scholarly journals The Influence of the Host Plant Is the Major Ecological Determinant of the Presence of Nitrogen-Fixing Root Nodule Symbiont Cluster II Frankia Species in Soil

2016 ◽  
Vol 83 (1) ◽  
Author(s):  
Kai Battenberg ◽  
Jannah A. Wren ◽  
Janell Hillman ◽  
Joseph Edwards ◽  
Liujing Huang ◽  
...  

ABSTRACT The actinobacterial genus Frankia establishes nitrogen-fixing root nodule symbioses with specific hosts within the nitrogen-fixing plant clade. Of four genetically distinct subgroups of Frankia, cluster I, II, and III strains are capable of forming effective nitrogen-fixing symbiotic associations, while cluster IV strains generally do not. Cluster II Frankia strains have rarely been detected in soil devoid of host plants, unlike cluster I or III strains, suggesting a stronger association with their host. To investigate the degree of host influence, we characterized the cluster II Frankia strain distribution in rhizosphere soil in three locations in northern California. The presence/absence of cluster II Frankia strains at a given site correlated significantly with the presence/absence of host plants on the site, as determined by glutamine synthetase (glnA) gene sequence analysis, and by microbiome analysis (16S rRNA gene) of a subset of host/nonhost rhizosphere soils. However, the distribution of cluster II Frankia strains was not significantly affected by other potential determinants such as host-plant species, geographical location, climate, soil pH, or soil type. Rhizosphere soil microbiome analysis showed that cluster II Frankia strains occupied only a minute fraction of the microbiome even in the host-plant-present site and further revealed no statistically significant difference in the α-diversity or in the microbiome composition between the host-plant-present or -absent sites. Taken together, these data suggest that host plants provide a factor that is specific for cluster II Frankia strains, not a general growth-promoting factor. Further, the factor accumulates or is transported at the site level, i.e., beyond the host rhizosphere. IMPORTANCE Biological nitrogen fixation is a bacterial process that accounts for a major fraction of net new nitrogen input in terrestrial ecosystems. Transfer of fixed nitrogen to plant biomass is especially efficient via root nodule symbioses, which represent evolutionarily and ecologically specialized mutualistic associations. Frankia spp. (Actinobacteria), especially cluster II Frankia spp., have an extremely broad host range, yet comparatively little is known about the soil ecology of these organisms in relation to the host plants and their rhizosphere microbiomes. This study reveals a strong influence of the host plant on soil distribution of cluster II Frankia spp.

2017 ◽  
Vol 84 (5) ◽  
Author(s):  
Seifeddine Ben Tekaya ◽  
Trina Guerra ◽  
David Rodriguez ◽  
Jeffrey O. Dawson ◽  
Dittmar Hahn

ABSTRACTActinorhizal plants form nitrogen-fixing root nodules in symbiosis with soil-dwelling actinobacteria within the genusFrankia, and specificFrankiataxonomic clusters nodulate plants in corresponding host infection groups. In same-soil microcosms, we observed that some host species were nodulated (Alnus glutinosa,Alnus cordata,Shepherdia argentea,Casuarina equisetifolia) while others were not (Alnus viridis,Hippophaë rhamnoides). Nodule populations were represented by eight different sequences ofnifHgene fragments. Two of these sequences characterized frankiae inS. argenteanodules, and three others characterized frankiae inA. glutinosanodules. Frankiae inA. cordatanodules were represented by five sequences, one of which was also found in nodules fromA. glutinosaandC. equisetifolia, while another was detected in nodules fromA. glutinosa. Quantitative PCR assays showed that vegetation generally increased the abundance of frankiae in soil, independently of the target gene (i.e.,nifHor the 23S rRNA gene). Targeted Illumina sequencing ofFrankia-specificnifHgene fragments detected 24 unique sequences from rhizosphere soils, 4 of which were also found in nodules, while the remaining 4 sequences in nodules were not found in soils. Seven of the 24 sequences from soils represented >90% of the reads obtained in most samples; the 2 most abundant sequences from soils were not found in root nodules, and only 2 of the sequences from soils were detected in nodules. These results demonstrate large differences between detectableFrankiapopulations in soil and those in root nodules, suggesting that root nodule formation is not a function of the abundance or relative diversity of specificFrankiapopulations in soils.IMPORTANCEThe nitrogen-fixing actinobacteriumFrankiaforms root nodules on actinorhizal plants, with members of specificFrankiataxonomic clusters nodulating plants in corresponding host infection groups. We assessedFrankiadiversity in root nodules of different host plant species, and we related specific populations to the abundance and relative distribution of indigenous frankiae in rhizosphere soils. Large differences were observed between detectableFrankiapopulations in soil and those in root nodules, suggesting that root nodule formation is not a function of the abundance or relative diversity of specificFrankiapopulations in soils but rather results from plants potentially selecting frankiae from the soil for root nodule formation. These data also highlight the necessity of using a combination of different assessment tools so as to adequately address methodological constraints that could produce contradictory data sets.


2014 ◽  
Vol 80 (18) ◽  
pp. 5709-5716 ◽  
Author(s):  
M. M. Perrineau ◽  
C. Le Roux ◽  
A. Galiana ◽  
A. Faye ◽  
R. Duponnois ◽  
...  

ABSTRACTIntroducing nitrogen-fixing bacteria as an inoculum in association with legume crops is a common practice in agriculture. However, the question of the evolution of these introduced microorganisms remains crucial, both in terms of microbial ecology and agronomy. We explored this question by analyzing the genetic and symbiotic evolution of twoBradyrhizobiumstrains inoculated onAcacia mangiumin Malaysia and Senegal 15 and 5 years, respectively, after their introduction. Based on typing of several loci, we showed that these two strains, although closely related and originally sampled in Australia, evolved differently. One strain was recovered in soil with the same five loci as the original isolate, whereas the symbiotic cluster of the other strain was detected with no trace of the three housekeeping genes of the original inoculum. Moreover, the nitrogen fixation efficiency was variable among these isolates (either recombinant or not), with significantly high, low, or similar efficiencies compared to the two original strains and no significant difference between recombinant and nonrecombinant isolates. These data suggested that 15 years after their introduction, nitrogen-fixing bacteria remain in the soil but that closely related inoculant strains may not evolve in the same way, either genetically or symbiotically. In a context of increasing agronomical use of microbial inoculants (for biological control, nitrogen fixation, or plant growth promotion), this result feeds the debate on the consequences associated with such practices.


2016 ◽  
Vol 83 (5) ◽  
Author(s):  
Seifeddine Ben Tekaya ◽  
Abirama Sundari Ganesan ◽  
Trina Guerra ◽  
Jeffrey O. Dawson ◽  
Michael R. J. Forstner ◽  
...  

ABSTRACT The nodule-forming actinobacterial genus Frankia can generally be divided into 4 taxonomic clusters, with clusters 1, 2, and 3 representing nitrogen-fixing strains of different host infection groups and cluster 4 representing atypical, generally non-nitrogen-fixing strains. Recently, quantitative PCR (qPCR)-based quantification methods have been developed for frankiae of clusters 1 and 3; however, similar approaches for clusters 2 and 4 were missing. We amended a database of partial 23S rRNA gene sequences of Frankia strains belonging to clusters 1 and 3 with sequences of frankiae representing clusters 2 and 4. The alignment allowed us to design primers and probes for the specific detection and quantification of these Frankia clusters by either Sybr Green- or TaqMan-based qPCR. Analyses of frankiae in different soils, all obtained from the same region in Illinois, USA, provided similar results, independent of the qPCR method applied, with abundance estimates of 10 × 105 to 15 × 105 cells (g soil)−1 depending on the soil. Diversity was higher in prairie soils (native, restored, and cultivated), with frankiae of all 4 clusters detected and those of cluster 4 dominating, while diversity in soils under Alnus glutinosa, a host plant for cluster 1 frankiae, or Betula nigra, a related nonhost plant, was restricted to cluster 1 and 3 frankiae and generally members of subgroup 1b were dominating. These results indicate that vegetation affects the basic composition of frankiae in soils, with higher diversity in prairie soils compared to much more restricted diversity under some host and nonhost trees. IMPORTANCE Root nodule formation by the actinobacterium Frankia is host plant specific and largely, but not exclusively, correlates with assignments of strains to specific clusters within the genus. Due to the lack of adequate detection and quantification tools, studies on Frankia have been limited to clusters 1 and 3 and generally excluded clusters 2 and 4. We have developed tools for the detection and quantification of clusters 2 and 4, which can now be used in combination with those developed for clusters 1 and 3 to retrieve information on the ecology of all clusters delineated within the genus Frankia. Our initial results indicate that vegetation affects the basic composition of frankiae in soils, with higher diversity in prairie soils compared to much more restricted diversity under some host and nonhost trees.


2014 ◽  
Vol 80 (7) ◽  
pp. 2094-2101 ◽  
Author(s):  
Marion Koch ◽  
Nathanaël Delmotte ◽  
Christian H. Ahrens ◽  
Ulrich Omasits ◽  
Kathrin Schneider ◽  
...  

ABSTRACTRhizobia have a versatile catabolism that allows them to compete successfully with other microorganisms for nutrients in the soil and in the rhizosphere of their respective host plants. In this study,Bradyrhizobium japonicumUSDA 110 was found to be able to utilize oxalate as the sole carbon source. A proteome analysis of cells grown in minimal medium containing arabinose suggested that oxalate oxidation extends the arabinose degradation branch via glycolaldehyde. A mutant of the key pathway genesoxc(for oxalyl-coenzyme A decarboxylase) andfrc(for formyl-coenzyme A transferase) was constructed and shown to be (i) impaired in growth on arabinose and (ii) unable to grow on oxalate. Oxalate was detected in roots and, at elevated levels, in root nodules of four differentB. japonicumhost plants. Mixed-inoculation experiments with wild-type andoxc-frcmutant cells revealed that oxalotrophy might be a beneficial trait ofB. japonicumat some stage during legume root nodule colonization.


mSystems ◽  
2020 ◽  
Vol 5 (1) ◽  
Author(s):  
Carolina A. Contador ◽  
Siu-Kit Lo ◽  
Siu H. J. Chan ◽  
Hon-Ming Lam

ABSTRACT Rhizobia are soil bacteria able to establish symbiosis with diverse host plants. Specifically, Sinorhizobium fredii is a soil bacterium that forms nitrogen-fixing root nodules in diverse legumes, including soybean. The strain S. fredii CCBAU45436 is a dominant sublineage of S. fredii that nodulates soybeans in alkaline-saline soils in the Huang-Huai-Hai Plain region of China. Here, we present a manually curated metabolic model of the symbiotic form of Sinorhizobium fredii CCBAU45436. A symbiosis reaction was defined to describe the specific soybean-microsymbiont association. The performance and quality of the reconstruction had a 70% score when assessed using a standardized genome-scale metabolic model test suite. The model was used to evaluate in silico single-gene knockouts to determine the genes controlling the nitrogen fixation process. One hundred forty-one of 541 genes (26%) were found to influence the symbiotic process, wherein 121 genes were predicted as essential and 20 others as having a partial effect. Transcriptomic profiles of CCBAU45436 were used to evaluate the nitrogen fixation capacity in cultivated versus in wild soybean inoculated with the microsymbiont. The model quantified the nitrogen fixation activities of the strain in these two hosts and predicted a higher nitrogen fixation capacity in cultivated soybean. Our results are consistent with published data demonstrating larger amounts of ureides and total nitrogen in cultivated soybean than in wild soybean. This work presents the first metabolic network reconstruction of S. fredii as an example of a useful tool for exploring the potential benefits of microsymbionts to sustainable agriculture and the ecosystem. IMPORTANCE Nitrogen is the most limiting macronutrient for plant growth, and rhizobia are important bacteria for agriculture because they can fix atmospheric nitrogen and make it available to legumes through the establishment of a symbiotic relationship with their host plants. In this work, we studied the nitrogen fixation process in the microsymbiont Sinorhizobium fredii at the genome level. A metabolic model was built using genome annotation and literature to reconstruct the symbiotic form of S. fredii. Genes controlling the nitrogen fixation process were identified by simulating gene knockouts. Additionally, the nitrogen-fixing capacities of S. fredii CCBAU45436 in symbiosis with cultivated and wild soybeans were evaluated. The predictions suggested an outperformance of S. fredii with cultivated soybean, consistent with published experimental evidence. The reconstruction presented here will help to understand and improve nitrogen fixation capabilities of S. fredii and will be beneficial for agriculture by reducing the reliance on fertilizer applications.


2016 ◽  
Vol 82 (8) ◽  
pp. 2336-2346 ◽  
Author(s):  
Yuan-Chen Zhang ◽  
Wen-Jie Cao ◽  
Le-Rong Zhong ◽  
H. Charles J. Godfray ◽  
Xiang-Dong Liu

ABSTRACTBuchnera aphidicolais an obligate endosymbiont that provides aphids with several essential nutrients. Though much is known about aphid-Buchnerainteractions, the effect of the host plant onBuchnerapopulation size remains unclear. Here we used quantitative PCR (qPCR) techniques to explore the effects of the host plant onBuchneradensities in the cotton-melon aphid,Aphis gossypii.Buchneratiters were significantly higher in populations that had been reared on cucumber for over 10 years than in populations maintained on cotton for a similar length of time. Aphids collected in the wild from hibiscus and zucchini harbored moreBuchnerasymbionts than those collected from cucumber and cotton. The effect of aphid genotype on the population size ofBuchneradepended on the host plant upon which they fed. When aphids from populations maintained on cucumber or cotton were transferred to novel host plants, host survival andBuchnerapopulation size fluctuated markedly for the first two generations before becoming relatively stable in the third and later generations. Host plant extracts from cucumber, pumpkin, zucchini, and cowpea added to artificial diets led to a significant increase inBuchneratiters in the aphids from the population reared on cotton, while plant extracts from cotton and zucchini led to a decrease inBuchneratiters in the aphids reared on cucumber. Gossypol, a secondary metabolite from cotton, suppressedBuchnerapopulations in populations from both cotton and cucumber, while cucurbitacin from cucurbit plants led to higher densities. Together, the results suggest that host plants influenceBuchnerapopulation processes and that this may provide phenotypic plasticity in host plant use for clonal aphids.


Forests ◽  
2019 ◽  
Vol 10 (11) ◽  
pp. 954
Author(s):  
Saiyaremu Halifu ◽  
Xun Deng ◽  
Xiaoshuang Song ◽  
Yuning An ◽  
Ruiqing Song

Pinus sylvestris var. mongolica is an important tree species for ecological construction and environmental restoration owing to its rapid growth rate and excellent stress resistance. Pinus sylvestris var. mongolica sphaeropsis blight is a widespread disease caused by Sphaeropsis sapinea. This study was focused on non-infected (CK) and infected (SS) Pinus sylvestris var. mongolica plants in Zhanggutai area, Liaoning Province, China. Illumina high-throughput sequencing based on the templates of sequencing-by-synthesis working with reversible terminators is a widely used approach. In the present study, systematic differences in relationships among rhizosphere soil physicochemical properties, bacterial community structure, diverse bacterial genera, and alpha diversity indices between the two categories were evaluated. The current findings are as follows: (1) Shannon’s index of SS soil was significantly higher than CK, and it was significantly lower in May than July and September (p < 0.05). (2) Non-metric multidimensional scaling (NMDS) showed a difference in bacterial community structure during May (spring), July (summer), and September. (3) At the phylum level, no significant difference was found in the bacterial genera between CK and SS soil for three seasons; however, at the genus level, there were about 19 different bacterial genera. The correlation studies between 19 different bacterial genera and environmental factors and α-diversity indicated that bacterial genera of non-infected and infected Pinus sylvestris var. mongolica were distributed differently. The bacterial genera with CK were positively correlated with soil physicochemical properties, while a negative correlation was found for SS. In conclusion, the differences in nutrient and microbial community structure in the rhizosphere soil of Pinus sylvestris var. mongolica are the main causes of shoot blight disease.


Nematology ◽  
2020 ◽  
Vol 22 (9) ◽  
pp. 1015-1024
Author(s):  
Qiuling Huang ◽  
Handa Song ◽  
Borong Lin ◽  
Xiaodan Zheng ◽  
Wenjun Wang ◽  
...  

Summary The use of Arabidopsis thaliana as a model plant increased the rate of molecular discoveries of plant-pathogen interactions. Although Meloidogyne graminicola has a relatively broad host range, it is not known whether it can infect A. thaliana. In this study, we showed that M. graminicola is able to invade A. thaliana and complete its life cycle 12-14 days after invasion. No significant difference in the total number of nematodes inside roots of A. thaliana and rice, Oryza sativa, was found at 14 day after inoculation (dai). Significantly more galls were formed in A. thaliana roots compared to the numbers in O. sativa roots at 14 dai. Females laid egg masses on the A. thaliana root surface and a large number of hatched juveniles of the next generation were obtained from infected A. thaliana roots. In addition, the infection of M. graminicola can induce expression of A. thaliana basal defence genes, such as AtMYB51, AtWRKY11, AtPR1 and AtFRK1, at 24 h after inoculation. Therefore, A. thaliana can be considered as a suitable host to study host-M. graminicola interactions and to understand the molecular mechanisms developed by M. graminicola to infect its dicotyledonous host plants. In addition, our results also showed that a delayed development of M. graminicola occurred in A. thaliana compared to O. sativa, and a higher proportion of empty galls appeared in A. thaliana roots than in O. sativa roots, suggesting A. thaliana is a less optimal host than rice.


2021 ◽  
Vol 87 (10) ◽  
Author(s):  
Parris Mayhood ◽  
Babur S. Mirza

ABSTRACT Soybean root nodules are known to contain a high diversity of both rhizobial endophytes and nonrhizobial endophytes (NREs). Nevertheless, the variation of these bacteria among different root nodules within single plants has not been reported. So far, it is unclear whether the selection of NREs among different root nodules within single plants is a random process or is strictly controlled by the host plant to favor a few specific NREs based on their beneficial influence on plant growth. As well, it is also unknown if the relative frequency of NREs within different root nodules is consistent or if it varies based on the location or size of a root nodule. We assessed the microbiomes of 193 individual soybean root nodules from nine plants using high-throughput DNA sequencing. Bradyrhizobium japonicum strains occurred in high abundance in all root nodules despite the presence of other soybean-compatible rhizobia, such as Ensifer, Mesorhizobium, and other species of Bradyrhizobium in soil. Nitrobacter and Tardiphaga were the two nonrhizobial genera that were uniformly detected within almost all root nodules, though they were in low abundance. DNA sequences related to other NREs that have frequently been reported, such as Bacillus, Pseudomonas, Flavobacterium, and Variovorax species, were detected in a few nodules. Unlike for Bradyrhizobium, the low abundance and inconsistent occurrence of previously reported NREs among different root nodules within single plants suggest that these microbes are not preferentially selected as endophytes by host plants and most likely play a limited part in plant growth as endophytes. IMPORTANCE Soybean (Glycine max L.) is a valuable food crop that also contributes significantly to soil nitrogen by developing a symbiotic association with nitrogen-fixing rhizobia. Bacterial endophytes (both rhizobial and nonrhizobial) are considered critical for the growth and resilience of the legume host. In the past, several studies have suggested that the selection of bacterial endophytes within root nodules can be influenced by factors such as soil pH, nutrient availability, host plant genotype, and bacterial diversity in soil. However, the influence of size or location of root nodules on the selection of bacterial endophytes within soybean roots is unknown. It is also unclear whether the selection of nonrhizobial endophytes within different root nodules of a single plant is a random process or is strictly regulated by the host. This information can be useful in identifying potential bacterial species for developing bioinoculants that can enhance plant growth and soil nitrogen.


2019 ◽  
Author(s):  
Hesham A.Y. Gibriel ◽  
Jinling Li ◽  
Longfu Zhu ◽  
Michael F. Seidl ◽  
Bart P.H.J. Thomma

Originality and significance statementDuring host colonization, plant pathogens secrete molecules that enable host colonization, also known as effector proteins. Here, we show that strains of the fungal plant pathogen Verticillium dahliae that are able to infect the same host plant harbour highly divergent LS effector repertoires. Our study outlines the variability within LS effector gene repertoires of V. dahliae strains, which may allow the various strains to be competitive in the co-evolution with their hosts.SummaryEffectors are proteins secreted by pathogens to support colonization of host plants, often by deregulating host immunity. Effector genes are often localized within dynamic lineage-specific (LS) genomic regions, allowing rapid evolution of effector catalogues. Such localization permits pathogens to be competitive in the co-evolutionary arms races with their hosts. For a broad host-range pathogen such as Verticillium dahliae it is unclear to what extent single members of their total effector repertoires contribute to disease development on multiple hosts. Here, we determined the core and LS effector repertoires of a collection of V. dahliae strains, as well as the ability of these strains to infect a range of plant species comprising tomato, cotton, Nicotiana benthamiana, Arabidopsis, and sunflower to assess whether the presence of particular LS effectors correlates with the ability to infect particular plant species. Surprisingly, we found that V. dahliae strains that are able to infect the same host plant harbor highly divergent LS effector repertoires. Furthermore, we observed differential V. dahliae core effector gene expression between host plants. Our data suggest that different V. dahliae lineages utilise divergent effector catalogs to colonize the same host plant, suggesting considerable redundancy among the activities of effector catalogs between lineages.


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