IPD3 Controls the Formation of Nitrogen-Fixing Symbiosomes in Pea and <i>Medicago</i> Spp.

Ovchinnikova, Evgenia; Journet, Etienne-Pascal; Chabaud, Mireille; Cosson, Viviane; Ratet, Pascal; Duc, Gérard; Fedorova, Elena; Liu, Wei; Camp, Rik Op den; Zhukov, Vladimir A.; Тихонович, И. А.; Borisov, A. Y.; Bisseling, Ton; Limpens, Erik

doi:10.1094/mpmi-01-11-0013

Cited by 144 publications

(111 citation statements)

References 61 publications

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“…The late symbiotic event of nodule cell infection is tightly coupled to nodulation, rendering its specific analysis difficult. A genetic link between nodulation/IT formation and nodule cell infection was also evidenced on the plant side as two genes of the Nod factor signaling pathway, the leucine-richrepeat-containing receptor kinase DMI2 and the calcium-and calmodulin-dependent kinase DMI3 interacting protein IPD3, were shown to be required for symbiosome formation (Capoen et al, 2005;Limpens et al, 2005;Ovchinnikova et al, 2011). Our findings on the bacterial side provide new clues on nodulation-intracellular infection relationships by pointing to a common control for bacterial invasion at the early nodulation/root hair infection and the late nodule cell entry levels ( Figure 3b).…”

Section: Discussionmentioning

confidence: 95%

Experimental evolution of nodule intracellular infection in legume symbionts

et al. 2013

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Soil bacteria known as rhizobia are able to establish an endosymbiosis with legumes that takes place in neoformed nodules in which intracellularly hosted bacteria fix nitrogen. Intracellular accommodation that facilitates nutrient exchange between the two partners and protects bacteria from plant defense reactions has been a major evolutionary step towards mutualism. Yet the forces that drove the selection of the late event of intracellular infection during rhizobium evolution are unknown. To address this question, we took advantage of the previous conversion of the plant pathogen Ralstonia solanacearum into a legume-nodulating bacterium that infected nodules only extracellularly. We experimentally evolved this draft rhizobium into intracellular endosymbionts using serial cycles of legume-bacterium cocultures. The three derived lineages rapidly gained intracellular infection capacity, revealing that the legume is a highly selective environment for the evolution of this trait. From genome resequencing, we identified in each lineage a mutation responsible for the extracellular-intracellular transition. All three mutations target virulence regulators, strongly suggesting that several virulence-associated functions interfere with intracellular infection. We provide evidence that the adaptive mutations were selected for their positive effect on nodulation. Moreover, we showed that inactivation of the type three secretion system of R. solanacearum that initially allowed the ancestral draft rhizobium to nodulate, was also required to permit intracellular infection, suggesting a similar checkpoint for bacterial invasion at the early nodulation/root infection and late nodule cell entry levels. We discuss our findings with respect to the spread and maintenance of intracellular infection in rhizobial lineages during evolutionary times.

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Section: Discussionmentioning

confidence: 95%

Experimental evolution of nodule intracellular infection in legume symbionts

et al. 2013

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“…Furthermore, in nodules, this common signaling pathway is also essential for the release of the rhizobia from infection threads (symbiosome formation), but not for infection thread formation. This result has been demonstrated for the receptor-like kinase SymRK, the calcium-and calmodulin-dependent kinase, as well as its interacting partner (IPD3) (15)(16)(17)(18)(19)(20). It is currently not known whether this common signaling pathway is activated by Nod-factor receptors in legume nodules.…”

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confidence: 90%

Rhizobium –legume symbiosis shares an exocytotic pathway required for arbuscule formation

Ivanov

Fedorova

Limpens

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Endosymbiotic interactions are characterized by the formation of specialized membrane compartments, by the host in which the microbes are hosted, in an intracellular manner. Two well-studied examples, which are of major agricultural and ecological importance, are the widespread arbuscular mycorrhizal symbiosis and the Rhizobium-legume symbiosis. In both symbioses, the specialized host membrane that surrounds the microbes forms a symbiotic interface, which facilitates the exchange of, for example, nutrients in a controlled manner and, therefore, forms the heart of endosymbiosis. Despite their key importance, the molecular and cellular mechanisms underlying the formation of these membrane interfaces are largely unknown. Recent studies strongly suggest that the Rhizobium-legume symbiosis coopted a signaling pathway, including receptor, from the more ancient arbuscular mycorrhizal symbiosis to form a symbiotic interface. Here, we show that two highly homologous exocytotic vesicle-associated membrane proteins (VAMPs) are required for formation of the symbiotic membrane interface in both interactions. Silencing of these Medicago VAMP72 genes has a minor effect on nonsymbiotic plant development and nodule formation. However, it blocks symbiosome as well as arbuscule formation, whereas root colonization by the microbes is not affected. Identification of these VAMP72s as common symbiotic regulators in exocytotic vesicle trafficking suggests that the ancient exocytotic pathway forming the periarbuscular membrane compartment has also been coopted in the Rhizobium-legume symbiosis.infection thread | unwalled infection droplet

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“…2C). To further support that medicago type-A RR genes are targets of the cytokinin phosphorelay pathway, we isolated RNA from medicago roots transformed with the gain-of-function MtCRE1 construct (35S:MtCRE1* [L267F]), which causes spontaneous nodule formation (Ovchinnikova et al, 2011). Quantitative reverse transcriptase (RT)-PCR on root RNA showed that, of all type-A RR genes, MtRR9 was most strongly induced and also that MtRR4, MtRR5, MtRR8, and MtRR11 were activated (Fig.…”

Section: And B)mentioning

confidence: 99%

“…The MtRR9 RNAi target sequence was cloned into the DsRed modified gateway vector pK7GWIWG2(II) driven by the CaMV35S promoter as described by Limpens et al (2005). 35S:MtCRE1*[L267F] was used as described by Ovchinnikova et al (2011).…”

Section: Vectors and Constructsmentioning

confidence: 99%

“…Genetic integration of the cytokinin phosphorelay pathway in Nod factor signaling is best demonstrated by gain-of-function and loss-of-function mutants of the His kinase cytokinin receptor (HK) LjLHK1/ MtCRE1 in lotus and medicago (Medicago truncatula). A functional LjLHK1/MtCRE1 gene is indispensable for nodule formation, and a dominant positive mutation in the receiver domain even leads to spontaneous nodule formation (Gonzalez-Rizzo et al, 2006;Murray et al, 2007;Tirichine et al, 2007;Ovchinnikova et al, 2011;Plet et al, 2011). Spontaneous nodulation driven by the gain-of-function HK mutant requires other components of the Nod factor-induced signaling pathway (e.g.…”

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confidence: 99%

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A Phylogenetic Strategy Based on a Legume-Specific Whole Genome Duplication Yields Symbiotic Cytokinin Type-A Response Regulators

et al. 2011

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Legumes host their Rhizobium spp. symbiont in novel root organs called nodules. Nodules originate from differentiated root cortical cells that dedifferentiate and subsequently form nodule primordia, a process controlled by cytokinin. A whole-genome duplication has occurred at the root of the legume Papilionoideae subfamily. We hypothesize that gene pairs originating from this duplication event and are conserved in distinct Papilionoideae lineages have evolved symbiotic functions. A phylogenetic strategy was applied to search for such gene pairs to identify novel regulators of nodulation, using the cytokinin phosphorelay pathway as a test case. In this way, two paralogous type-A cytokinin response regulators were identified that are involved in root nodule symbiosis. Response Regulator9 (MtRR9) and MtRR11 in medicago (Medicago truncatula) and an ortholog in lotus (Lotus japonicus) are rapidly induced upon Rhizobium spp. Nod factor signaling. Constitutive expression of MtRR9 results in arrested primordia that have emerged from cortical, endodermal, and pericycle cells. In legumes, lateral root primordia are not exclusively formed from pericycle cells but also require the involvement of the root cortical cell layer. Therefore, the MtRR9-induced foci of cell divisions show a strong resemblance to lateral root primordia, suggesting an ancestral function of MtRR9 in this process. Together, these findings provide a proof of principle for the applied phylogenetic strategy to identify genes with a symbiotic function in legumes.

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IPD3 Controls the Formation of Nitrogen-Fixing Symbiosomes in Pea and Medicago Spp.

Cited by 144 publications

References 61 publications

Experimental evolution of nodule intracellular infection in legume symbionts

Experimental evolution of nodule intracellular infection in legume symbionts

Rhizobium –legume symbiosis shares an exocytotic pathway required for arbuscule formation

A Phylogenetic Strategy Based on a Legume-Specific Whole Genome Duplication Yields Symbiotic Cytokinin Type-A Response Regulators

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