A Positive Regulator of Nodule Organogenesis, NODULE INCEPTION, Acts as a Negative Regulator of Rhizobial Infection in Lotus japonicus    

Abstract

Legume-rhizobium symbiosis occurs in specialized root organs called nodules. To establish the symbiosis, two major genetically controlled events, rhizobial infection and organogenesis, must occur. For a successful symbiosis, it is essential that the two phenomena proceed simultaneously in different root tissues. Although several symbiotic genes have been identified during genetic screenings of nonsymbiotic mutants, most of the mutants harbor defects in both infection and organogenesis pathways, leading to experimental difficulty in investigating the molecular genetic relationships between the pathways. In this study, we isolated a novel nonnodulation mutant, daphne, in Lotus japonicus that shows complete loss of nodulation but a dramatically increased numbers of infection threads. Characterization of the locus responsible for these phenotypes revealed a chromosomal translocation upstream of NODULE INCEPTION (NIN) in daphne. Genetic analysis using a known nin mutant revealed that daphne is a novel nin mutant allele. Although the daphne mutant showed reduced induction of NIN after rhizobial infection, the spatial expression pattern of NIN in epidermal cells was broader than that in the wild type. Overexpression of NIN strongly suppressed hyperinfection in daphne, and daphne phenotypes were partially rescued by cortical expression of NIN. These observations suggested that the daphne mutation enhanced the role of NIN in the infection pathway due to a specific loss of the role of NIN in nodule organogenesis. Based on these results, we provide evidence that the bifunctional transcription factor NIN negatively regulates infection but positively regulates nodule organogenesis during the course of the symbiosis.

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

“…This interval enables AON to suppress nodulation stimulated by subsequent infection through repression of this gene essential to nodule organogenesis. In addition, NIN expression in the cortex also locally inhibits rhizobial infection, whereas this gene is essential for infection thread development and for cortical cell division to generate nodule primordia (24). This report and our data show that NIN has multiple functions in nodulation.…”

“…These findings indicate that NIN-GR activates AON to systemically inhibit nodulation. The number of nodules in GFPpositive Pro35S-NIN-GR roots tended to be reduced in these mutants, likely related to local inhibitory effects of NIN expression on rhizobial infection (24). Alternatively, morphological alteration of roots caused by NIN overexpression might affect infection frequency.…”

A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis

“…This would be similar to NIN, which is required for symbiotic gene induction in the epidermis and cortex, as well as Rhizobium spp. infection and nodule initiation, while restricting ENOD11 expression on the one hand and nodulation on the other hand, via CLE peptides Soyano et al, 2013Soyano et al, , 2014Laloum et al, 2014;Yoro et al, 2014;Fournier et al, 2015;Vernié et al, 2015). Consequently, the impact of the pEPI:AtCKX3 construct might depend on the relative efficiency of different processes (e.g.…”

The Symbiosis-Related ERN Transcription Factors Act in Concert to Coordinate Rhizobial Host Root Infection

“…A few of them have been shown to be directly involved in early NF signaling and these include the GRAS-type NSP1/ NSP2 (Smit et al, 2005;Kaló et al, 2005;Heckmann et al, 2006;Murakami et al, 2006), the CCAAT-box binding NF-YA1/A2 (Laloum et al, 2014), Nodule Inception (NIN; Marsh et al, 2007;Yoro et al, 2014;Vernié et al, 2015), and the ERF Required for Nodulation1 (ERN1; Andriankaja et al, 2007;Middleton et al, 2007;Cerri et al, 2012). Gene expression and functional studies indicate that these TFs are involved in both NF signaling and rhizobial infection and can participate in overlapping transcription networks.…”