The<i>Medicago truncatula</i>E3 Ubiquitin Ligase PUB1 Interacts with the LYK3 Symbiotic Receptor and Negatively Regulates Infection and Nodulation

Mbengue, Malick; Camut, Sylvie; Carvalho-Niebel, Fernanda de; Deslandes, Laurent; Froidure, Solène; Klaus-Heisen, Dörte; Moreau, Sandra; Rivas, Susana; Timmers, Ton; Hervé, Christine; Cullimore, Julie V.; Lefebvre, Benoît

doi:10.1105/tpc.110.075861

Cited by 156 publications

(132 citation statements)

References 63 publications

Supporting

Mentioning

124

Contrasting

Unclassified

Order By: Relevance

“…Indeed, the interaction between U-box type E3 ligases and kinases, especially receptor kinases with functions in diverse processes such as symbioses, self-incompatibility, and immunity, is a common theme (Gu et al, 1998;Samuel et al, 2008;Mbengue et al, 2010;Lu et al, 2011). Our study doesn't exclude the possibility that PUB22 is also controlled by additional kinases nor that MPK3 may regulate the activity of additional PUB E3s.…”

Section: Discussion Negative Regulatory Loops In the Immune Responsementioning

confidence: 79%

“…Similar interactions were suggested to extend to related E3s and kinases (Samuel et al, 2008). Additional examples include the phosphorylation of PUB1, PUB12, and PUB13 by receptor kinases (Mbengue et al, 2010;Lu et al, 2011). In spite of phosphorylation of PUB E3s being a recurrent phenomenon, it is not known how phosphorylation incorporates mechanistically into the activity of E3 ligases.…”

Section: Introductionmentioning

confidence: 86%

See 1 more Smart Citation

Changes in PUB22 Ubiquitination Modes Triggered by MITOGEN-ACTIVATED PROTEIN KINASE3 Dampen the Immune Response

et al. 2017

View full text Add to dashboard Cite

Crosstalk between posttranslational modifications, such as ubiquitination and phosphorylation, play key roles in controlling the duration and intensity of signaling events to ensure cellular homeostasis. However, the molecular mechanisms underlying the regulation of negative feedback loops remain poorly understood. Here, we uncover a pathway in Arabidopsis thaliana by which a negative feedback loop involving the E3 ubiquitin ligase PUB22 that dampens the immune response is triggered by MITOGEN-ACTIVATED PROTEIN KINASE3 (MPK3), best known for its function in the activation of signaling. PUB22's stability is controlled by MPK3-mediated phosphorylation of residues localized in and adjacent to the E2 docking domain. We show that phosphorylation is critical for stabilization by inhibiting PUB22 oligomerization and, thus, autoubiquitination. The activity switch allows PUB22 to dampen the immune response. This regulatory mechanism also suggests that autoubiquitination, which is inherent to most single unit E3s in vitro, can function as a self-regulatory mechanism in vivo.

show abstract

Section: Discussion Negative Regulatory Loops In the Immune Responsementioning

confidence: 79%

Section: Introductionmentioning

confidence: 86%

Changes in PUB22 Ubiquitination Modes Triggered by MITOGEN-ACTIVATED PROTEIN KINASE3 Dampen the Immune Response

et al. 2017

View full text Add to dashboard Cite

show abstract

“…Together, these observations corroborate our in vitro results showing kinase activity of purified NFR1 and also strengthen the conclusion that the NFR1 protein used for binding studies was folded and functional. Similar to NFR1 in A. thaliana, stable transgenic lines overexpressing LYK3 could not be obtained in Medicago (32).…”

Section: Discussionmentioning

confidence: 96%

Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding

Broghammer

Krusell

Blaise

et al. 2012

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

316

228

View full text Add to dashboard Cite

Lipochitin oligosaccharides called Nod factors function as primary rhizobial signal molecules triggering legumes to develop new plant organs: root nodules that host the bacteria as nitrogen-fixing bacteroids. Here, we show that the Lotus japonicus Nod factor receptor 5 (NFR5) and Nod factor receptor 1 (NFR1) bind Nod factor directly at high-affinity binding sites. Both receptor proteins were posttranslationally processed when expressed as fusion proteins and extracted from purified membrane fractions of Nicotiana benthamiana or Arabidopsis thaliana. The N-terminal signal peptides were cleaved, and NFR1 protein retained its in vitro kinase activity. Processing of NFR5 protein was characterized by determining the N-glycosylation patterns of the ectodomain. Two different glycan structures with identical composition, Man 3 XylFucGlcNAc 4 , were identified by mass spectrometry and located at amino acid positions N68 and N198. Receptor-ligand interaction was measured by using ligands that were labeled or immobilized by application of chemoselective chemistry at the anomeric center. High-affinity ligand binding was demonstrated with both solid-phase and free solution techniques. The K d values obtained for Nod factor binding were in the nanomolar range and comparable to the concentration range sufficient for biological activity. Structure-dependent ligand specificity was shown by using chitin oligosaccharides. Taken together, our results suggest that ligand recognition through direct ligand binding is a key step in the receptor-mediated activation mechanism leading to root nodule development in legumes.lysin motif proteins | plant-microbe interactions | symbiotic signalling | lysin motif receptor-like kinase | non-self recognition F ormation of nitrogen-fixing root nodules relies on an intriguing signal exchange between the legume host and the bacterial microsymbiont (1). In this two-way exchange, Nod factors synthesized by rhizobia function as central signal molecules, which induce early physiological responses, gene expression, and cell division in susceptible legumes (1-3). In root cells of the legume hosts, perception is mediated by Nod factor receptors (NFRs) containing ectodomains with three lysin motif (LysM) modules and cytoplasmic serine/threonine kinase domains (4-9). Mutant studies in the model legumes Lotus japonicus (Lotus) and Medicago truncatula (Medicago) as well as the crop legumes soybean (10, 11) and pea (5, 6) have shown that NFRs are required for nodulation. Mutant analysis in Lotus identified two NFRs, NFR1 and NFR5, and phenotypic analysis showed that both nfr1 and nfr5 mutants are equally impaired in nodule initiation (4, 5). In Medicago, only mutation of the Nfr5 ortholog, Nfp, results in a nonnodulating phenotype, whereas the Nfr1 homolog Lyk3 is required for progression of infection threads (7-9, 12).The earliest plant responses to Nod factor, such as membrane depolarization, cytoplasmic alkalinization, calcium fluxes, calcium spiking, and root hair deformation (3, 13), are either strongly at...

show abstract

“…We have also highlighted different mechanisms underlying infection and nodule organogenesis, and provided more data concerning the coordination of these symbiotic processes. LYK3 is another putative NF receptor that is expressed in both the epidermis and the cortex of M. truncatula roots (Haney et al, 2011;Mbengue et al, 2010), and lyk3 mutants are defective in both PIT formation and infection (Catoira et al, 2001). Hence, LYK3 is also likely to play a role in coordinating the infection process in both cell layers.…”

Section: Discussionmentioning

confidence: 99%

Epidermal and cortical roles ofNFPandDMI3in coordinating early steps of nodulation inMedicago truncatula

et al. 2012

View full text Add to dashboard Cite

SUMMARYLegumes have evolved the capacity to form a root nodule symbiosis with soil bacteria called rhizobia. The establishment of this symbiosis involves specific developmental events occurring both in the root epidermis (notably bacterial entry) and at a distance in the underlying root cortical cells (notably cell divisions leading to nodule organogenesis). The processes of bacterial entry and nodule organogenesis are tightly linked and both depend on rhizobial production of lipo-chitooligosaccharide molecules called Nod factors. However, how these events are coordinated remains poorly understood. Here, we have addressed the roles of two key symbiotic genes of Medicago truncatula, the lysin motif (LysM) domain-receptor like kinase gene NFP and the calcium-and calmodulindependent protein kinase gene DMI3, in the control of both nodule organogenesis and bacterial entry. By complementing mutant plants with corresponding genes expressed either in the epidermis or in the cortex, we have shown that epidermal DMI3, but not NFP, is sufficient for infection thread formation in root hairs. Epidermal NFP is sufficient to induce cortical cell divisions leading to nodule primordia formation, whereas DMI3 is required in both cell layers for these processes. Our results therefore suggest that a signal, produced in the epidermis under the control of NFP and DMI3, is responsible for activating DMI3 in the cortex to trigger nodule organogenesis. We integrate these data to propose a new model for epidermal/cortical crosstalk during early steps of nodulation.

show abstract

TheMedicago truncatulaE3 Ubiquitin Ligase PUB1 Interacts with the LYK3 Symbiotic Receptor and Negatively Regulates Infection and Nodulation

Cited by 156 publications

References 63 publications

Changes in PUB22 Ubiquitination Modes Triggered by MITOGEN-ACTIVATED PROTEIN KINASE3 Dampen the Immune Response

Changes in PUB22 Ubiquitination Modes Triggered by MITOGEN-ACTIVATED PROTEIN KINASE3 Dampen the Immune Response

Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding

Epidermal and cortical roles ofNFPandDMI3in coordinating early steps of nodulation inMedicago truncatula

Contact Info

Product

Resources

About