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•Rhizosphere microbial communities are important for plant health.•Specialized metabolites in the rhizosphere influence the microbial communities.•Isoflavones and saponins are major ...specialized metabolites secreted by soybean.•Secretion is regulated developmentally and nutritionally.•Possible links between specialized metabolites and microbial communities are highlighted.
The rhizosphere is the region close to a plant’s roots, where various interactions occur. Recent evidence indicates that plants influence rhizosphere microbial communities by secreting various metabolites and, in turn, the microbes influence the growth and health of the plants. Despite the importance of plant-derived metabolites in the rhizosphere, relatively little is known about their spatiotemporal distribution and dynamics. In addition to being an important crop, soybean (Glycine max) is a good model plant with which to study these rhizosphere interactions, because soybean plants have symbiotic relationships with rhizobia and arbuscular mycorrhizal fungi and secrete various specialized metabolites, such as isoflavones and saponins, into the soil. This review summarizes the characteristics of the soybean rhizosphere from the viewpoint of specialized metabolites and microbes and discusses future research perspectives. In sum, secretion of these metabolites is developmentally and nutritionally regulated and potentially alters the rhizosphere microbial communities.
Plant specialized metabolites (PSMs) are considerably diverse compounds with multifaceted roles in the adaptation of plants to various abiotic and biotic stresses. PSMs are frequently secreted into ...the rhizosphere, a small region around the roots, where they facilitate interactions between plants and soil microorganisms. PSMs shape the host-specific rhizosphere microbial communities that potentially influence plant growth and tolerance to adverse conditions. Plant mutants defective in PSM biosynthesis contribute to reveal the roles of each PSM in plant–microbiota interactions in the rhizosphere. Recently, various approaches have been used to directly supply PSMs to soil by in vitro methods or through addition in pots with plants. This review focuses on the feasibility of the direct PSM application methods to reveal rhizospheric plant–microbiota interactions and discusses the possibility of applying the knowledge gained to future engineering of rhizospheric traits.
Highly diverse communities of bacteria inhabiting soybean rhizospheres play pivotal roles in plant growth and crop production; however, little is known about the changes that occur in these ...communities during growth. We used both culture-dependent physiological profiling and culture independent DNA-based approaches to characterize the bacterial communities of the soybean rhizosphere during growth in the field. The physiological properties of the bacterial communities were analyzed by a community-level substrate utilization assay with BioLog Eco plates, and the composition of the communities was assessed by gene pyrosequencing. Higher metabolic capabilities were found in rhizosphere soil than in bulk soil during all stages of the BioLog assay. Pyrosequencing analysis revealed that differences between the bacterial communities of rhizosphere and bulk soils at the phylum level; i.e., Proteobacteria were increased, while Acidobacteria and Firmicutes were decreased in rhizosphere soil during growth. Analysis of operational taxonomic units showed that the bacterial communities of the rhizosphere changed significantly during growth, with a higher abundance of potential plant growth promoting rhizobacteria, including Bacillus, Bradyrhizobium, and Rhizobium, in a stage-specific manner. These findings demonstrated that rhizosphere bacterial communities were changed during soybean growth in the field.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Plants interact with microorganisms in the phyllosphere and rhizosphere. Here the roots exude plant specialized metabolites (PSMs) that have diverse biological and ecological functions. Recent ...reports have shown that these PSMs influence the rhizosphere microbiome, which is essential for the plant's growth and health. This review summarizes several specialized metabolites secreted into the rhizosphere of the tomato plant (Solanum lycopersicum), which is an important model species for plant research and a commercial crop. In this review, we focused on the effects of such plant metabolites on plant-microbe interactions. We also reviewed recent studies on improving the growth of tomatoes by analyzing and reconstructing the rhizosphere microbiome and discussed the challenges to be addressed in establishing sustainable agriculture.
Abstract
Root exudates are plant metabolites secreted from the roots into the soil. These exudates are involved in many important biological processes, including acquisition of nutrients, defense and ...signaling to rhizosphere bacteria, such as isoflavones of soybean crucial for the symbiosis with rhizobium. Less is known, however, about other types of root exudates. This study shows that soybean roots secrete large amounts of soyasaponins (triterpenoid glycosides) as root exudates. The soyasaponins are classified into four groups, with group A being the most secreted of these compounds, whereas DDMP (2,3-dihydro-2,5-dihydroxy-6-methyl-4H-pyran-4-one) soyasaponins is the group showing greatest accumulation in root tissues, suggesting a selection system for secreted compounds. Time-course experiments showed that the soyasaponin secretion peaked during early vegetative stages. In particular, soyasaponin Ah was the major compound secreted by soybean roots, whereas the deacetylated derivative Af was the major compound secreted specifically during the VE stage. The secretion of soyasaponins containing glycosyl moieties is an apparent loss of photosynthates. This phenomenon has been also observed in other legume species, although the composition of secreted soyasaponins is plant species dependent. The identification of triterpenoid saponins as major metabolites in legume root exudates will provide novel insights into chemical signaling in the rhizosphere between plants and other organisms.
Plant roots constantly secrete compounds into the soil to interact with neighboring organisms presumably to gain certain functional advantages at different stages of development. Accordingly, it has ...been hypothesized that the phytochemical composition present in the root exudates changes over the course of the lifespan of a plant. Here, root exudates of in vitro grown Arabidopsis plants were collected at different developmental stages and analyzed using GC-MS. Principle component analysis revealed that the composition of root exudates varied at each developmental stage. Cumulative secretion levels of sugars and sugar alcohols were higher in early time points and decreased through development. In contrast, the cumulative secretion levels of amino acids and phenolics increased over time. The expression in roots of genes involved in biosynthesis and transportation of compounds represented in the root exudates were consistent with patterns of root exudation. Correlation analyses were performed of the in vitro root exudation patterns with the functional capacity of the rhizosphere microbiome to metabolize these compounds at different developmental stages of Arabidopsis grown in natural soils. Pyrosequencing of rhizosphere mRNA revealed strong correlations (p<0.05) between microbial functional genes involved in the metabolism of carbohydrates, amino acids and secondary metabolites with the corresponding compounds released by the roots at particular stages of plant development. In summary, our results suggest that the root exudation process of phytochemicals follows a developmental pattern that is genetically programmed.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Saponins are the group of plant specialized metabolites which are widely distributed in angiosperm plants and have various biological activities. The present study focused on α-tomatine, a major ...saponin present in tissues of tomato (Solanum lycopersicum) plants. α-Tomatine is responsible for defense against plant pathogens and herbivores, but its biological function in the rhizosphere remains unknown. Secretion of tomatine was higher at the early growth than the green-fruit stage in hydroponically grown plants, and the concentration of tomatine in the rhizosphere of field-grown plants was higher than that of the bulk soil at all growth stages. The effects of tomatine and its aglycone tomatidine on the bacterial communities in the soil were evaluated in vitro, revealing that both compounds influenced the microbiome in a concentration-dependent manner. Numerous bacterial families were influenced in tomatine/tomatidine-treated soil as well as in the tomato rhizosphere. Sphingomonadaceae species, which are commonly observed and enriched in tomato rhizospheres in the fields, were also enriched in tomatine- and tomatidine-treated soils. Moreover, a jasmonate-responsive ETHYLENE RESPONSE FACTOR 4 mutant associated with low tomatine production caused the root-associated bacterial communities to change with a reduced abundance of Sphingomonadaceae. Taken together, our results highlight the role of tomatine in shaping the bacterial communities of the rhizosphere and suggest additional functions of tomatine in belowground biological communication.
Isoflavones play important roles in rhizosphere plant-microbe interactions. Daidzein and genistein secreted by soybean roots induce the symbiotic interaction with rhizobia and may modulate ...rhizosphere interactions with microbes. Yet despite their important roles, little is known about the biosynthesis, secretion and fate of isoflavones in field-grown soybeans. Here, we analyzed isoflavone contents and the expression of isoflavone biosynthesis genes in field-grown soybeans. In roots, isoflavone contents and composition did not change with crop growth, but the expression of UGT4, an isoflavone-specific 7-O-glucosyltransferase, and of ICHG (isoflavone conjugates hydrolyzing beta-glucosidase) was decreased during the reproductive stages. Isoflavone contents were higher in rhizosphere soil than in bulk soil during both vegetative and reproductive stages, and were comparable in the rhizosphere soil between these two stages. We analyzed the degradation dynamics of daidzein and its glucosides to develop a model for predicting rhizosphere isoflavone contents from the amount of isoflavones secreted in hydroponic culture. Conjugates of daidzein were degraded much faster than daidzein, with degradation rate constants of 8.51 d-1 for malonyldaidzin and 11.6 d-1 for daidzin, vs. 9.15 × 10-2 d-1 for daidzein. The model suggested that secretion of isoflavones into the rhizosphere is higher during vegetative stages than during reproductive stages in field-grown soybean.
Isoflavones play important roles in plant-microbe interactions in rhizospheres. Soybean roots secrete daidzein and genistein to attract rhizobia. Despite the importance of isoflavones in ...plant-microbe interactions, little is known about the developmental and nutritional regulation of isoflavone secretion from soybean roots. In this study, soybeans were grown in hydroponic culture, and isoflavone contents in tissues, isoflavone secretion from the roots, and the expression of isoflavone conjugates hydrolyzing beta-glucosidase (ICHG) were investigated. Isoflavone contents did not show strong growth-dependent changes, while secretion of daidzein from the roots dramatically changed, with higher secretion during vegetative stages. Coordinately, the expression of ICHG also peaked at vegetative stages. Nitrogen deficiency resulted in 8- and 15-fold increases in secretion of daidzein and genistein, respectively, with no induction of ICHG. Taken together, these results suggest that large amounts of isoflavones were secreted during vegetative stages via the hydrolysis of (malonyl)glucosides with ICHG.
Daidzein secretion from soybean roots is higher at vegetative stages with higher isoflavone conjugates hydrolyzing beta-glucosidase expression.
The plant root-associated environments such as the rhizosphere, rhizoplane, and endosphere are different from the outer soil region (bulk soil). They establish characteristic conditions including ...microbiota, metabolites, and minerals, and they can directly affect plant growth and development. However, comprehensive insights into those characteristic environments, especially the rhizosphere, and molecular mechanisms of their formation are not well understood. In the present study, we investigated the spatiotemporal dynamics of the root-associated environment in actual field conditions by multi-omics analyses (mineral, microbiome, and transcriptome) of soybean plants. Mineral and microbiome analyses demonstrated a characteristic rhizosphere environment in which most of the minerals were highly accumulated and bacterial communities were distinct from those in the bulk soil. Mantel's test and co-abundance network analysis revealed that characteristic community structures and dominant bacterial taxa in the rhizosphere significantly interact with mineral contents in the rhizosphere, but not in the bulk soil. Our field multi-omics analysis suggests a rhizosphere-specific close association between the microbiota and mineral environment.
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