Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization

Nitrogen‐fixing filamentous Frankia colonize the root tissues of its actinorhizal host Discaria trinervis via an exclusively intercellular pathway. Here we present studies aimed at uncovering mechanisms associated with this little‐researched mode of root entry, and in particular the extent to which the host plant is an active partner during this process. Detailed characterization of the expression patterns of infection‐associated actinorhizal host genes has provided valuable tools to identify intercellular infection sites, thus allowing in vivo confocal microscopic studies of the early stages of Frankia colonization. The subtilisin‐like serine protease gene Dt12, as well as its Casuarina glauca homolog Cg12, are specifically expressed at sites of Frankia intercellular colonization of D. trinervis outer root tissues. This is accompanied by nucleo‐cytoplasmic reorganization in the adjacent host cells and major remodeling of the intercellular apoplastic compartment. These findings lead us to propose that the actinorhizal host plays a major role in modifying both the size and composition of the intercellular apoplast in order to accommodate the filamentous microsymbiont. The implications of these findings are discussed in the light of the analogies that can be made with the orchestrating role of host legumes during intracellular root hair colonization by nitrogen‐fixing rhizobia.

Instituto de Fisiología y Recursos Genéticos Vegetales

Fil: Fournier, Joëlle. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia

Fil: Imanishi, Leandro Ezequiel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología. Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina

Fil: Chabaud, Mireille. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia

Fil: Abdou‐Pavy, Iltaf. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia

Fil: Genre, Andrea. University of Torino. Department of Life Sciences and Systems Biology; Italia

Fil: Brichet, Lukas. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia

Fil: Lascano, Hernan Ramiro. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina

Fil: Muñoz, Nacira Belen. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina

Fil: Vayssières, Alice. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia

Fil: Pirolles, Elodie. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia

Fil: Brottier, Laurent. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia

Fil: Gherbi, Hassen. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia

Fil: Hocher, Valérie. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia

Fil: Svistoonoff, Sergio. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia. Centre de Recherche de Bel Air. Laboratoire Mixte International Adaptation des Plantes et Microorganismes Associés aux Stress Environnementaux; Senegal. Institut de Recherche pour le Développement-Institut Sénégalais des Recherches Agricoles-Université Cheikh Anta Diop. Laboratoire Commun de Microbiologie; Senegal

Fil: Barker, David G. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia

Fil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología. Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina