Nodulation outer proteins: double-edged swords of symbiotic rhizobia

Rhizobia are nitrogen-fixing bacteria that establish a nodule symbiosis with legumes. Nodule formation is the result of a complex bacterial infection process, which depends on signals and surface determinants produced by both symbiotic partners. Among them, rhizobial nodulation outer proteins (Nops) play a crucial symbiotic role in many strain-host combinations. Nops are defined as proteins secreted via a rhizobial type 3 secretion system (T3SS). Functional T3SSs have been characterized in various rhizobial strains belonging to the genera Sinorhizobium, Bradyrhizobium, Mesorhizobium and Cupriavidus. Expression of Nops in rhizobia is usually induced by flavonoid signals of the host plant. Nops have been indentified using various genetic, biochemical, proteomic, genomic and experimental approaches. Certain Nops represent extracellular components of the T3SS, which are visible in electron micrographs as bacterial surface appendages called type 3 (T3) pili. Other Nops are T3 effector proteins that can be translocated via T3 pili into plant cells. Some rhizobial T3 effectors are structurally related to effectors of pathogenic bacteria, while others are specific for rhizobia. Once delivered to host cells, a set of rhizobial T3 effectors manipulate cellular processes to suppress plant defense responses against rhizobia. Other T3 effectors appear to promote symbiosis-related processes. Accordingly, mutant strains deficient in synthesis or secretion of T3 effectors show reduced symbiotic properties on certain host plants. On the other hand, direct or indirect recognition of T3 effectors by plant cells expressing specific resistance (R) proteins can result in effector triggered defense responses that negatively affect rhizobial infection and nodule formation. Hence, Nops are double-edged swords that may promote establishment of symbiosis with one legume (symbiotic factors) and impair symbiotic processes when bacteria are inoculated on another legume species (asymbiotic factors). In this present review, we provide an overview of our current understanding of Nops. We summarize their symbiotic effects, their biochemical properties and their possible modes of action. Finally, we discuss future perspectives in the field of T3 effector research.