Arbuscular mycorrhizal fungi possess a CLAVATA3/embryo surrounding region-related gene that positively regulates symbiosis

• Published in: The New phytologist 2019-04, Vol.222 (2), p.1030-1042
• Main Authors: Le Marquer, Morgane, Bécard, Guillaume, dit Frey, Nicolas Frei
• Format: Article
• Language: English
• Subjects: Alfalfa; Amino Acid Sequence; Animal embryos; Arbuscular mycorrhizas; CLE peptides; Embryos; endomycorrhizal symbiosis; Fungal Proteins - chemistry; Fungal Proteins - genetics; Fungal Proteins - metabolism; Fungi; Gene Expression Regulation, Fungal - drug effects; Genes; Genes, Fungal; Gigaspora rosea; Glomeromycotina; Life Sciences; Medicago truncatula - drug effects; Medicago truncatula - microbiology; Mycorrhizae - drug effects; Mycorrhizae - genetics; Mycorrhizae - growth & development; Nematodes; Peptides; Peptides - pharmacology; Phylogeny; Plant Roots - drug effects; Plant Roots - growth & development; Plant Roots - microbiology; Pretreatment; Rhizophagus spp; RNA, Messenger - genetics; RNA, Messenger - metabolism; root development; Roots; Secretion; Seedlings; Symbionts; Symbiosis; Symbiosis - drug effects; Symbiosis - genetics; Transcription; Transcription, Genetic - drug effects; Vegetal Biology
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.15643

The arbuscular mycorrhizal (AM) symbiosis is a beneficial association established between land plants and the members of a subphylum of fungi, the Glomeromycotina. How the two symbiotic partners regulate their association is still enigmatic. Secreted fungal peptides are candidates for regulating this interaction. We searched for fungal peptides with similarities with known plant signalling peptides. We identified CLAVATA (CLV)/EMBRYO SURROUNDING REGION (ESR)-RELATED PROTEIN (CLE) genes in phylogenetically distant AM fungi: four Rhizophagus species and one Gigaspora species. These CLE genes encode a signal peptide for secretion and the conserved CLE C-terminal motif. They seem to be absent in the other fungal clades. Rhizophagus irregularis and Gigaspora rosea CLE genes (RiCLE1 and GrCLE1) are transcriptionally induced in symbiotic vs asymbiotic conditions. Exogenous application of synthetic RiCLE1 peptide on Medicago truncatula affects root architecture, by slowing the apical growth of primary roots and stimulating the formation of lateral roots. In addition, pretreatment of seedlings with RiCLE1 peptide stimulates mycorrhization. Our findings demonstrate for the first time that in addition to plants and nematodes,AMfungi also possess CLE genes. These results pave the way for deciphering new mechanisms by which AM fungi modulate plant cellular responses during the establishment of AM symbiosis.