Abstract
Legume plants form symbiotic associations with either nitrogen-fixing bacteria or arbuscular mycorrhizal (AM) fungi, which are regulated by a set of common symbiotic signaling pathway genes. Central to the signaling pathway is the activation of the DMI3/IPD3 protein complex by Ca2+ oscillations, and the initiation of nodule organogenesis and mycorrhizal symbiosis. DMI3 is essential for rhizobial infection and nodule organogenesis; however, ipd3 mutants have been shown to be impaired only in infection thread formation but not in root nodule organogenesis in Medicago truncatula. We identified an IPD3-like (IPD3L) gene in the M. truncatula genome. A single ipd3l mutant exhibits a normal root nodule phenotype. The ipd3l/ipd3-2 double mutant is completely unable to initiate infection threads and nodule primordia. IPD3L can functionally replace IPD3 when expressed under the control of the IPD3 promoter, indicating functional redundancy between these two transcriptional regulators. We constructed a version of IPD3 that was phosphomimetic with respect to two conserved serine residues (IPD3-2D). This was sufficient to trigger root nodule organogenesis, but the increased multisite phosphorylation of IPD3 (IPD3-8D) led to low transcriptional activity, suggesting that the phosphorylation levels of IPD3 fine-tune its transcriptional activity in the root nodule symbiosis. Intriguingly, the phosphomimetic version of IPD3 triggers spontaneous root-like nodules on the roots of dmi3-1 and dmi2-1 (DMI2 is an LRR-containing receptor-like kinase gene which is required for Ca2+ spiking), but not on the roots of wild-type or ipd3l ipd3-2 plants. In addition, fully developed arbuscules were formed in the ipd3l ipd3-2 mutants but not the ccamk/dmi3-1 mutants. Collectively, our data indicate that, in addition to IPD3 and IPD3L, another new genetic component or other new phosphorylation sites of IPD3 function downstream of DMI3 in rhizobial and mycorrhizal symbioses.
Highlights
The symbiosis between the majority of land plants and arbuscular mycorrhizal (AM) fungi results in highly branched intracellular symbiotic structures called arbuscules, which can deliver soil phosphate to the host plant (Parniske, 2008; Oldroyd, 2013; Wang et al, 2017)
We searched for a homologous protein sequence in the phytozome database using the IPD3 full-length protein sequence, and a protein composed of 626 AA was found, which we named IPD3like (IPD3L)
A phylogenetic tree showed that IPD3L is more closely related to IPD3 than to an IPD3 homolog in the non-mycorrhizal plant Arabidopsis, suggesting that IPD3L might function in root nodule and mycorrhizal symbioses (Figure S1)
Summary
The symbiosis between the majority of land plants and arbuscular mycorrhizal (AM) fungi results in highly branched intracellular symbiotic structures called arbuscules, which can deliver soil phosphate to the host plant (Parniske, 2008; Oldroyd, 2013; Wang et al, 2017). Legume plants form symbiosis with soil rhizobia and develop a new root-derived organ called nodule in which differentiated bacteria convert atmospheric nitrogen into a form that can be assimilated by the host plant (Oldroyd, 2013) The establishment of both root nodule and mycorrhizal symbioses is initiated through recognizing lipochitooligosaccharides, namely nodulation (Nod) factors or mycorrhizal (Myc) factors by the LysM receptor kinase proteins, and is regulated by a set of common symbiotic signaling pathway genes (Limpens et al, 2003; Madsen et al, 2003; Radutoiu et al, 2003; Arrighi et al, 2006; Zhang et al, 2007, 2015). CCaMK/DMI3 acts as a central regulator in the root nodule and mycorrhizal symbioses; the mechanism underlying differentially activating root nodule symbiosis and arbuscular mycorrhizal symbiosis-related signal pathways by CCaMK/DMI3 is largely unknown
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