LysM domains mediate lipochitin–oligosaccharide recognition and Nfr genes extend the symbiotic host range

Radutoiu, Simona; Madsen, Lene Heegaard; Madsen, Esben Bjørn; Jurkiewicz, Anna; Fukai, Eigo; Quistgaard, E.M.; Albrektsen, Anita S.; James, Euan K.; Thirup, Søren; Stougaard, Jens

doi:10.1038/sj.emboj.7601826

Cited by 339 publications

(284 citation statements)

References 58 publications

Supporting

Mentioning

263

Contrasting

Unclassified

Order By: Relevance

“…The perception of bacterial signaling molecules, the nodulation factors (NFs), by specific LysM-type receptor-like kinases (RLKs) in the epidermis of the host plant elicits various responses to allow root hair invasion and cell division Radutoiu et al, 2003Radutoiu et al, , 2007Jones et al, 2007;Oldroyd and Downie, 2008). While the inner cortical cells divide, outer cortical cells arrest in the G2 phase of the cell cycle, resulting in cytoplasmic bridges, the preinfection threads, through which the infection threads grow (Yang et al, 1994;van Spronsen et al, 2001).…”

mentioning

confidence: 99%

CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically

Mortier

Herder²,

Whitford³

et al. 2010

Plant Physiology

303

409

View full text Add to dashboard Cite

The CLAVATA3/embryo-surrounding region (CLE) peptides control the fine balance between proliferation and differentiation in plant development. We studied the role of CLE peptides during indeterminate nodule development and identified 25 MtCLE peptide genes in the Medicago truncatula genome, of which two genes, MtCLE12 and MtCLE13, had nodulation-related expression patterns that were linked to proliferation and differentiation. MtCLE13 expression was up-regulated early in nodule development. A high-to-low expression gradient radiated from the inner toward the outer cortical cell layers in a region defining the incipient nodule. At later stages, MtCLE12 and MtCLE13 were expressed in differentiating nodules and in the apical part of mature, elongated nodules. Functional analysis revealed a putative role for MtCLE12 and MtCLE13 in autoregulation of nodulation, a mechanism that controls the number of nodules and involves systemic signals mediated by a leucine-rich repeat receptor-like kinase, SUNN, which is active in the shoot. When MtCLE12 and MtCLE13 were ectopically expressed in transgenic roots, nodulation was abolished at the level of the nodulation factor signal transduction, and this inhibition involved long-distance signaling. In addition, composite plants with roots ectopically expressing MtCLE12 or MtCLE13 had elongated petioles. This systemic effect was not observed in transgenic roots ectopically expressing MtCLE12 and MtCLE13 in a sunn-1 mutant background, although nodulation was still strongly reduced. These results suggest multiple roles for CLE signaling in nodulation.

show abstract

mentioning

confidence: 99%

CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically

Mortier

Herder²,

Whitford³

et al. 2010

Plant Physiology

303

409

View full text Add to dashboard Cite

show abstract

“…NFs are perceived by two receptor kinases, nodulation factor receptor1 (NFR1) and NFR5, which belong to the Lysin-motif receptor-like kinases (RLKs; Madsen et al, 2003;Radutoiu et al, 2003Radutoiu et al, , 2007. Recognition of NFs by their receptors leads to activation of the common symbiosis pathway, which is required for establishing symbiotic relationships with rhizobia and nutritionimproving mycorrhizal fungi (Kistner and Parniske, 2002;Banba et al, 2008).…”

mentioning

confidence: 99%

A Ubiquitin Ligase of Symbiosis Receptor Kinase Involved in Nodule Organogenesis

et al. 2012

View full text Add to dashboard Cite

The symbiosis receptor kinase (SymRK) is required for morphological changes of legume root hairs triggered by rhizobial infection. How protein turnover of SymRK is regulated and how the nodulation factor signals are transduced downstream of SymRK are not known. In this report, a SymRK-interacting E3 ubiquitin ligase (SIE3) was shown to bind and ubiquitinate SymRK. The SIE3-SymRK interaction and the ubiquitination of SymRK were shown to occur in vitro and in planta. SIE3 represents a new class of plant-specific E3 ligases that contain a unique pattern of the conserved CTLH (for C-terminal to LisH), CRA (for CT11-RanBPM), and RING (for Really Interesting New Gene) domains. Expression of SIE3 was detected in all tested tissues of Lotus japonicus plants, and its transcript level in roots was enhanced by rhizobial infection. The SIE3 protein was localized to multiple subcellular locations including the nuclei and plasma membrane, where the SIE3-SymRK interaction took place. Overexpression of SIE3 promoted nodulation in transgenic hairy roots, whereas downregulation of SIE3 transcripts by RNA interference inhibited infection thread development and nodule organogenesis. These results suggest that SIE3 represents a new class of E3 ubiquitin ligase, acts as a regulator of SymRK, and is involved in rhizobial infection and nodulation in L. japonicus.

show abstract

“…NFR1 and NFR5 are Nod factor receptors based on the observations that (1) they encode receptor-like kinases with LysM domains known to function in polysaccharide binding Radutoiu et al, 2003;Arrighi et al, 2006); (2) nfr1 and nfr5 mutants show no Nod factor responses Miwa et al, 2006a); (3) NFR1 and NFR5 bind Nod factors with high affinity (Broghammer et al, 2012); (4) the specificity of Nod factor recognition has been shown to be a function of the LysM domains of NFR5 (Bek et al, 2010); and (5) transfer of NFR1 and NFR5 to M. truncatula transferred the specificity of the L. japonicus rhizobial interaction (Radutoiu et al, 2007). The data on root hair deformation were analyzed using Student's t test, and the effects of Nod factor (compared with the no-Nod factor control) were found to be significant for both the wild type (P , 0.003) and the 59D LNP antisense line (P , 0.001).…”

Section: Discussionmentioning

confidence: 99%

“…In parallel, genetic studies implicate the LysM receptor-like kinases in specific Nod factor recognition (Radutoiu et al, 2007), and high-affinity Nod factor binding to purified NFR1 and NFR5 has been demonstrated recently (Broghammer et al, 2012). In order to better understand the function that Nod factor binding to LNP plays in the establishment of symbiotic interactions, we generated transgenic lines of Lotus japonicus that have markedly reduced LNP levels.…”

mentioning

confidence: 99%

“…This suggests a highly specific Nod factor recognition mechanism, which can discriminate between different Nod factor structures. The LysM receptor-like kinases NFR1/LYK3 and NFR5/ NFP have emerged as strong candidates to function as Nod factor receptors based on the findings that purified NFR1 and NFR5 bind Nod factors with high affinity (Broghammer et al, 2012) and that the specificity of Nod factor recognition resides within the LysM domains (Radutoiu et al, 2007;Bek et al, 2010).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Rhizobial and Mycorrhizal Symbioses in Lotus japonicus Require Lectin Nucleotide Phosphohydrolase, Which Acts Upstream of Calcium Signaling

Morieri

Kalsi

et al. 2012

Plant Physiology

View full text Add to dashboard Cite

(J.S., P.M.G.)Nodulation in legumes requires the recognition of rhizobially made Nod factors. Genetic studies have revealed that the perception of Nod factors involves LysM domain receptor-like kinases, while biochemical approaches have identified LECTIN NUCLEOTIDE PHOSPHOHYDROLASE (LNP) as a Nod factor-binding protein. Here, we show that antisense inhibition of LNP blocks nodulation in Lotus japonicus. This absence of nodulation was due to a defect in Nod factor signaling based on the observations that the early nodulation gene NODULE INCEPTION was not induced and that both Nod factor-induced perinuclear calcium spiking and calcium influx at the root hair tip were blocked. However, Nod factor did induce root hair deformation in the LNP antisense lines. LNP is also required for infection by the mycorrhizal fungus Glomus intraradices, suggesting that LNP plays a role in the common signaling pathway shared by the rhizobial and mycorrhizal symbioses. Taken together, these observations indicate that LNP acts at a novel position in the early stages of symbiosis signaling. We propose that LNP functions at the earliest stage of the common nodulation and mycorrhization symbiosis signaling pathway downstream of the Nod factor receptors; it may act either by influencing signaling via changes in external nucleotides or in conjunction with the LysM receptor-like kinases for recognition of Nod factor.

show abstract

LysM domains mediate lipochitin–oligosaccharide recognition and Nfr genes extend the symbiotic host range

Cited by 339 publications

References 58 publications

CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically

CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically

A Ubiquitin Ligase of Symbiosis Receptor Kinase Involved in Nodule Organogenesis

Rhizobial and Mycorrhizal Symbioses in Lotus japonicus Require Lectin Nucleotide Phosphohydrolase, Which Acts Upstream of Calcium Signaling

Contact Info

Product

Resources

About