Biological nitrogen fixation in non-legume plants

Abstract

Background: Nitrogen is an essential nutrient in plant growth. The ability of a plant to supply all or part of its requirements from biological nitrogen fixation (BNF) thanks to interactions with endosymbiotic, associative and endophytic symbionts, confers a great competitive advantage over non-nitrogen-fixing plants.

Scope: Because BNF in legumes is well documented, this review focuses on BNF in non-legume plants. Despite the phylogenic and ecological diversity among diazotrophic bacteria and their hosts, tightly regulated communication is always necessary between the microorganisms and the host plant to achieve a successful interaction. Ongoing research efforts to improve knowledge of the molecular mechanisms underlying these original relationships and some common strategies leading to a successful relationship between the nitrogen-fixing microorganisms and their hosts are presented.

Conclusions: Understanding the molecular mechanism of BNF outside the legume-rhizobium symbiosis could have important agronomic implications and enable the use of N-fertilizers to be reduced or even avoided. Indeed, in the short term, improved understanding could lead to more sustainable exploitation of the biodiversity of nitrogen-fixing organisms and, in the longer term, to the transfer of endosymbiotic nitrogen-fixation capacities to major non-legume crops.

Fig. 1.

Schematic representation of actinorhizal root infection by Frankia. Frankia penetrates via a root hair infection process in host plants from the families Betulaceae, Casuarinaceae and Myricaceae, and intercellularly in Eleagnaceae, Rosaceae and Rhamnaceae. Prenodule formation resulting from mitotic activity in the root cortical cells is observed only during the intracellular infection process. Nodule primordia arise from divisions in root pericycle cells, located opposite a protoxylem pole, and near the site of infection. Frankia hyphae progress either from cell to cell in the intracellular mode of infection, or apoplastically in a matrix secreted into the intercellular spaces. Frankia hyphae progress towards the nodule primordium where they will penetrate developing cortical cells intracellularly. Mature nodules consist of multiple lobes. Adapted from Franche and Bogusz (2011)).

Fig. 2.

Schematic representation of the infection process in cyanobacteria–plant symbioses. In nitrogen-free medium, Nostoc sp. filaments consist of vegetative cells (V) and regularly spaced heterocysts (H) that fix nitrogen. A hormogonium inducing factor (HIF) produced by the host under nitrogen starvation conditions leads to differentiation of motile small-celled hormogonial structures. Following the exchange of appropriate recognition signals, hormogonia penetrate the host symbiotic cavities and revert to vegetative filaments with a large number of heterocysts. The repression of hormogonia is linked to a hormogonia repressing factor (HRF). In ageing symbiotic tissues, multiple contiguous heterocysts are observed that exhibit low nitrogen-fixation activity. Adapted from Rai et al. (2000) and Meeks (2005b).