Mycelial network-mediated rhizobial dispersal enhances legume nodulation.
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ABSTRACT:
SUBMITTER: Zhang W
PROVIDER: S-EPMC7082348 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Root-nodule symbiosis between leguminous plants and nitrogen-fixing bacteria (rhizobia) involves molecular communication between the two partners. Key components for the establishment of symbiosis are rhizobium-derived lipochitooligosaccharides (Nod factors; NFs) and their leguminous receptors (NFRs) that initiate nodule development and bacterial entry. Here we demonstrate that the soybean microsymbiont Bradyrhizobium elkanii uses the type III secretion system (T3SS), which is known for its delivery of virulence factors by pathogenic bacteria, to promote symbiosis. Intriguingly, wild-type B. elkanii, but not the T3SS-deficient mutant, was able to form nitrogen-fixing nodules on soybean nfr mutant En1282. Furthermore, even the NF-deficient B. elkanii mutant induced nodules unless T3SS genes were mutated. Transcriptional analysis revealed that expression of the soybean nodulation-specific genes ENOD40 and NIN was increased in the roots of En1282 inoculated with B. elkanii but not with its T3SS mutant, suggesting that T3SS activates host nodulation signaling by bypassing NF recognition. Root-hair curling and infection threads were not observed in the roots of En1282 inoculated with B. elkanii, indicating that T3SS is involved in crack entry or intercellular infection. These findings suggest that B. elkanii has adopted a pathogenic system for activating host symbiosis signaling to promote its infection.
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Project description:Legumes possess the autoregulation of nodulation (AON) pathway which is responsible for maintaining optimal root nodule number. In Lotus japonicus, AON comprises the CLE-HAR1-TML module, which plays an essential role in transmitting signals via root-to-shoot-to-root long-distance signaling. In addition to AON's principal role of negatively regulating nodule number, a recent study revealed another in the systemic control of rhizobial infection. Nitrate also negatively regulates the pleiotropic phases of legume-Rhizobium symbioses, including rhizobial infection and nodule number. Nitrate signaling has recently been shown to use AON components such as CLE-RS2 and HAR1 to control nodule number. Here we consider the role of a loss-of-function mutation in CLE-RS1, -RS2 and TML in rhizobial infection in relation to nitrate. Our results agree with previous findings and support the hypothesis that AON is required for the control of rhizobial infection but not for its nitrate-induced control. Furthermore, we confirm that the tml mutants exhibit nitrate sensitivity that differs from that of cle-rs2 and har1. Hence, while the nitrate-induced control mechanism of nodule number uses AON components, an unknown pathway specific to nitrate may exist downstream of HAR1, acting in parallel with the HAR1> TML pathway.
| S-EPMC7194392 | biostudies-literature
Project description:Rhizobia-legume symbiosis is the most well researched biological nitrogen fixation system. Coating legume seeds with rhizobia is now a recognized practical measure for improving the production of legume corp. However, the efficacy of some commercial rhizobia inoculants cannot be guaranteed in China due to the low rate of live rhizobia in these products. A greenhouse experiment was conducted to assess the effects of different rhizobial inoculant formulations on alfalfa productivity and nitrogen fixation. Two rhizobia strains, (ACCC17631 and ACCC17676), that are effective partners with alfalfa variety Zhongmu No. 1 were assessed with different concentrations of ammonium molybdate in seed-coat formulations with two different coating adhesives. Our study showed that the growth, nodulation, and nitrogen fixation ability of the plants inoculated with the ACCC17631 rhizobial strain were greatest when the ammonium molybdate application was0.2% of the formulation. An ammonium molybdate concentration of 0.1% was most beneficial to the growth of the plants inoculated with the ACCC17676 rhizobial strain. The sodium carboxymethyl cellulose and sodium alginate, used as coating adhesives, did not have a significant effect on alfalfa biomass and nitrogen fixation. However, the addition of skimmed milk to the adhesive improved nitrogenase activity. These results demonstrate that a new rhizobial seed-coat formulation benefitted alfalfa nodulation and yield.
| S-EPMC5242510 | biostudies-literature
Project description:Plant NADPH oxidases, formerly known as respiratory burst oxidase homologues (RBOHs), are plasma membrane enzymes dedicated to reactive oxygen species (ROS) production. These oxidases are implicated in a wide variety of processes, ranging from tissue and organ growth and development to signaling pathways in response to abiotic and biotic stimuli. Research on the roles of RBOHs in the plant's response to biotic stresses has mainly focused on plant-pathogen interactions; nonetheless, recent findings have shown that these oxidases are also involved in the legume-rhizobia symbiosis. The legume-rhizobia symbiosis leads to the formation of the root nodule, where rhizobia reduce atmospheric nitrogen to ammonia. A complex signaling and developmental pathway in the legume root hair and root facilitate rhizobial entrance and nodule organogenesis, respectively. Interestingly, several reports demonstrate that RBOH-mediated ROS production displays versatile roles at different stages of nodulation. The evidence collected to date indicates that ROS act as signaling molecules that regulate rhizobial invasion and also function in nodule senescence. This review summarizes discoveries that support the key and versatile roles of various RBOH members in the legume-rhizobia symbiosis.
| S-EPMC4881506 | biostudies-other
Project description:Certain alpha- and beta-proteobacteria, the rhizobia, are able to infect legume roots, elicit root nodules, and live therein as endosymbiotic, nitrogen-fixing bacteroids. Host recognition and specificity are the results of consecutive programming events in bacteria and host plants in which important signaling molecules, e.g. plant flavonoids and rhizobial lipooligosaccharides, play key roles. Here, we introduce a new aspect of this symbiosis: the adaptive response to hosts. In contrast to host specificity, which determines early steps in bacteria-plant interaction, the adaptation to hosts refers to late events in mature bacteroids where specific genes are transcribed and translated that help the endosymbionts to meet the disparate environmental requirements imposed by the hosts in which they live. This concept was elaborated with Bradyrhizobium japonicum and three different legumes (soybean, cowpea, siratro). We systematically analyzed and compared the transcriptomes as well as the proteomes in bacteroids from root nodules of the three hosts. Transcripts and proteins were thus identified which are induced in only one of the three hosts. We then focused on those determinants that were congruent in the two data sets of host-specific transcripts and proteins, and arrived at 20 for soybean, 7 for siratro, and 4 for cowpea. One conspicuous gene cluster for a predicted ABC-type transporter, differentially expressed in siratro, was deleted. The corresponding mutant had a symbiotic defect on siratro rather than on soybean or cowpea. This result demonstrates the value of the applied approach and corroborates the host-specific adaptation concept.
2010-03-07 | GSE18884 | GEO
Project description:Lipochitin oligosaccharides called Nod factors function as primary rhizobial signal molecules triggering legumes to develop new plant organs: root nodules that host the bacteria as nitrogen-fixing bacteroids. Here, we show that the Lotus japonicus Nod factor receptor 5 (NFR5) and Nod factor receptor 1 (NFR1) bind Nod factor directly at high-affinity binding sites. Both receptor proteins were posttranslationally processed when expressed as fusion proteins and extracted from purified membrane fractions of Nicotiana benthamiana or Arabidopsis thaliana. The N-terminal signal peptides were cleaved, and NFR1 protein retained its in vitro kinase activity. Processing of NFR5 protein was characterized by determining the N-glycosylation patterns of the ectodomain. Two different glycan structures with identical composition, Man(3)XylFucGlcNAc(4), were identified by mass spectrometry and located at amino acid positions N68 and N198. Receptor-ligand interaction was measured by using ligands that were labeled or immobilized by application of chemoselective chemistry at the anomeric center. High-affinity ligand binding was demonstrated with both solid-phase and free solution techniques. The K(d) values obtained for Nod factor binding were in the nanomolar range and comparable to the concentration range sufficient for biological activity. Structure-dependent ligand specificity was shown by using chitin oligosaccharides. Taken together, our results suggest that ligand recognition through direct ligand binding is a key step in the receptor-mediated activation mechanism leading to root nodule development in legumes.
| S-EPMC3427107 | biostudies-literature
Project description:The environmental context of the nitrogen-fixing mutualism between leguminous plants and rhizobial bacteria varies over space and time. Variation in resource availability, population density, and composition likely affect the ecology and evolution of rhizobia and their symbiotic interactions with hosts. We examined how host genotype, nitrogen addition, rhizobial density, and community complexity affected selection on 68 rhizobial strains in the Sinorhizobium meliloti-Medicago truncatula mutualism. As expected, host genotype had a substantial effect on the size, number, and strain composition of root nodules (the symbiotic organ). The understudied environmental variable of rhizobial density had a stronger effect on nodule strain frequency than the addition of low nitrogen levels. Higher inoculum density resulted in a nodule community that was less diverse and more beneficial but only in the context of the more selective host genotype. Higher density resulted in more diverse and less beneficial nodule communities with the less selective host. Density effects on strain composition deserve additional scrutiny as they can create feedback between ecological and evolutionary processes. Finally, we found that relative strain rankings were stable across increasing community complexity (2, 3, 8, or 68 strains). This unexpected result suggests that higher-order interactions between strains are rare in the context of nodule formation and development. Our work highlights the importance of examining mechanisms of density-dependent strain fitness and developing theoretical predictions that incorporate density dependence. Furthermore, our results have translational relevance for overcoming establishment barriers in bioinoculants and motivating breeding programs that maintain beneficial plant-microbe interactions across diverse agroecological contexts. IMPORTANCE Legume crops establish beneficial associations with rhizobial bacteria that perform biological nitrogen fixation, providing nitrogen to plants without the economic and greenhouse gas emission costs of chemical nitrogen inputs. Here, we examine the influence of three environmental factors that vary in agricultural fields on strain relative fitness in nodules. In addition to manipulating nitrogen, we also use two biotic variables that have rarely been examined: the rhizobial community's density and complexity. Taken together, our results suggest that (i) breeding legume varieties that select beneficial strains despite environmental variation is possible, (ii) changes in rhizobial population densities that occur routinely in agricultural fields could drive evolutionary changes in rhizobial populations, and (iii) the lack of higher-order interactions between strains will allow the high-throughput assessments of rhizobia winners and losers during plant interactions.
| S-EPMC9361818 | biostudies-literature
Project description:Certain alpha- and beta-proteobacteria, the rhizobia, are able to infect legume roots, elicit root nodules, and live therein as endosymbiotic, nitrogen-fixing bacteroids. Host recognition and specificity are the results of consecutive programming events in bacteria and host plants in which important signaling molecules, e.g. plant flavonoids and rhizobial lipooligosaccharides, play key roles. Here, we introduce a new aspect of this symbiosis: the adaptive response to hosts. In contrast to host specificity, which determines early steps in bacteria-plant interaction, the adaptation to hosts refers to late events in mature bacteroids where specific genes are transcribed and translated that help the endosymbionts to meet the disparate environmental requirements imposed by the hosts in which they live. This concept was elaborated with Bradyrhizobium japonicum and three different legumes (soybean, cowpea, siratro). We systematically analyzed and compared the transcriptomes as well as the proteomes in bacteroids from root nodules of the three hosts. Transcripts and proteins were thus identified which are induced in only one of the three hosts. We then focused on those determinants that were congruent in the two data sets of host-specific transcripts and proteins, and arrived at 20 for soybean, 7 for siratro, and 4 for cowpea. One conspicuous gene cluster for a predicted ABC-type transporter, differentially expressed in siratro, was deleted. The corresponding mutant had a symbiotic defect on siratro rather than on soybean or cowpea. This result demonstrates the value of the applied approach and corroborates the host-specific adaptation concept. B. japonicum transcriptome was determined for the three different host plants
2010-05-06 | E-GEOD-18884 | biostudies-arrayexpress
Project description:We hypothesized that population diversities of partners in nitrogen-fixing rhizobium-legume symbiosis can be matched for "interplaying" genes. We tested this hypothesis using data on nucleotide polymorphism of symbiotic genes encoding two components of the plant-bacteria signaling system: (a) the rhizobial nodA acyltransferase involved in the fatty acid tail decoration of the Nod factor (signaling molecule); (b) the plant NFR5 receptor required for Nod factor binding. We collected three wild-growing legume species together with soil samples adjacent to the roots from one large 25-year fallow: Vicia sativa, Lathyrus pratensis, and Trifolium hybridum nodulated by one of the two Rhizobium leguminosarum biovars (viciae and trifolii). For each plant species, we prepared three pools for DNA extraction and further sequencing: the plant pool (30 plant indiv.), the nodule pool (90 nodules), and the soil pool (30 samples). We observed the following statistically significant conclusions: (a) a monotonic relationship between the diversity in the plant NFR5 gene pools and the nodule rhizobial nodA gene pools; (b) higher topological similarity of the NFR5 gene tree with the nodA gene tree of the nodule pool, than with the nodA gene tree of the soil pool. Both nonsynonymous diversity and Tajima's D were increased in the nodule pools compared with the soil pools, consistent with relaxation of negative selection and/or admixture of balancing selection. We propose that the observed genetic concordance between NFR5 gene pools and nodule nodA gene pools arises from the selection of particular genotypes of the nodA gene by the host plant.
| S-EPMC6787799 | biostudies-literature
Project description:Among legumes (Fabaceae) capable of nitrogen-fixing nodulation, several Aeschynomene spp. use a unique symbiotic process that is independent of Nod factors and infection threads. They are also distinctive in developing root and stem nodules with photosynthetic bradyrhizobia. Despite the significance of these symbiotic features, their understanding remains limited. To overcome such limitations, we conduct genetic studies of nodulation in Aeschynomene evenia, supported by the development of a genome sequence for A. evenia and transcriptomic resources for 10 additional Aeschynomene spp. Comparative analysis of symbiotic genes substantiates singular mechanisms in the early and late nodulation steps. A forward genetic screen also shows that AeCRK, coding a receptor-like kinase, and the symbiotic signaling genes AePOLLUX, AeCCamK, AeCYCLOPS, AeNSP2, and AeNIN are required to trigger both root and stem nodulation. This work demonstrates the utility of the A. evenia model and provides a cornerstone to unravel mechanisms underlying the rhizobium-legume symbiosis.
| S-EPMC7864950 | biostudies-literature