Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway

Abstract

SummaryLegumes form two different types of intracellular root symbioses, with fungi and bacteria, resulting in arbuscular mycorrhiza and nitrogen-fixing nodules, respectively. Rhizobial signalling molecules, called Nod factors, play a key role in establishing the rhizobium-legume association and genes have been identified in Medicago truncatula that control a Nod factor signalling pathway leading to nodulation. Three of these genes, the so-called DMI1, DMI2 and DMI3 genes, are also required for formation of mycorrhiza, indicating that the symbiotic pathways activated by both the bacterial and the fungal symbionts share common steps. To analyse possible cross-talk between these pathways we have studied the effect of treatment with Nod factors on mycorrhization in M. truncatula. We show that Nod factors increase mycorrhizal colonization and stimulate lateral root formation. The stimulation of lateral root formation by Nod factors requires both the same structural features of Nod factors and the same plant genes (NFP, DMI1, DMI2, DMI3 and NSP1) that are required for other Nod factor-induced symbiotic responses such as early nodulin gene induction and cortical cell division. A diffusible factor from arbuscular mycorrhizal fungi was also found to stimulate lateral root formation, while three root pathogens did not have the same effect. Lateral root formation induced by fungal signal(s) was found to require the DMI1 and DMI2 genes, but not DMI3. The idea that this diffusible fungal factor might correspond to a previously hypothesized mycorrhizal signal, the 'Myc factor', is discussed.

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

“…Consistent with this proposal, it has been shown that Nod factor and Myc factors can both induce LR development (Oláh et al, 2005;Maillet et al, 2011). Within the G1, G2, and G3 clusters, we identified 22 genes homologous to known Arabidopsis regulators of root and LR development (Table I).…”

“…Nod factors stimulate the formation of LRs (Oláh et al, 2005); thus, the increased expression of LR developmental genes could simply reflect additional LR initiation. Alternatively, the genes regulating LR primordium initiation may perform analogous functions required for the initiation of nodule development.…”

NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes

“…Consistent with this hypothesis, it has been shown that both Nod and Myc symbiotic factors, in addition to their role in host recognition and nodule organ formation, stimulate lateral root development (Oláh et al, 2005;Maillet et al, 2011). This effect on lateral root development may represent their ancestral function, suggesting that nodule organogenesis programs have evolved by co-option of lateral root developmental programs triggered by Nod factor-like signaling molecules.…”

The exudate from an arbuscular mycorrhizal fungus induces nitric oxide accumulation in Medicago truncatula roots

“…While the production of NO is evident, its role in the early response of the host plants to AM fungal signals remains unclear. One possibility is that NO is active in the signaling pathway that stimulates lateral root formation (Oláh et al 2005;Mukherjee and Ané 2011); both responses are in fact DMI1-/DMI2-dependent and DMI3-independent. This intriguing possibility, which requires further investigation, is also supported by the well-known presence of NO in root meristems and at sites of lateral root emergence (Correa-Aragunde et al 2004.…”

“…Recently, the upregulation of a membrane steroid-binding protein was also shown to be induced in epidermal/subepidermal cells in the vicinity of AM fungal hyphae (Kuhn et al 2010). Diffusible AM fungal signals were also shown to activate early events, such as changes in cytosolic (Navazio et al 2007;Kosuta et al 2008) and nuclear Ca2+ concentration (Chabaud et al 2011), and delayed processes, such as root branching (Oláh et al 2005) and starch accumulation in the root cortex (Gutjahr et al 2009). Recently, fungal exudates from Glomus intraradices were shown to contain a mixture of sulfated and nonsulfated lipochitooligosaccharides (LCO), which are responsible for the activation of MtENOD11 gene expression and the induction of lateral roots formation (Maillet et al 2011).…”