Nitric oxide and phytoglobin PHYTOGB1 are regulatory elements in the Solanum lycopersicum–Rhizophagus irregularis mycorrhizal symbiosis

• Published in: The New phytologist 2019-08, Vol.223 (3), p.1560-1574
• Main Authors: Martínez-Medina, Ainhoa, Pescador, Leyre, Fernández, Iván, Rodríguez-Serrano, María, García, Juan M., Romero-Puertas, María C., Pozo, María J.
• Format: Article
• Language: English
• Subjects: Accumulation; arbuscular mycorrhiza (AM); Arbuscular mycorrhizas; Cell Wall - metabolism; Deregulation; fungal‐plant signaling; Fungi; Fusarium oxysporum; Gene Expression Regulation, Plant; Gene Silencing; Glomeromycota - physiology; Lycopersicon esculentum - genetics; Lycopersicon esculentum - metabolism; Lycopersicon esculentum - microbiology; Mycorrhizae - physiology; Nitric oxide; Nitric Oxide - metabolism; nonsymbiotic hemoglobins; Pathogens; phytoglobins; Plant Proteins - genetics; Plant Proteins - metabolism; Regulatory sequences; Rhizophagus irregularis; Roots; Spores, Fungal - physiology; Symbiosis; Time Factors; tomato; Tomatoes; Up-Regulation - genetics
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.15898

The regulatory role of nitric oxide (NO) and phytoglobins in plant response to pathogenic and mutualistic microbes has been evidenced. However, little is known about their function in the arbuscular mycorrhizal (AM) symbiosis. We investigated whether NO and phytoglobin PHYTOGB1 are regulatory components in the AM symbiosis. Rhizophagus irregularis in vitro-grown cultures and tomato plants were used to monitor AM-associated NO-related root responses as compared to responses triggered by the pathogen Fusarium oxysporum. A genetic approach was conducted to understand the role of PHYTOGB1 on NO signaling during both interactions. After a common early peak in NO levels in response to both fungi, a specific NO accumulation pattern was triggered in tomato roots during the onset of the AM interaction. PHYTOGB1 was upregulated by the AM interaction. By contrast, the pathogen triggered a continuous NO accumulation and a strong downregulation of PHYTOGB1. Manipulation of PHYTOGB1 levels in overexpressing and silenced roots led to a deregulation of NO levels and altered mycorrhization and pathogen infection. We demonstrate that the onset of the AM symbiosis is associated with a specific NO-related signature in the host root. We propose that NO regulation by PHYTOGB1 is a regulatory component of the AM symbiosis.