Nod Factor Receptors Form Heteromeric Complexes and Are Essential for Intracellular Infection in<i>Medicago</i>Nodules

Moling, Sjef; Pietraszewska-Bogiel, Anna; Postma, Marten; Fedorova, Elena; Hink, Mark A.; Limpens, Erik; Gadella, Theodorus W. J.; Bisseling, Ton

doi:10.1105/tpc.114.129502

Cited by 89 publications

(76 citation statements)

References 43 publications

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“…The potential for MtNFP and MtLYK3 to provoke defense responses has been suggested as a reason why the accumulation and interaction of these two proteins are highly restricted in nodules [27]. The authors have suggested that the localization of MtNFP and MtLYK3 to just two cell layers is achieved through transcriptional control combined with high protein turnover [27]. In our N. benthamiana experiments, the attenuation of the MtNFPMtLYK3-induced cell death response, by co-expressing MtLYR3 (Fig.…”

Section: Discussionmentioning

confidence: 61%

“…This response depends on the presence of the intracellular domains of both proteins, and the kinase activity of MtLYK3/LjNFR1, but is independent of Nod factor [25,26]. The potential for MtNFP and MtLYK3 to provoke defense responses has been suggested as a reason why the accumulation and interaction of these two proteins are highly restricted in nodules [27]. The authors have suggested that the localization of MtNFP and MtLYK3 to just two cell layers is achieved through transcriptional control combined with high protein turnover [27].…”

Section: Discussionmentioning

confidence: 99%

“…It appears to functionally interact with MtLYK3/ LjNFR1 as coexpression of MtNFP/MtLYK3 or LjNFR5/LjNFR1 pairs in Nicotiana benthamiana leaf cells leads to activation of defense responses [25,26]. Recently MtNFP and MtLYK3 have also been shown to interact physically in M. truncatula root nodules [27].…”

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confidence: 99%

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LYR3, a high‐affinity LCO‐binding protein of Medicago truncatula, interacts with LYK3, a key symbiotic receptor

et al. 2016

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Edited by Julian Schroeder LYR3, LYK3, and NFP are lysin motif-containing receptor-like kinases (LysM-RLKs) from Medicago truncatula, involved in perception of symbiotic lipo-chitooligosaccharide (LCO) signals. Here, we show that LYR3, a highaffinity LCO-binding protein, physically interacts with LYK3, a key player regulating symbiotic interactions. In vitro, LYR3 is phosphorylated by the active kinase domain of LYK3. Fluorescence lifetime imaging/F€ orster resonance energy transfer (FLIM/FRET) experiments in tobacco protoplasts show that the interaction between LYR3 and LYK3 at the plasma membrane is disrupted or inhibited by addition of LCOs. Moreover, LYR3 attenuates the cell death response, provoked by coexpression of NFP and LYK3 in tobacco leaves.Keywords: FLIM/FRET; lipo-chitooligosaccharides; LysM-RLK; Medicago truncatula; membrane receptor complex; phosphoproteomics The extracellular domains of plant RLKs are built up of different protein domains which serve as sensors for endogenous and outer stimuli, as diverse as peptides, hormones, (peptido-) glycans, and (lipo-) chitooligosaccharides. Two prevalent extracellular protein domains consist of either leucine-rich repeats (LRRs) or lysin motifs (LysMs), which might interact with peptides or with N-acetyl-D-glucosamine (GlcNAc)-containing compounds, respectively [1,2].Recent advances in functional and structural analyses of plant RLKs, particularly in Arabidopsis, suggest that plant RLKs act in multimeric complexes [3]. For example, the LysM-RLK chitin elicitor receptor kinase 1 of A. thaliana (AtCERK1) interacts with other receptor proteins to mediate responses to different signals. This protein can bind chitooligosaccharides (COs) [4], but it also interacts with two CO-binding LysM-RLKs with dead kinase domains (AtLYK5/ AtLYK4) [5] and with two peptidoglycan-binding LysM receptor-like proteins (AtLYM1/AtLYM3) [6] to mediate defense responses to these GlcNAc-containing signals. In contrast, OsCERK1 from rice

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Section: Discussionmentioning

confidence: 61%

Section: Discussionmentioning

confidence: 99%

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LYR3, a high‐affinity LCO‐binding protein of Medicago truncatula, interacts with LYK3, a key symbiotic receptor

et al. 2016

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“…Recently, the interaction of two NF receptors, NFP and LYK3, has been reported. One study indicates that the interaction of NFP and LYK3 was detected in the heterologous N. benthamiana system and that their coexpression causes cell death (PietraszewskaBogiel et al, 2013), and another study reveals that NFP and LYK3 form heteromeric complexes at the cell periphery in nodules (Moling et al, 2014). Therefore, it is probable that the GTP-bound ROP10 forms a protein complex with NFP and LYK3.…”

Section: Discussionmentioning

confidence: 99%

The Small GTPase ROP10 of Medicago truncatula Is Required for Both Tip Growth of Root Hairs and Nod Factor-Induced Root Hair Deformation

Lei

Wang

et al. 2015

Plant Cell

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Rhizobia preferentially enter legume root hairs via infection threads, after which root hairs undergo tip swelling, branching, and curling. However, the mechanisms underlying such root hair deformation are poorly understood. Here, we showed that a type II small GTPase, ROP10, of Medicago truncatula is localized at the plasma membrane (PM) of root hair tips to regulate root hair tip growth. Overexpression of ROP10 and a constitutively active mutant (ROP10CA) generated depolarized growth of root hairs, whereas a dominant negative mutant (ROP10DN) inhibited root hair elongation. Inoculated with Sinorhizobium meliloti, the depolarized swollen and ballooning root hairs exhibited extensive root hair deformation and aberrant infection symptoms. Upon treatment with rhizobia-secreted nodulation factors (NFs), ROP10 was transiently upregulated in root hairs, and ROP10 fused to green fluorescent protein was ectopically localized at the PM of NF-induced outgrowths and curls around rhizobia. ROP10 interacted with the kinase domain of the NF receptor NFP in a GTP-dependent manner. Moreover, NF-induced expression of the early nodulin gene ENOD11 was enhanced by the overexpression of ROP10 and ROP10CA. These data suggest that NFs spatiotemporally regulate ROP10 localization and activity at the PM of root hair tips and that interactions between ROP10 and NF receptors are required for root hair deformation and continuous curling during rhizobial infection.

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“…Nod factor receptors, which include Lysine motif domain-containing receptorlike kinase3 (LYK3) and Nodulation factor perception (NFP) in Medicago truncatula and Nodulation factor receptor1 (NFR1) and NFR5 in Lotus japonicus, are plasma membrane-localized receptor-like kinase and kinase-like (RLK) proteins (Amor et al, 2003;Smit et al, 2007;Haney et al, 2011;Moling et al, 2014) consisting of an intracellular kinase domain and an extracellular region with two or three chitin-binding Lys motifs (LysM). LysM domains bind Nod factors through their chitin backbone (Petutschnig et al, 2010;Broghammer et al, 2012) and are implicated in Nod factor recognition specificity .…”

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confidence: 99%

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

et al. 2015

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The legume-rhizobium symbiosis is initiated through the activation of the Nodulation (Nod) factor-signaling cascade, leading to a rapid reprogramming of host cell developmental pathways. In this work, we combine transcriptome sequencing with molecular genetics and network analysis to quantify and categorize the transcriptional changes occurring in roots of Medicago truncatula from minutes to days after inoculation with Sinorhizobium medicae. To identify the nature of the inductive and regulatory cues, we employed mutants with absent or decreased Nod factor sensitivities (i.e. Nodulation factor perception and Lysine motif domain-containing receptor-like kinase3, respectively) and an ethylene (ET)-insensitive, Nod factor-hypersensitive mutant (sickle). This unique data set encompasses nine time points, allowing observation of the symbiotic regulation of diverse biological processes with high temporal resolution. Among the many outputs of the study is the early Nod factorinduced, ET-regulated expression of ET signaling and biosynthesis genes. Coupled with the observation of massive transcriptional derepression in the ET-insensitive background, these results suggest that Nod factor signaling activates ET production to attenuate its own signal. Promoter:b-glucuronidase fusions report ET biosynthesis both in root hairs responding to rhizobium as well as in meristematic tissue during nodule organogenesis and growth, indicating that ET signaling functions at multiple developmental stages during symbiosis. In addition, we identified thousands of novel candidate genes undergoing Nod factor-dependent, ET-regulated expression. We leveraged the power of this large data set to model Nod factor-and ET-regulated signaling networks using MERLIN, a regulatory network inference algorithm. These analyses predict key nodes regulating the biological process impacted by Nod factor perception. We have made these results available to the research community through a searchable online resource.

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Nod Factor Receptors Form Heteromeric Complexes and Are Essential for Intracellular Infection inMedicagoNodules

Cited by 89 publications

References 43 publications

LYR3, a high‐affinity LCO‐binding protein of Medicago truncatula, interacts with LYK3, a key symbiotic receptor

LYR3, a high‐affinity LCO‐binding protein of Medicago truncatula, interacts with LYK3, a key symbiotic receptor

The Small GTPase ROP10 of Medicago truncatula Is Required for Both Tip Growth of Root Hairs and Nod Factor-Induced Root Hair Deformation

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

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