Atypical Receptor Kinase RINRK1 Required for Rhizobial Infection But Not Nodule Development in Lotus japonicus.

Xiaolin Li,Zhiqiong Zheng,Dugald Reid,Ji Xu,Giles E D Oldroyd,Xiangxiao Kong,Jongho Sun,Stig U Andersen,Haojie Jin,J Allan Downie,Jens Stougaard,Fang Xie,Liping Qiu

doi:10.1104/pp.19.00509

Abstract

During the legume-rhizobium symbiotic interaction, rhizobial invasion of legumes is primarily mediated by a plant-made tubular invagination called an infection thread (IT). Here, we identify a gene in Lotus japonicus encoding a Leu-rich repeat receptor-like kinase (LRR-RLK), RINRK1 (Rhizobial Infection Receptor-like Kinase1), that is induced by Nod factors (NFs) and is involved in IT formation but not nodule organogenesis. A paralog, RINRK2, plays a relatively minor role in infection. RINRK1 is required for full induction of early infection genes, including Nodule Inception (NIN), encoding an essential nodulation transcription factor. RINRK1 displayed an infection-specific expression pattern, and NIN bound to the RINRK1 promoter, inducing its expression. RINRK1 was found to be an atypical kinase localized to the plasma membrane and did not require kinase activity for rhizobial infection. We propose RINRK1 is an infection-specific RLK, which may specifically coordinate output from NF signaling or perceive an unknown signal required for rhizobial infection.

Highlights

During the initiation of symbiotic nitrogen-fixation in legumes, signaling receptor complexes perceive nodulation factors (NFs) synthesized by rhizobia, which induce and coordinate rhizobial infection and nodule organogenesis (Oldroyd and Downie, 2008)
The mutation causing the infection defect was previously mapped to the short arm of linkage group I, using a mapping population generated by crossing itd4 with L. japonicus Miyakojima (MG20; Lombardo et al, 2006)
Mutation of rinrk1 and rinrk1 rinrk2 revealed what appeared to be two phases of Nod factors (NFs) induction of the Nodule Inception (NIN) gene: an initial early phase of induction that was retained in the rinrk1 and rinrk1 rinrk2 mutants, and a second phase of induction (12–24 h) that was lost in these mutants

Summary

Introduction

During the initiation of symbiotic nitrogen-fixation in legumes, signaling receptor complexes perceive nodulation factors (NFs) synthesized by rhizobia, which induce and coordinate rhizobial infection and nodule organogenesis (Oldroyd and Downie, 2008). In Lotus japonicus, NFs made by Mesorhizobium loti are perceived by a receptor complex containing NFR1 and NFR5 (Nod factor receptors 1 and 5; Madsen et al, 2003; Radutoiu et al, 2003). Knockout mutations in either NFR1 or NFR5 eliminate almost all NF-inducible responses, including induction of root hair deformation, perinuclear calcium oscillations (calcium spiking), calcium influx, and induction of genes required for the development and infection of nodules (Madsen et al, 2003; Radutoiu et al, 2003; Miwa et al, 2006; Høgslund et al, 2009 ), fitting with their function as signaling receptors. Several proteins required for infection thread formation have been identified including a nodulation-specific pectate lyase (NPL; Xie et al, 2012); several components of the WAVE/SCAR-APR2/3 complex (NAP, PIR, SCARN, and ARPC1; Yokota et al, 2009; Miyahara et al, 2010; Hossain et al, 2012; Qiu et al, 2015) required for actin nucleation; a putative ubiquitin- E3 ligase LIN/CERBERUS; a coil-coil domain protein RPG; and Vapyrin, which contains a VAMP-associated protein (VAP)/ major sperm protein (MSP) domain and several ankyrin-repeat domains (Arrighi et al, 2008; Kiss et al, 2009; Yano et al, 2009; Murray et al, 2011)

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