The Rhizobial Type 3 Secretion System: The Dr. Jekyll and Mr. Hyde in the Rhizobium-Legume Symbiosis

Abstract

Rhizobia are soil bacteria that can establish a symbiotic association with legumes. As a result, plant nodules are formed on the roots of the host plants where rhizobia differentiate to bacteroids capable of fixing atmospheric nitrogen into ammonia. This ammonia is transferred to the plant in exchange of a carbon source and an appropriate environment for bacterial survival. This process is subjected to a tight regulation with several checkpoints to allow the progression of the infection or its restriction. The type 3 secretion system (T3SS) is a secretory system that injects proteins, called effectors (T3E), directly into the cytoplasm of the host cell, altering host pathways or suppressing host defense responses. This secretion system is not present in all rhizobia but its role in symbiosis is crucial for some symbiotic associations, showing two possible faces as Dr. Jekyll and Mr. Hyde: it can be completely necessary for the formation of nodules, or it can block nodulation in different legume species/cultivars. In this review, we compile all the information currently available about the effects of different rhizobial effectors on plant symbiotic phenotypes. These phenotypes are diverse and highlight the importance of the T3SS in certain rhizobium-legume symbioses.

Keywords: T3SS; effector; rhizobium; symbiosis; type 3 secretion system.

Figure 1

General checkpoints in rhizobia–legumes symbiosis. (A) Specificity in nod factor and flavonoid production and detection during rhizobial colonization, infection, and invasion throughout the nodulation process. (B) Rhizobial surface polysaccharides [exopolysaccharides (EPS), lipopolysaccharides (LPS), K-antigen polysaccharides (KPS) and cyclin glucans (CG)] play a role either as signal molecules required for the progression of symbiosis and/or as protective agents against plant defense responses. (C) Effectors translocated through the rhizobial type III secretion system (T3SS), type IV secretion system (T4SS) or type VI secretion system (T6SS) can modulate plant defense responses to facilitate bacterial infection of the host. The T6SS can also be used as a killing machine devoted to outcompeting other rhizosphere bacteria.