Soybean Nodulation: Unveiling the Symbiotic Signaling Pathway

Soybean (Glycine max) is a major source of oil and proteins for human consumption. This leguminous crop forms symbiotic root nodules and undergoes nitrogen fixation by interacting with rhizobia in the soil (Oldroyd et al., 2011; Oldroyd, 2013). The symbiotic signaling pathway for sensing rhizobia is well established in model legumes, including Lotus japonicus and Medicago truncatula. In L. japonicus, Nod factors secreted by rhizobia are recognized by the LysM receptor-like kinases Nod factor receptor 1 (NFR1, also known as LYK3 in M. truncatula) and Nod factor receptor 5 (NFR5, also known as NFP in M. truncatula), which activate the downstream signaling cascade (Madsen et al., 2003; Radutoiu et al., 2003). Calcium spikes in the nucleus, a hallmark of symbiotic responses, are decoded by Ca2+/calmodulin-dependent protein kinase (CCaMK, also known as DMI3 in M. truncatula) (Levy et al., 2004; Mitra et al., 2004; Gleason et al., 2006; Tirichine et al., 2006). CCaMK interacts with and phosphorylates CYCLOPS (also known as IPD3 in M. truncatula) (Messinese et al., 2007; Yano et al., 2008; Singh et al., 2014). In addition, the GRAS domain transcription factor NSP1 and the transcriptional regulator NSP2 are essential components that activate downstream signaling after the calcium spikes in M. truncatula (Kalo et al., 2005; Smit et al., 2005). NSP1 directly binds to the promoter regions of early responsive genes in the symbiotic signaling pathway, including nodule inception (NIN), ethylene response factor required for nodulation 1 (ERN1), and ENOD11; NSP2 is required for this DNA binding in vivo (Hirsch et al., 2009). DELLA proteins, another class of GRAS transcriptional regulators, also participate in the symbiotic signaling pathway in M. truncatula by forming protein complexes with IPD3 and NSP2 (Fonouni-Farde et al., 2016; Jin et al., 2016).