An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize

Abstract

Most terrestrial plants, including crops, engage in beneficial interactions with arbuscular mycorrhizal fungi. Vital to the association is mutual recognition involving the release of diffusible signals into the rhizosphere. Previously, we identified the maize no perception 1 (nope1) mutant to be defective in early signaling. Here, we report cloning of ZmNOPE1 on the basis of synteny with rice. NOPE1 encodes a functional homolog of the Candida albicans N-acetylglucosamine (GlcNAc) transporter NGT1, and represents the first plasma membrane GlcNAc transporter identified from plants. In C. albicans, exposure to GlcNAc activates cell signaling and virulence. Similarly, in Rhizophagus irregularis treatment with rice wild type but not nope1 root exudates induced transcriptome changes associated with signaling function, suggesting a requirement of NOPE1 function for presymbiotic fungal reprogramming.

Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis

“…The recent discovery that an N-acetylglucosamine (GlcNAc) transporter of rice and maize, called NOPE1, is required for early signalling in the AM symbiosis, points to the existence of additional and GlcNAc-based diffusible plant molecules, which may trigger presymbiotic fungal reprogramming (Nadal et al, 2017;Fig. 2).…”

“…2). nope1 mutants display very low levels of root colonization and root exudates from the mutant differ from wild-type (WT) exudates in their ability to induce transcriptome changes associated with the GO-term 'signalling' in the AMF Rhizophagus irregularis (Nadal et al, 2017). Although the exact molecular function of NOPE1 and its substrate are so far unknown, the strong mycorrhizal phenotype of the nope1 mutant indicates a crucial role in plant-fungal communication.…”

“…It is yet unclear whether the karrikin-like (KARL) ligand of D14L/KAI2, relevant for AM symbiosis is of plant or fungal origin. The recent finding that a plasmamembrane-resident plant Nacetylglucosamine (GlcNAc) transporter (NOPE1) is required for early signalling in AM suggests the existence of GlcNAc-based diffusible plant molecules, which may trigger presymbiotic fungal reprogramming (Nadal et al, 2017). Also AMF use GlcNAc-based molecules, which include lipochito-oligosaccharides (LCOs; Maillet et al, 2011) and short chitin tetraand pentamers (COs; Genre et al, 2013); these are perceived by plant LysM-RLKs (Zipfel & Oldroyd, 2017) and activate plant symbiotic responses.…”

The impact of domestication and crop improvement on arbuscular mycorrhizal symbiosis in cereals: insights from genetics and genomics

“…The establishment and maintenance of AM symbiosis requires an exchange of multiple chemical signals between fungus and plant. The current catalogue of signalling molecules includes the butenolides strigolactone (Akiyama et al, 2005;Besserer et al, 2006) and karrikin, N-acetylglucosamine (GlcNAc)-based chitinaceous molecules (Maillet et al, 2011;Genre et al, 2013;Nadal et al, 2017), and the phytohormones auxin and gibberellin (Floss et al, 2013;Etemadi et al, 2014;Yu et al, 2014;Takeda et al, 2015). Mutation in either the synthesis or perception of any one of these signals is sufficient to disrupt AM symbiosis.…”

The future has roots in the past: the ideas and scientists that shaped mycorrhizal research

“…Despite the striking effects of strigolactones, it is hard to believe that plants seeking arbuscular mycorrhizal symbiosis rely exclusively on released strigolactones to capture the fungi that are present in the soil. The discovery of a plant transporter of N ‐acetylglucosamine in maize ( Zea mays ) and rice ( Oryza sativa ) that is also required during the precontact phase (Nadal et al ., ) suggests that other signalling molecules could be important during the precontact phase. Lastly and surprisingly, ectomycorrhizal plants have been poorly investigated in this context.…”