponia nodulation is somehow less advanced than in legumes (Behm et al, 2014): our results point to similar levels of nodulation control as found in some legume species. Specifically, it has been shown that at high nitrogen levels, legumes can control nodule formation and mass-a process known as autoregulation of nodulation (Cho and Harper, 1991;Sueyoshi et al, 2003;Jeudy et al, 2010).…”

Section: Discussionsupporting

confidence: 75%

The Non-Legume Parasponia andersonii Mediates the Fitness of Nitrogen-Fixing Rhizobial Symbionts Under High Nitrogen Conditions

2020

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Organisms rely on symbiotic associations for metabolism, protection, and energy. However, these intimate partnerships can be vulnerable to exploitation. What prevents microbial mutualists from parasitizing their hosts? In legumes, there is evidence that hosts have evolved sophisticated mechanisms to manage their symbiotic rhizobia, but the generality and evolutionary origins of these control mechanisms are under debate. Here, we focused on the symbiosis between Parasponia hosts and N 2-fixing rhizobium bacteria. Parasponia is the only non-legume lineage to have evolved a rhizobial symbiosis and thus provides an evolutionary replicate to test how rhizobial exploitation is controlled. A key question is whether Parasponia hosts can prevent colonization of rhizobia under high nitrogen conditions, when the contribution of the symbiont becomes nonessential. We grew Parasponia andersonii inoculated with Bradyrhizobium elkanii under four ammonium nitrate concentrations in a controlled growth chamber. We measured shoot and root dry weight, nodule number, nodule fresh weight, nodule volume. To quantify viable rhizobial populations in planta, we crushed nodules and determined colony forming units (CFU), as a rhizobia fitness proxy. We show that, like legumes and actinorhizal plants, P. andersonii is able to control nodule symbiosis in response to exogenous nitrogen. While the relative host growth benefits of inoculation decreased with nitrogen fertilization, our highest ammonium nitrate concentration (3.75 mM) was sufficient to prevent nodule formation on inoculated roots. Rhizobial populations were highest in nitrogen free medium. While we do not yet know the mechanism, our results suggest that control mechanisms over rhizobia are not exclusive to the legume clade.

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Section: Discussionsupporting

confidence: 75%

The Non-Legume Parasponia andersonii Mediates the Fitness of Nitrogen-Fixing Rhizobial Symbionts Under High Nitrogen Conditions

2020

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“…They enabled unravelling gene loss linked to the lack of developing a symbiosis in certain plant lineages but also to identify new symbiosis genes (for arbuscular mycorrhizal symbiosis (Delaux et al ., 2014; Bravo et al ., 2016); for the nodulating symbiosis (Delaux et al ., 2015; Griesmann et al ., 2018). Comparative work on symbiotic plants is often hindered, however, either by the absence of closely related species which display gain or loss of symbiotic function or, when these are present, by the lack of a well-understood genetic framework, as outlined in Behm et al . (2014), Delaux et al .…”

Section: Discussionmentioning

confidence: 99%

“…(2016), Sprent (2017). Nevertheless, in the case of the nodulating Parasponia /non-nodulating Trema system, a fine comparative analysis was very powerful to demonstrate a parallel loss of the key symbiotic genes NFR5, NIN and RGP, in the non-nodulating species, challenging the long-standing assumption that Parasponia specifically acquired the potential to nodulate (Behm et al ., 2014; Geurts et al ., 2016; van Velzen et al ., 2018). In this respect, the uncovering of the genetic evolution of the genus Aeschynomene and related genera along with the identification of diploid species outside of the Nod-independent clade, provided a robust phylogenetic framework that can now be exploited to guide the choice of Nod-dependent diploid species for comparative genetic research.…”

Section: Discussionmentioning

confidence: 99%

A phylogenetic framework of the legume genusAeschynomenefor comparative genetic analysis of the Nod-dependent and Nod-independent symbioses

Brottier

Chaintreuil

Simion

et al. 2018

Preprint

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SUMMARYSome Aeschynomene legume species have the property of being nodulated by photosynthetic Bradyrhizobium lacking the nodABC genes. Knowledge of this unique Nod (factor)-independent symbiosis has been gained from the model A. evenia but our understanding remains limited due to the lack of comparative genetics with related taxa using a Nod-dependent process.To fill this gap, this study significantly broadened previous taxon sampling, including in allied genera, to construct a comprehensive phylogeny. This backbone tree was matched with data on chromosome number, genome size, low-copy nuclear genes and strengthened by nodulation tests and a comparison of the diploid species.The phylogeny delineated five main lineages that all contained diploid species while polyploid groups were clustered in a polytomy and were found to originate from a single paleo-allopolyploid event. In addition, new nodulation behaviours were revealed and Nod-dependent diploid species were shown to be tractable.The extended knowledge of the genetics and biology of the different lineages in the legume genus Aeschynomene provides a solid research framework. Notably, it enabled the identification of A. americana and A. patula as the most suitable species to undertake a comparative genetic study of the Nod-independent and Nod-dependent symbioses.

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“…In nonlegumes and early-diverging legumes, cracks in the root epidermis allow nitrogen-fixing bacteria to opportunistically colonize root interiors. In some host taxa the rhizobia form fixation threads (Box 1) in which they are only partially internalized in host cells (Behm et al, 2014;Sprent et al, 2017). By contrast, infection is highly coordinated in many derived legume taxa, in which root hairs curl and entrap compatible rhizobia, the rhizobia become encased by plant-derived membranes, and differentiated bacteroids live in tightly controlled organelle-like structures called symbiosomes (Box 1).…”

Section: Selecting Beneficial Symbionts: One Problem Many Solutionsmentioning

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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Parasponia: a novel system for studying mutualism stability

Cited by 53 publications

References 61 publications

The Non-Legume Parasponia andersonii Mediates the Fitness of Nitrogen-Fixing Rhizobial Symbionts Under High Nitrogen Conditions

The Non-Legume Parasponia andersonii Mediates the Fitness of Nitrogen-Fixing Rhizobial Symbionts Under High Nitrogen Conditions

A phylogenetic framework of the legume genusAeschynomenefor comparative genetic analysis of the Nod-dependent and Nod-independent symbioses

Legumes versus rhizobia: a model for ongoing conflict in symbiosis

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