Plant-activated bacterial receptor adenylate cyclases modulate epidermal infection in the Sinorhizobium meliloti–Medicago symbiosis

• Published in: Proceedings of the National Academy of Sciences - PNAS 2012-04, Vol.109 (17), p.6751-6756
• Main Authors: Tian, Chang Fu, Garnerone, Anne-Marie, Mathieu-Demazière, Céline, Masson-Boivin, Catherine, Batut, Jacques
• Format: Article
• Language: English
• Subjects: Adenylate cyclase; Adenylyl Cyclases; Adenylyl Cyclases - metabolism; Bacteria; Biological Sciences; Cyclic AMP; Cyclic AMP - metabolism; disease control; Ensifer meliloti; Flowers & plants; genes; Genotype & phenotype; Gram-negative bacteria; Infection; Infections; Legumes; Life Sciences; Medicago; Medicago - parasitology; metabolism; Nodulation; Nodules; Organogenesis; parasitology; pathogenicity; plant development; Plant roots; Plants; Plants - metabolism; Plasmids; Proteins; Root hairs; Signal Transduction; Sinorhizobium meliloti; Sinorhizobium meliloti - pathogenicity; soil bacteria; Soil microorganisms; Symbionts; Symbiosis; Vegetal Biology
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1120260109

Legumes and soil bacteria called rhizobia have coevolved a facultative nitrogen-fixing symbiosis. Establishment of the symbiosis requires bacterial entry via root hair infection threads and, in parallel, organogenesis of nodules that subsequently are invaded by bacteria. Tight control of nodulation and infection is required to maintain the mutualistic character of the interaction. Available evidence supports a passive bacterial role in nodulation and infection after the microsymbiont has triggered the symbiotic plant developmental program. Here we identify in Sinorhizobium meliloti, the Medicago symbiont, a cAMP-signaling regulatory cascade consisting of three receptor-like adenylate cyclases, a Crp-like regulator, and a target gene of unknown function. The cascade is activated specifically by a plant signal during nodule organogenesis. Cascade inactivation results in a hyperinfection phenotype consisting of abortive epidermal infection events uncoupled from nodulation. These findings show that, in response to a plant signal, rhizobia play an active role in the control of infection. We suggest that rhizobia may modulate the plant’s susceptibility to infection. This regulatory loop likely aims at optimizing legume infection.