Legumes are able to form a symbiotic relationship with nitrogen-fixing soil bacteria called rhizobia. It is well documented that inter-strain exchange of nodD genes can alter the response of the recipient strain to a different set. The association between leguminous plants and symbiotic rhizobia has stirred the Consequently, in order to promote legume-based phytoremediation through .. Although there can be numerous inter-replicon functional. Access to mineral nitrogen often limits plant growth, and so symbiotic relationships have evolved between plants and a variety of nitrogen-fixing.
Advanced Search Abstract Agricultural practices contribute to climate change by releasing greenhouse gases such as nitrous oxide that are mainly derived from nitrogen fertilizers.
Therefore, understanding biological nitrogen fixation in farming systems is beneficial to agriculture and environmental preservation. In this context, a better grasp of nitrogen-fixing systems and nitrogen-fixing bacteria-plant associations will contribute to the optimization of these biological processes.
Legumes and actinorhizal plants can engage in a symbiotic interaction with nitrogen-fixing rhizobia or actinomycetes, resulting in the formation of specialized root nodules. The legume-rhizobia interaction is mediated by a complex molecular signal exchange, where recognition of different bacterial determinants activates the nodulation program in the plant. To invade plants roots, bacteria follow different routes, which are determined by the host plant.
Entrance via root hairs is probably the best understood.
Alternatively, entry via intercellular invasion has been observed in many legumes. Although there are common features shared by intercellular infection mechanisms, differences are observed in the site of root invasion and bacterial spread on the cortex reaching and infecting a susceptible cell to form a nodule. This review focuses on intercellular bacterial invasion of roots observed in the Fabaceae and considers, within an evolutionary context, the different variants, distribution and molecular determinants involved.
Intercellular invasion of actinorhizal plants and Parasponia is also discussed. Actinorhizal plantsintercellular invasionlegumesmolecular signalingrhizobiasymbioses. Introduction The atmosphere is the major source of nitrogen in the biosphere. However, atmospheric nitrogen remains inaccessible to the majority of living organisms. Only a limited number of prokaryotes are able to convert atmospheric nitrogen into ammonia, making it available to be incorporated by the plants and, consequently, by the rest of the biota components.
Throughout evolution, leguminous and actinorhizal plants all belonging to the nitrogen-fixing clade within the Fabids or Eurosid I acquired the ability to develop an endosymbiotic relationship with these bacteria. In this symbiosis, prokaryotes fix nitrogen that is supplied to the plants in exchange for carbon sources and a controlled environment. The most extensively studied symbiotic association within the nitrogen-fixing clade is that established between legumes and rhizobia.
This symbiotic association is quite common in the Fabaceae family Soltis et al. The evidence for the importance of flavonoids in determining host range primarily comes from bacterial genetics, and the plant genes involved are less studied. Since legume roots secrete a complex mixture of flavonoid compounds, it is difficult to pinpoint which flavonoids play a more critical role, and when and where they are produced.
Recent studies in soybeans and Medicago truncatula have highlighted key flavonoids required for rhizobial infection reviewed in Liu and Murray, Although luteolin was the first flavonoid identified that can induce nod gene expression across a wide range of rhizobial strains, it is not legume-specific, mainly produced in germinating seeds, and has not been detected in root exudates or nodules. In contrast, methoxychalcone has been shown to be one of the strong host infection signals from Medicago and closely related legumes that form indeterminate nodules, while genistein and daidzein are crucial signals from soybeans that form determinate nodules.
Part of the flavonoid compounds may also function as phytoalexins, acting to reinforce symbiosis specificity Liu and Murray, For example, Bradyrhizobium japonicum and Mesorhizobium loti, but not the Medicago symbiont S.
Pankhurst and Biggs, ; Breakspear et al. Specificity Mediated by Nod-Factor Perception Nod factors produced by rhizobia are an essential signaling component for symbiosis development in most legumes. The common nodABC genes contribute to the synthesis of the chitin backbone, while other strain-specific nod genes act to modify the backbone by changing the size and saturation of the acyl chain, or adding to the terminal sugar units with acetyl, methyl, carbamoyl, sulfuryl or glycosyl groups.
Structural variations in Nod factors are a key determinant of host range, because these Nod factors have to be recognized by the host in order to initiate infection and nodulation Perret et al.
Nod factors are perceived by Nod-factor receptors e. Direct binding of Nod factors to the extracellular LysM domains of the receptor complex leads to activation of the downstream nodulation signaling pathways Broghammer et al. Specificity in Nod-factor binding is widely thought to be critical for recognition between the prospective symbiotic partners.
This hypothesis has been strongly supported by genetic evidence even though such binding specificity has not been demonstrated. The best examples are from the pea-R. In this case, allelic variation coupled with gene duplication and diversification contribute to alterations in symbiotic compatibility.
Nod factor recognition presumably plays a more critical role in determining host range at species level, which has been best illustrated on the bacterial side.
However, natural polymorphisms in Nod-factor receptors that are responsible for nodulation specificity between different legumes have not been well studied at the genetic level, simply because the plants cannot be interbred. Specificity Mediated by Perception of Rhizobial Exopolysaccharides In addition to Nod factors, rhizobial surface polysaccharides such as exopolysaccharides EPSlipopolysaccharides LPSand capsular polysaccharides KPS are also thought to be important for establishing symbiotic relationships Fraysse et al.
These surface components are proposed to be able to suppress plant defense, but their active roles in promoting bacterial infection and nodulation remain elusive and are dependent on the specific interactions studied. Exopolysaccharides have been shown to be required for rhizobial infection in multiple symbiotic interactions. This has been best illustrated in the Sinorhizobium-Medicago symbiosis, in which succinoglycan, a major EPS produced by S. For instance, a subset of EPS mutants of M.BASF Inoculants - The Basics Behind Rhizobia Bacteria
It was proposed that full-length EPS serves as a signal to compatible hosts to modulate plant defense responses and allow bacterial infection, and R7A mutants that make no EPS could avoid or suppress the plant surveillance system and therefore retain the ability to form nodules.
In contrast, strains that produce modified or truncated EPS trigger plant defense responses resulting in block of infection Kelly et al. EPS production is common in rhizobial bacteria, and the composition of EPS produced by different species varies widely Skorupska et al.
Several studies have suggested the involvement of the EPS structures in determining infective specificity Hotter and Scott, ; Kannenberg et al. Interestingly, Epr3 gene expression is contingent on Nod-factor signaling, suggesting that the bacterial entry to the host is controlled by two successive steps of receptor-mediated recognition of Nod factor and EPS signals Kawaharada et al.
The receptor-ligand interaction supports the notion that EPS recognition plays a role in regulation of symbiosis specificity. However, natural variation in host-range specificity that results from specific recognition between host receptors and strain-specific EPS has not been demonstrated in any legume-rhizobial interactions.
It is noteworthy that acidic EPS of bacterial pathogens also promote infection to cause plant disease Newman et al. Thus, rhizobial EPS might also be recognized by host immune receptors to induce defense responses that negatively regulate symbiosis development.
Rj4 encodes a thaumatin-like defense-related protein that restricts nodulation by specific strains of B. The function of these genes is dependent on the bacterial type III secretion system and its secreted effectors Krishnan et al. These studies indicate an important role of effector-triggered immunity in the regulation of nodulation specificity in soybeans.
Many rhizobial bacteria use the type III secretion system to deliver effectors into host cells to promote infection, and in certain situations, the delivered effector s are required for Nod-factor independent nodulation as demonstrated in the soybean-B. On the other hand, however, recognition of the effectors by host resistance genes triggers immune responses to restrict rhizobial infection.
The nodulation resistance genes occur frequently in natural populations, raising a question why host evolve and maintain such seemingly unfavorable alleles.
This could happen because of balancing selection, as the same alleles may also contribute to disease resistance against pathogens, considering that some rhizobial effectors are homologous to those secreted by bacterial pathogens Dai et al. Alternatively, legume may take advantage of R genes to exclude nodulation with less efficient nitrogen-fixing strains and selectively interact with strains with high nitrogen fixation efficiency, which is the case of the soybean Rj4 allele.
A single dominant locus, called NS1, was also identified in M. Unlike R gene-controlled host specificity in soybeans, which depends on bacterial type III secretion system, Rm41 strain lacks genes encoding such a system. It will be interesting to know what host gene s control this specificity and what bacterial signals are involved. Specificity in Nitrogen Fixation Symbiotic specificity is not confined to the early recognition stages; incompatible host-strain combinations can lead to formation of nodules that are defective in nitrogen fixation Fix.
For example, a screen of a core collection of Medicago accessions using multiple S. The Fix- phenotype was not due to a lack of infection but caused by bacteroid degradation after differentiation Yang et al. Host genetic control of nitrogen fixation specificity is very complicated in the Medicago-Sinorhizobium symbiosis, involving multiple linked loci with complex epistatic and allelic interactions.
By using the residual heterozygous lines identified from a recombination inbred line population, Zhu and colleagues were able to clone two of the underlying genes, namely NFS1 and NFS2, that regulate strain-specific nitrogen fixation concerning the S.
The NFS1 and NFS2 peptides function to provoke bacterial cell death and early nodule senescence in an allele-specific and rhizobial strain-specific manner, and their function is dependent on host genetic background. NCRs were previously shown to be positive regulators of symbiotic development, essential for terminal bacterial differentiation and for maintenance of bacterial survival in the nodule cells Van de Velde et al.
The genomes of M. These NCR genes, similar to bacterial type III effectors or MAMPs, can play both positive and negative roles in symbiotic development and both roles are associated with the antimicrobial property of the peptides.
On one hand, the host uses this antimicrobial strategy for promoting terminal bacteroid differentiation to enhance nitrogen fixation efficiency Oono and Denison, ; Oono et al.
On the other hand, some rhizobial strains cannot survive the antibacterial activity of certain peptide isoforms. The vulnerability of particular bacterial strains in response to a peptide is contingent on the genetic constitution of the bacteria as well as the genetic background of the host. It was proposed that this host-strain adaptation drives the coevolution of both symbiotic partners, leading to the rapid amplification and diversification of the NCR genes in galegoid legumes Wang et al.