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 signalling. Here, we report cloning of ZmNope1 on the basis of synteny with rice. NOPE1 encodes a functional homologue 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 signalling and virulence. Similarly, in Rhizophagus irregularis treatment with rice wild-type but not nope1 root exudates induced transcriptome changes associated with signalling function, suggesting a requirement of NOPE1 function for presymbiotic fungal reprogramming.
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References
Nadal, M. & Paszkowski, U. Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 16, 473–479 (2013).
Zipfel, C. & Oldroyd, G. E. Plant signalling in symbiosis and immunity. Nature 543, 328–336 (2017).
Gutjahr, C. & Parniske, M. Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu. Rev. Cell Dev. Biol. 29, 593–617 (2013).
Miyata, K. et al. The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol. 55, 1864–1872 (2014).
Zhang, X. et al. The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J. 81, 258–267 (2015).
Gutjahr, C. et al. Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 350, 1521–1524 (2015).
Bécard, G., Douds, D. D. & Pfeffer, P. E. Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal fungi in the presence of CO2 and flavonols. Appl. Environ. Microbiol. 58, 821–825 (1992).
Nagahashi, G. & Douds, D. D., Jr. The effects of hydroxy fatty acids on the hyphal branching of germinated spores of AM fungi. Fungal Biol. 115, 351–358 (2011).
Akiyama, K., Matsuzaki, K. & Hayashi, H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827 (2005).
Besserer, A., Becard, G., Jauneau, A., Roux, C. & Sejalon-Delmas, N. GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus gigaspora rosea by boosting its energy metabolism. Plant Physiol. 148, 402–413 (2008).
Besserer, A. et al. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4, e226 (2006).
Gomez-Roldan, V. et al. Strigolactone inhibition of shoot branching. Nature 455, 189–194 (2008).
Bécard, G., Taylor, L., Jr, D. D., Pfeffer, P. & Doner, L. Flavonoids are not necessary plant signals in arbuscular mycorrhizal symbiosis. Mol. Plant Microbe In. 8, 252–258 (1995).
Wang, E. et al. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22, 2242–2246 (2012).
Wewer, V., Brands, M. & Dormann, P. Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus Rhizophagus irregularis during mycorrhization of Lotus japonicus. Plant J. 79, 398–412 (2014).
Paszkowski, U., Jakovleva, L. & Boller, T. Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. Plant J. 47, 165–173 (2006).
Alvarez, F. J. & Konopka, J. B. Identification of an N-acetylglucosamine transporter that mediates hyphal induction in candida albicans. Mol. Biol. Cell 18, 965–975 (2007).
Naseem, S. & Konopka, J. B. N-acetylglucosamine regulates virulence properties in microbial pathogens. PLoS Pathog. 11, e1004947 (2015).
Jeong, D. H. et al. Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J. 45, 123–132 (2006).
Güimil, S. et al. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc. Natl Acad. Sci. USA 102, 8066–8070 (2005).
Gutjahr, C. et al. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20, 2989–3005 (2008).
Marcel, S., Sawers, R., Oakeley, E., Angliker, H. & Paszkowski, U. Tissue-adapted invasion strategies of the rice blast fungus Magnaporthe oryzae. Plant Cell 22, 3177–3187 (2010).
Ahern, K. R. et al. Regional mutagenesis using Dissociation in maize. Methods 49, 248–254 (2009).
Vollbrecht, E. et al. Genome-wide distribution of transposed Dissociation elements in maize. Plant Cell 22, 1667–1685 (2010).
Paszkowski, U., Kroken, S., Roux, C. & Briggs, S. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl Acad. Sci. USA 99, 13324–13329 (2002).
Nagy, R. et al. Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol. 8, 186–197 (2006).
Winter, D. et al. An ‘Electronic fluorescent pictograph’ browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2, e718 (2007).
Konopka, J. B. N-acetylglucosamine (GlcNAc) functions in cell signaling. Scientifica (Cairo) 2012 (2012).
Whiteway, M. & Oberholzer, U. Candida morphogenesis and host-pathogen interactions. Curr. Opin. Microbiol. 7, 350–357 (2004).
Simonetti, N., Strippoli, V. & Cassone, A. Yeast-mycelial conversion induced by N-acetyl-D-glucosamine in candida albicans. Nature 250, 344–346 (1974).
Naseem, S., Gunasekera, A., Araya, E. & Konopka, J. B. N-acetylglucosamine (GlcNAc) induction of hyphal morphogenesis and transcriptional responses in Candida albicans are not dependent on its metabolism. J. Biol. Chem. 286, 28671–28680 (2011).
Yamada, K. et al. Monosaccharide absorption activity of Arabidopsis roots depends on expression profiles of transporter genes under high salinity conditions. J. Biol. Chem. 286, 43577–43586 (2011).
Kobae, Y. et al. Up-regulation of genes involved in N-acetylglucosamine uptake and metabolism suggests a recycling mode of chitin in intraradical mycelium of arbuscular mycorrhizal fungi. Mycorrhiza 25, 411–417 (2015).
Gadkar, V. et al. Root exudate of pmi tomato mutant M161 reduces AM fungal proliferation in vitro. FEMS Microbiol. Lett. 223, 193–198 (2003).
Vanholme, B. et al. Accumulation of N-acetylglucosamine oligomers in the plant cell wall affects plant architecture in a dose-dependent and conditional manner. Plant Physiol. 165, 290–308 (2014).
Jiang, H. et al. A novel short-root gene encodes a glucosamine-6-phosphate acetyltransferase required for maintaining normal root cell shape in rice. Plant Physiol. 138, 232–242 (2005).
Gilmore, S. A., Naseem, S., Konopka, J. B. & Sil, A. N-acetylglucosamine (GlcNAc) triggers a rapid, temperature-responsive morphogenetic program in thermally dimorphic fungi. PLoS Genetics 9, e1003799 (2013).
Boulanger, A. et al. The plant pathogen Xanthomonas campestris pv. campestris exploits N-acetylglucosamine during infection. mBio 5, e01527–14 (2014).
Killiny, N., Prado, S. S. & Almeida, R. P. Chitin utilization by the insect-transmitted bacterium xylella fastidiosa. Appl. Environ. Microbiol. 76, 6134–6140 (2010).
Pan, M., Schwartzman, J. A., Dunn, A. K., Lu, Z. & Ruby, E. G. A single host-derived glycan impacts key regulatory nodes of symbiont metabolism in a coevolved mutualism. mBio 6, e00811 (2015).
Acknowledgements
We kindly thank J. Gheyselinck and A. Bates for their technical assistance. We are grateful to J. Arbuckle (DuPont/Pioneer) for helping with mapping the maize nope1 mutation and S. Brockington for guidance with advanced BLAST searches. Research in the U.P. laboratories was supported by the Swiss National Science Foundation grants 3100A0-104132, PP00A-110874, PP00P3-130704 and by the Gatsby Charitable Foundation grant RG60824. S.N. and J.B.K. were supported by a grant from the National Institutes of Health (R01GM116048).
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M.N., R.S., N.G., E.M., J.B.K., T.P.B. and U.P. designed the experiments. M.N., R.S., S.N., B.B., C.K., A.S., G.A., K.R.A., A.R., C.G. and C.R., performed the experiments. C.R. performed bioinformatics and statistical analyses of the RNAseq data. M.N., R.S., C.R., E.M., J.B.K. and U.P. wrote the manuscript.
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Nadal, M., Sawers, R., Naseem, S. et al. An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize. Nature Plants 3, 17073 (2017). https://doi.org/10.1038/nplants.2017.73
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DOI: https://doi.org/10.1038/nplants.2017.73
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