The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling

Abstract

These authors contributed equally to this work. SUMMARYThe establishment of symbiotic interactions between mycorrhizal fungi, rhizobial bacteria and their legume hosts involves a common symbiosis signalling pathway. This signalling pathway is activated by Nod factors produced by rhizobia and these are recognised by the Nod factor receptors NFR1/LYK3 and NFR5/NFP. Mycorrhizal fungi produce lipochitooligosaccharides (LCOs) similar to Nod factors, as well as short-chain chitin oligomers (CO4/5), implying commonalities in signalling during mycorrhizal and rhizobial associations. Here we show that NFR1/LYK3, but not NFR5/NFP, is required for the establishment of the mycorrhizal interaction in legumes. NFR1/LYK3 is necessary for the recognition of mycorrhizal fungi and the activation of the symbiosis signalling pathway leading to induction of calcium oscillations and gene expression. Chitin oligosaccharides also act as microbe associated molecular patterns that promote plant immunity via similar LysM receptor-like kinases. CERK1 in rice has the highest homology to NFR1 and we show that this gene is also necessary for the establishment of the mycorrhizal interaction as well as for resistance to the rice blast fungus. Our results demonstrate that NFR1/LYK3/OsCERK1 represents a common receptor for chitooligosaccharide-based signals produced by mycorrhizal fungi, rhizobial bacteria (in legumes) and fungal pathogens. It would appear that mycorrhizal recognition has been conserved in multiple receptors across plant species, but additional diversification in certain plant species has defined other signals that this class of receptors can perceive.

Trade-Offs in Arbuscular Mycorrhizal Symbiosis: Disease Resistance, Growth Responses and Perspectives for Crop Breeding

“…The similarity of intracellular structures formed during interaction with AMF and pathogens, plus similarity of host genetic responses led to the prediction that plants may use overlapping signal-transduction pathways to respond to AMF, rhizobia and pathogens. Transcriptomic studies [34] and identification of CERK1 [119,145] and RAM2 [35] have supported this. However, further research is needed to identify shared components because these could be targets for exploitation by pathogens, for example research into the role of MLO during AM symbiosis.…”

“…Chitin oligosaccharides act as PAMPs that promote plant immunity via Lysine Motif Receptor-like Kinases (LysM-RLK). Some LysM-RLKs, such as Chitin Elicitor Receptor Kinase 1 (CERK1) have a dual role in pathogenic and symbiotic interactions [119] (Figure 2). CERK1 plays a central role in PTI against fungal pathogens and has been shown to be required for the recognition of chitin in both Arabidopsis thaliana (L.) Heynh and rice [120,121].…”

PUB1 Interacts with the Receptor Kinase DMI2 and Negatively Regulates Rhizobial and Arbuscular Mycorrhizal Symbioses through Its Ubiquitination Activity in Medicago truncatula

“…DMI2/SYMRK is required both for the nitrogen-fixing root nodule symbiosis with rhizobia to initiate nodule organogenesis and infection in legumes (Stracke et al, 2002;Endre et al, 2002), and for AM fungal colonization (Catoira et al, 2000;Endre et al, 2002;Stracke et al, 2002). LYK3 is essential for nodulation (Catoira et al, 2000;Limpens et al, 2003;Smit et al, 2007) and plays a weak role in the AM symbiosis (Zhang et al, 2015a). DMI2, LYK3, and PUB1 show overlapping expression patterns during nodulation (Bersoult et al, 2005;Mbengue et al, 2010;Supplemental Fig.…”

Lipo-chitooligosaccharidic nodulation factors and their perception by plant receptors

“…However, the Nod factor receptor NFP itself shows traces of this evolutionary history since it is still involved in Myc-LCO signaling [5,6]. A comparable origin was recently retraced for LYK3 and NFR1, involving two rounds of gene duplications in legumes prior to the evolution of the rhizobial symbiosis leading to three paralogous gene copies, from which one copy evolved to encode host-specific Nod factor receptors, which, again, still possess remnants of mycorrhizal functions [73,74]. Apparently, AtCERK1, the nonlegume LYK3/NFR1 homolog, shares the same symbiotic origin, since it clusters within a clade containing the other LysMRLKs, except for A. thaliana, and has retained two motifs in the kinase domain that were shown to be required for symbiotic signaling [73,75].…”