Activation of Symbiosis Signaling by Arbuscular Mycorrhizal Fungi in Legumes and Rice

Abstract

Establishment of arbuscular mycorrhizal interactions involves plant recognition of diffusible signals from the fungus, including lipochitooligosaccharides (LCOs) and chitooligosaccharides (COs). Nitrogen-fixing rhizobial bacteria that associate with leguminous plants also signal to their hosts via LCOs, the so-called Nod factors. Here, we have assessed the induction of symbiotic signaling by the arbuscular mycorrhizal (Myc) fungal-produced LCOs and COs in legumes and rice (Oryza sativa). We show that Myc-LCOs and tetra-acetyl chitotetraose (CO4) activate the common symbiosis signaling pathway, with resultant calcium oscillations in root epidermal cells of Medicago truncatula and Lotus japonicus. The nature of the calcium oscillations is similar for LCOs produced by rhizobial bacteria and by mycorrhizal fungi; however, Myc-LCOs activate distinct gene expression. Calcium oscillations were activated in rice atrichoblasts by CO4, but not the Myc-LCOs, whereas a mix of CO4 and Myc-LCOs activated calcium oscillations in rice trichoblasts. In contrast, stimulation of lateral root emergence occurred following treatment with Myc-LCOs, but not CO4, in M. truncatula, whereas both Myc-LCOs and CO4 were active in rice. Our work indicates that legumes and non-legumes differ in their perception of Myc-LCO and CO signals, suggesting that different plant species respond to different components in the mix of signals produced by arbuscular mycorrhizal fungi.

MtLAX2, a Functional Homologue of the Arabidopsis Auxin Influx Transporter AUX1, Is Required for Nodule Organogenesis

“…Analysis of calcium spiking was done in the presence of the chemicals and 1 3 10 29 M Nod factor as described previously (Sun et al, 2015).…”

Modulation of Host Cell Biology by Plant Pathogenic Microbes

“…Exogenous application of LCO promotes lateral root formation in M. truncatula, and CO4 as well as LCO display similar activity in rice (Maillet et al 2011, Sun et al 2015. Overexpression of LjSymRK, the most upstream common signaling element in the calcium spiking triggered by LCO and CO4, is sufficient to trigger nodule formation.…”

“…Designation of LCOs and CO4 as symbiotic signatures was inspired by observed changes in cellular and developmental plant processes. These include root hair curling, lateral root formation, and nuclear calcium spiking, which are dependent on genetic elements required for symbiosis (Gough & Cullimore 2011, Maillet et al 2011, Sun et al 2015. Furthermore, CO4 released by symbiotic fungi trigger a spike in nuclear calcium following a similar signaling route as LCOs and are therefore considered symbiotic signals (Genre et al 2013).…”

Lipo-chitooligosaccharidic nodulation factors and their perception by plant receptors

“…COs with a degree of polymerization higher than six are potent elicitors of plant defense whereas shorter COs, produced in addition to Myc-LCOs by endomycorrhizal fungi, are additional components of symbiotic signaling mechanisms in legumes and non-legumes [8,57]. Since LCOs and COs are perceived by structurally-related LysM receptors, one of the main challenges for plant biologists is to identify the molecular mechanisms underlying ligand recognition and receptor activation for these signals.…”

“…However, root treatment with exogenous Myc-LCOs stimulates mycorrhization in legumes and nonlegumes indicating that Myc-LCOs are biologically active on a variety of plants. Moreover, Myc-LCOs, just like Nod factors, stimulate root development and induce calcium spiking and transcriptional changes in Medicago truncatula [5][6][7][8].…”