Nodulation outer proteins: double-edged swords of symbiotic rhizobia

Abstract

Rhizobia are nitrogen-fixing bacteria that establish a nodule symbiosis with legumes. Nodule formation depends on signals and surface determinants produced by both symbiotic partners. Among them, rhizobial Nops (nodulation outer proteins) play a crucial symbiotic role in many strain-host combinations. Nops are defined as proteins secreted via a rhizobial T3SS (type III secretion system). Functional T3SSs have been characterized in many rhizobial strains. Nops have been identified 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 T3 (type III) pili. Other Nops are T3 effector proteins that can be translocated into plant cells. Rhizobial T3 effectors manipulate cellular processes in host cells to suppress plant defence responses against rhizobia and 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 R (resistance) proteins can result in effector triggered defence responses that negatively affect rhizobial infection. 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 the 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.

The Sinorhizobium (Ensifer) fredii HH103 Nodulation Outer Protein NopI Is a Determinant for Efficient Nodulation of Soybean and Cowpea Plants

“…In Sinorhizobium fredii, mutations in genes coding for components of the T3SS machinery, including the extracellular appendages, completely block the secretion of Nops. However, inactivation of genes coding for potential effectors does not alter the secretion of other nodulation outer proteins (21). It is worth noting that the bands corresponding to the Nops previously identified in HH103, with the exception of NopD, which is not easy to detect in gels due to its high molecular mass, were present in the lanes corresponding to the parental strain HH103 Rif r and the nopI mutant (Fig.…”

“…All of these results indicated that NopI can be considered a nodulation outer protein. In Sinorhizobium fredii, mutations in genes coding for components of the T3SS machinery, including the extracellular appendages, completely block the secretion of Nops (21). The mutation of nopI and nopL did not affect secretion to the extracellular medium of Nops other than NopI and NopL, respectively, suggesting that they were not essential components of the T3SS machinery (Fig.…”

“…Analyses of T3SS-dependent translocations of putative effectors from several Sinorhizobium fredii (not including HH103) and Bradyrhizobium japonicum strains using heterologous Pseudomonas-Arabidopsis and Pseudomonas-tobacco systems have been performed (19,20). However, in some cases, positive results were obtained with components of the T3SS machinery, indicating that these results must be interpreted with caution (21). Other authors have confirmed direct delivery of Nops to the cytoplasm of the host cell by fusing to the carboxy terminus of the T3SS effector the calmodulin-dependent adenylate cyclase (Cya) reporter protein.…”

“…In the case of NopL, translocation studies have been performed in Nicotiana benthamiana and Arabidopsis leaves using heterologous Pseudomonas systems (19,20). However, results obtained with these systems must be interpreted with caution, and more experiments are required to clarify the discrepancies obtained with this type of study to unequivocally describe a nodulation outer protein as a symbiotic effector (21). Interestingly, NopL, NopP, and NopC are specific to rhizobia and have no homologues in plant and animal pathogens.…”

High-quality permanent draft genome sequence of the Bradyrhizobium elkanii type strain USDA 76T, isolated from Glycine max (L.) Merr

“…The Type III secretion system (T3SS) [55] can either promote or impair the establishment of symbiosis, depending on the legume host [56], and has been characterized as a host determinant for rj1, Rfg1, Rj2 and Rj4 soybean cultivars [33, 57, 58]. The dominant soybean genes Rj2 and Rj4 restrict nodulation with specific strains of Bradyrhizobium [33].…”