New perspectives on nodule nitrogen assimilation in actinorhizal symbioses Alison M. Berry A,E , Alberto Mendoza-Herrera B , Ying-Yi Guo A , Jennifer Hayashi A , Tomas Persson C , Ravi Barabote A , Kirill Demchenko D , Shuxiao Zhang A and Katharina Pawlowski C A Department of Plant Sciences, University of California, Davis, CA 95616, USA. B Centro de Biotecnología Genómica, Instituto Politécnico Nacional, 88710 Reynosa, Tamaulipas, Mexico. C Department of Botany, Stockholm University, 10691 Stockholm, Sweden. D Komarov Botanical Institute, Russian Academy of Sciences, St Petersburg 197376, Russia. E Corresponding author. Email: amberry@ucdavis.edu This paper originates from a presentation at the 16th International Meeting on Frankia and Actinorhizal Plants, Oporto, Portugal, 5–8 September 2010. Abstract. Nitrogen-fixing root nodules are plant organs specialised for symbiotic transfer of nitrogen and carbon between microsymbiont and host. The organisation of nitrogen assimilation, storage and transport processes is partitioned at the subcellular and tissue levels, in distinctive patterns depending on the symbiotic partners. In this review, recent advances in understanding of actinorhizal nodule nitrogen assimilation are presented. New findings indicate that Frankia within nodules of Datisca glomerata (Presl.) Baill. carries out both primary nitrogen assimilation and biosynthesis of arginine, rather than exporting ammonium. Arginine is a typical storage form of nitrogen in plant tissues, but is a novel nitrogen carrier molecule in root nodule symbioses. Thus Frankia within D. glomerata nodules exhibits considerable metabolic independence. Furthermore, nitrogen reassimilation is likely to take place in the host in the uninfected nodule cortical cells of this root nodule symbiosis, before amino acid export to host sink tissues via the xylem. The role of an augmented pericycle in carbon and nitrogen exchange in root nodules deserves further attention in actinorhizal symbiosis, and further highlights the importance of a comprehensive, structure–function approach to understanding function in root nodules. Moreover, the multiple patterns of compartmentalisation in relation to nitrogen flux within root nodules demonstrate the diversity of possible functional interactions between host and microsymbiont that have evolved in the nitrogen-fixing clade. Additional keywords: Datisca glomerata, Frankia, nitrogen fixation, root nodule, symbiosis. Introduction The biological reduction of atmospheric dinitrogen (nitrogen fixation) is the fundamental process that provides essential nitrogen to the biosphere as ammonium. A major fraction of symbiotic nitrogen fixation worldwide is contributed by actinorhizal symbioses formed by the association between soil-dwelling, Gram-positive actinobacteria of the genus Frankia and a group of more than 200 mostly woody plant species from eight different families, collectively called actinorhizal plants. Actinorhizal plants fall into three phylogenetically-related groups (see review by Pawlowski et al. 2011): Fagales (Betulaceae, Casuarinaceae, Myricaceae), Cucurbitales (Datiscaceae, Coriariaceae) and Rosales (Rosaceae, Elaeagnaceae, Rhamnaceae), which, together with the legumes (Fabales), form a single ‘nitrogen-fixing clade’ within the angiosperms (Soltis et al. 1995). In all of these symbioses, the host plants form root nodules, highly-specialised organs for nitrogen production, wherein the bacteria carry out nitrogen fixation while being supplied by the plant with photosynthetically-derived carbon. Understanding the functional partitioning of carbon and nitrogen fluxes in root nodules is of key importance in unravelling the molecular and evolutionary basis of symbiotic adaptation between the partners. This partitioning is very complex, involving subcellular metabolic interactions between the host organelles and the microsymbiont, and higher-order patterns of cell–cell interaction and tissue specialisation, to enable metabolite transport and the sequential steps of metabolite transformation (Schubert 1986; Lodwig et al. 2003; Valverde and Huss-Danell 2008). For legume symbioses and many of the actinorhizal symbioses, strategies for functional partitioning of nodule CSIRO PUBLISHING Review www.publish.csiro.au/journals/fpb Functional Plant Biology, 2011, 38, 645–652 Ó CSIRO 2011 10.1071/FP11095 1445-4408/11/090645