Host-secreted antimicrobial peptide enforces symbiotic selectivity in <i>Medicago truncatula</i>

Abstract

Legumes engage in root nodule symbioses with nitrogen-fixing soil bacteria known as rhizobia. In nodule cells, bacteria are enclosed in membrane-bound vesicles called symbiosomes and differentiate into bacteroids that are capable of converting atmospheric nitrogen into ammonia. Bacteroid differentiation and prolonged intracellular survival are essential for development of functional nodules. However, in the <i>Medicago truncatula</i>-<i>Sinorhizobium meliloti</i> symbiosis, incompatibility between symbiotic partners frequently occurs, leading to the formation of infected nodules defective in nitrogen fixation (Fix^-). Here, we report the identification and cloning of the <i>M. truncatula NFS2</i> gene that regulates this type of specificity pertaining to <i>S. meliloti</i> strain Rm41. We demonstrate that <i>NFS2</i> encodes a nodule-specific cysteine-rich (NCR) peptide that acts to promote bacterial lysis after differentiation. The negative role of <i>NFS2</i> in symbiosis is contingent on host genetic background and can be counteracted by other genes encoded by the host. This work extends the paradigm of NCR function to include the negative regulation of symbiotic persistence in host-strain interactions. Our data suggest that NCR peptides are host determinants of symbiotic specificity in <i>M. truncatula</i> and possibly in closely related legumes that form indeterminate nodules in which bacterial symbionts undergo terminal differentiation.