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Observed bacterial (A,B) and fungal (C,D) diversity in samples. Shannon index (alpha diversity) as well as beta diversity obtained by Bray–Curtis distance matrix is shown. Significant differences are indicated by different letters as well as given p-values.
Source publication
Recently, it was shown that long-term plant breeding does not only shape plant characteristics but also impacts plant-associated microbiota substantially. This requires a microbiome-integrative breeding approach, which was not yet shown. Here we investigate this for the Styrian oil pumpkin (Cucurbita pepo L. subsp. pepo var. styriaca Greb.) by anal...
Citations
... In the first step primers 515F-GTGYCAGCMGCCGCGGTAA and 806R-GGACTACNVGGGTWTCTAAT (Walters et al., 2016), with an Illumina adapter overhang nucleotide sequence were used with 515F-adapter: 50-TCGTCGGCAGCGTCAGATGTGTATAAGAGACAG-30 and 806R-adapter: 50-GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAG-30. In order to perform first PCR round the Q5 High-Fidelity DNA Polymerase system (M0491, NEB) was used i.e.: 1× Q5 Reaction Buffer with 2 mM MgCl 2 , 200 mM dNTP mix, 1× Q5 High GC Enhancer (for the roots endophytes samples), 0.25 μM forward or reverse primer, and 0.02 U/ml Q5 High-Fidelity DNA polymerase, and 5 mM mitoPNA blocker (PNA Bio PCR Blockers, 2021), 5 mM plastid PNA blocker (Kusstatscher et al., 2021;Mierzejewska et al., 2022b). The PCR program was preceded by initial denaturation (3 min at 98 • C). ...
... Plants and their associated microbes form functional assemblages of species that are referred to as holobionts (Cordovez et al. 2019;Vandenkoornhuyse et al. 2015). The plant microbiota is mainly assembled from seed and soil microorganisms and forms distinct microbial communities in each plant compartment (Abdelfattah et al. 2022;Berg and Raaijmakers 2018;Kusstatscher et al. 2021). The soil-root interface, also known as the rhizosphere, is a hotspot for plantmicrobe interactions with high microbial abundances and activity due to the high nutrient content (Bakker et al. 2013;Berendsen et al. 2012;de la Fuente Cantó et al. 2020). ...
Aims
Plant-specific microbial diversity reflecting host-microbe coevolution was frequently shown at the structural level but less on the functional scale. We studied the microbiome of three compartments at the soil root interface (root endosphere, rhizosphere, bulk soil) of medicinal plants cultivated under organic management in Egypt. The study aimed to examine the impact of the rhizosphere on microbial community composition and diversity in desert agricultural soil, as well as to identify specific functions associated with the rhizosphere.
Methods
The microbiome community structure, diversity, and microbial functioning were evaluated through the utilization of 16S rRNA gene amplicon and shotgun metagenome sequencing.
Results
We found the typical rhizosphere effect and plant-species-specific enrichment of bacterial diversity. The annual plants Calendula officinalis and Matricaria chamomilla (Asteraceae) were more similar than the perennial Solanum distichum (Solanaceae). Altogether, plant species explained 50.5% of the variation in bacterial community structures in the rhizosphere. Our results indicate a stronger effect of the plant species in terms of modulating bacterial community structures in the rhizosphere than in root endosphere samples. The plant-driven rhizosphere effect could be linked to redundant plant beneficial functions in the microbiome, while enrichment of specific genes related to amino acid ion transport and metabolism, carbohydrate transport and metabolism, defense mechanisms, and secondary metabolites biosynthesis were more specific.
Conclusions
The study explores the microbiome continuum at the soil-root interface of medicinal plant species, revealing significant bacterial community structure shifts and plant specificity. The study provides insights into the essential microbiome components contributing to rhizosphere functionality.
... Thus, although our initial hypothesis about the importance of abiotic treatment in driving seed endophyte microbiome variation was not supported, there was clear evidence that a stable seed microbiome was transmitted in all conditions of our study. As the need for sustainable solutions to maintain or improve agricultural productiv ity increases, plant microbiome management, microbiome engineering, and breeding plants for improved microbiomes will be critical strategies (75)(76)(77). Applying beneficial plant microbiome members via seed treatments or soil inoculation has shown promise in improving plant growth or health (78,79). Our objectives here were to understand how the environmental conditions of the parent plant impact the assembly and transmission of the seed endophyte microbiome. ...
Microbiota that originate in the seed can have consequences for the education of the plant immune system, competitive exclusion of pathogens from the host tissue, and host access to critical nutrients. Our research objective was to investigate the consequences of the environmental conditions of the parent plant for bacterial seed microbiome assembly and transmission across plant generations. Using a fully factorial, three-generational experimental design, we investigated endophytic seed bacterial communities of common bean lines (Phaseolus vulgaris L.) grown in the growth chamber and exposed to either control conditions, drought, or excess nutrients at each generation. We applied 16S rRNA microbiome profiling to the seed endophytes and measured plant health outcomes. We discovered stable transmission of 22 bacterial members, regardless of the parental plant condition. This study shows the maintenance of bacterial members of the plant microbiome across generations, even under environmental stress. Overall, this work provides insights into the ability of plants to safeguard microbiome members, which has implications for crop microbiome management in the face of climate change.
IMPORTANCE
Seed microbiomes initiate plant microbiome assembly and thus have critical implications for the healthy development and performance of crops. However, the consequences of environmental conditions of the parent plant for seed microbiome assembly and transmission are unknown, but this is critical information, given the intensifying stressors that crops face as the climate crisis accelerates. This study provides insights into the maintenance of plant microbiomes across generations, with implications for durable plant microbiome maintenance in agriculture on the changing planet.
... Cucurbitaceae-specific secondary metabolites, such as cucurbitacin, may also have exerted an effect on the recruitment of soil microbes (Kusstatscher et al., 2021). In future studies, targeted quantification of JA, salicylic acid and their conjugates as well as other defence metabolites and expression of defence-related genes in diverse cropping systems will help us to understand the underlying mechanisms of soil-mediated suppression of aphid pests in these systems. ...
Intensive agriculture often comes at the expense of soil health. A shift towards practices that foster soil health will support yield and defences against pests and diseases. Growing crops in monoculture is the standard in modern agriculture, though strip‐cropping, in which different crops are planted in strips, is a promising strategy in the transition towards sustainable agriculture. Increasing crop diversity is hypothesized to positively influence arbuscular mycorrhizal fungi (AMF), thereby enhancing soil health, but the mechanisms by which AMF‐plant symbioses contribute to higher yields and reduced pest populations in strip‐cropping systems remain unclear.
We used a green‐house experiment with potato plants to explore the soil legacy effects of mono‐cropping versus strip‐cropping systems, AMF inoculation and aphid infestation on AMF root colonization, the induction of plant defences (untargeted LCMS‐based metabolomics), aphid population size and potato yield.
We found that potato plants grown in strip‐cropping soil had higher AMF colonization than plants grown in mono‐cropping soil. Potato plants grown in strip‐cropping soil also had higher shoot nitrogen content, increased solamargine levels, and reduced aphid populations. AMF root colonization was only enhanced by the addition of commercial AMF in mono‐cropping soils. Potato plant metabolites were affected by strip‐cropping soil, including jasmonic acid (JA) derivatives. Structural equation models revealed that strip‐cropping soil directly reduced aphid populations and also had a negative direct effect on the JA precursor OPC‐8, and hydroxyJA‐glucosides, indicating complex effects of strip‐cropping soils on JA‐inducible plant defences. Indirect benefits of strip‐cropping soil and AMF inoculation on tuber yield were mediated by their direct positive effects on plant nitrogen content.
Our results emphasize the potential of strip‐cropping to enhance AMF root colonization in the field. We show that soil legacy effects of strip‐cropping alter the plant metabolome in ways that suppress of aphid populations. Strip‐cropping legacy effects are the result of crop diversity, crop neighbour and edge effects resulting from crop management practices. While the mechanisms by which soil from strip‐cropping supresses pest populations still need to be identified, our study underscores the potential for strip‐cropping to enhance pest control and yield via soil mediated processes.
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... Recent studies have highlighted the impact of plant genotypes on microbial community composition in their rhizosphere and phyllosphere, showing distinct differences between inbred lines and their F 1 hybrids [4,5]. For example, research on maize demonstrated significant variations in microbial communities associated with hybrids compared to inbred lines, suggesting that specific traits in hybrid plants potentially impact their microbiome composition [6]. ...
Heterosis, or hybrid vigor, is characterized by the enhanced performance of F1 progeny in terms of yield, biomass, and environmental adaptation compared to their parental lines. Recent studies underscore the significant influence of soil microbes on heterosis, revealing that plant genotypes shape microbial communities which, in turn, have the potential to support plant growth through complex host‐microbe interactions. The deeper insight into microbial roles suggests innovative ways to boost crop performance and sustainability by managing the plant microbiome to further enhance heterosis. image
... It was demonstrated that parent and offspring seeds can reveal different bacterial communities. Consequently, a proposition was made that, akin to mammals, which can pass on beneficial microorganisms to their progeny, plants also transfer selected beneficial bacteria to the next generation [7,69]. The transmission of microorganisms from the mother plant to the offspring and further on to the seedling are critical and complex processes. ...
Background
Seed endophytes have a significant impact on plant health and fitness. They can be inherited and passed on to the next plant generation. However, the impact of breeding on their composition in seeds is less understood. Here, we studied the indigenous seed microbiome of a recently domesticated perennial grain crop (Intermediate wheatgrass, Thinopyrum intermedium L.) that promises great potential for harnessing microorganisms to enhance crop performance by a multiphasic approach, including amplicon and strain libraries, as well as molecular and physiological assays.
Results
Intermediate wheatgrass seeds harvested from four field sites in Europe over three consecutive years were dominated by Proteobacteria (88%), followed by Firmicutes (10%). Pantoea was the most abundant genus and Pantoea agglomerans was identified as the only core taxon present in all samples. While bacterial diversity and species richness were similar across all accessions, the relative abundance varied especially in terms of low abundant and rare taxa. Seeds from four different breeding cycles (TLI C3, C5, C704, C801) showed significant differences in bacterial community composition and abundance. We found a decrease in the relative abundance of the functional genes nirK and nifH as well as a drop in bacterial diversity and richness. This was associated with a loss of amplicon sequence variants (ASVs) in Actinobacteria , Alphaproteobacteria , and Bacilli , which could be partially compensated in offspring seeds, which have been cultivated at a new site. Interestingly, only a subset assigned to potentially beneficial bacteria, e.g. Pantoea, Kosakonia , and Pseudomonas , was transmitted to the next plant generation or shared with offspring seeds.
Conclusion
Overall, this study advances our understanding of the assembly and transmission of endophytic seed microorganisms in perennial intermediate wheatgrass and highlights the importance of considering the plant microbiome in future breeding programs.
... Studies have shown that long-term plant breeding not only shapes plant traits but also has a significant impact on the plant-associated microbiota [3]. This suggests a microbiome-integrated breeding approach [20]. Owing to the association of crop genetics with microbiota-based quantitative traits, host-microbiota interactions can be treated as an external quantitative trait, suggesting the need for strategies to integrate microbiota manipulation into crop selection programs [21]. ...
Vertically transmitted endophytes (VTEs) with multi-host-supporting functions are considered plant-acquired heritable traits, which can be manipulated to develop plants with the stable inheritance of these VTEs, defined here as ‘plant endophytic modification (PEM)’. To translate this hypothetical strategy into agricultural and horticultural practice, a PEM was carried out by introducing an anti-fungal pathogenic bacterium, Bacillus cereus (strain ID: ZX-2), into grapevine cuttings and growing the cuttings into vine plants. Bacterial strain XZ-2 is highly efficient in infecting grapevine cuttings and colonizing the interior of the infected cuttings, various parts of the subsequently established vine plants, and next year’s emerging vine shoots and leaves. Profiling the endophytic microbiota by high-throughput sequencing to the grapevines revealed that the colonization with exogenous ZX-2 slightly affected endophytic diversity, while significantly altering the composition and the predicted phenotypes of endophytic microbiota in ZX-2-modified grapevines (ZX-2mg). Most importantly, leaves (from both first- and second-year grapevines) of ZX-2mg conferred significantly higher (p < 0.001) anti-fungal pathogen abilities and a reduction in naturally occurring lesion area than leaves compared to the control grapevines. For all detected vines, a significant correlation (N = 37, r = 0.418; p < 0.01) between fungal pathogen inhibition rates and B. cereus (ZX-2) isolation rates was observed. In addition, ZX-2mg showed some growth promotion and a delay (15–20 days) in leaf abscission. The work established an alternative strategy to create plant lines with functions of specific VTEs via PEM, confirming the practical value of PEM in future organic farming systems.
... Hybrid maize rhizosphere and leaf microbiota and hybrid rice root microbiota exhibit heterosis as seen in their community diversity and composition when compared with their respective parental lines (22,23). The impact of breeding on microbial communities is more pronounced in seeds compared with other plant compartments (24). Several pioneering studies have indicated that seed endophytic microbiomes in hybrids are distinct from their parental lines across a variety of plants, including Styrian oil pumpkin (24), rice (25), and maize (26). ...
... The impact of breeding on microbial communities is more pronounced in seeds compared with other plant compartments (24). Several pioneering studies have indicated that seed endophytic microbiomes in hybrids are distinct from their parental lines across a variety of plants, including Styrian oil pumpkin (24), rice (25), and maize (26). However, it remains largely unknown whether the observed differences in microbiome composition between hybrids and inbred varieties contribute to plant trait heterosis, such as promoting germination. ...
... Genotype-specific seed microbial communities have been previously studied and identified in several plant species (28)(29)(30). Notably, there are significant differences in the diversity of seed endophytic microbes observed between hybrid and parental lines in rice, maize, and Styrian oil pumpkin (24)(25)(26). In this study, host genotypes accounted for 11.6% and 8.83% of the overall variation in bacterial and fungal microbiome composition, respectively. ...
Seed endophytic microbiomes are shaped by host and environmental factors and play a crucial role in their host growth and health. Studies have demonstrated that host genotype, including hybridization, affects seed microbiomes. Heterosis features are also observed in root-associated microbiomes. It remains unclear, however, whether heterosis exists in seed endophytic microbiomes and whether hybrid microbiota provide noticeable advantages to host plant growth, especially to seed germination. Here, we investigated the structure of seed endophytic bacterial and fungal communities from three hybrid rice varieties and their respective parents using amplicon sequencing targeting 16S rRNA and ITS2 genes. Heterosis was found in diversity and composition of seed endophytic microbiomes in hybrids, which hosted more diverse communities and significantly higher abundances of plant growth-promoting taxa, such as Pseudomonas and Rhizobium genera compared with their parental lines. Co-occurrence network analysis revealed that there are potentially tighter microbial interactions in the hybrid seeds compared with their parent seeds. Finally, inoculation of seed-cultivable endophytes, isolated from hybrids, resulted in a greater promotion of seed germination compared with those isolated from parent lines. These findings suggest that heterosis exists not only in plant traits but also in seed endophytic microbiota, the latter in turn promotes seed germination, which offers valuable guidance for microbiome-assisted rice breeding.
IMPORTANCE
Genetic and physiological changes associated with plant hybridization have been studied for many crop species. Still, little is known about the impact of hybridization on the seed microbiota. In this study, we indicate that hybridization has a significant impact on the endophytic bacterial and fungal communities in rice seeds. The seed endophytic microbiomes of hybrids displayed distinct characteristics from those of their parental lines and exhibited potential heterosis features. Furthermore, the inoculation of seed-cultivable endophytes isolated from hybrids exhibited a greater promotion effect on seed germination compared with those isolated from the parents. Our findings make a valuable contribution to the emerging field of microbiome-assisted plant breeding, highlighting the potential for a targeted approach that aims to achieve not only desired plant traits but also plant-beneficial microbial communities on the seeds.
... This knowledge could serve as the foundation for upcoming studies that delve into potential vertical transmission processes of the olive tree microbiota. Moreover, it will be relevant for the assessment of the impact that the seed microbiota has on germination, for breeding programs [30][31][32][33], and for targeted isolation of microorganisms advantageous for the health, development, adaptation and resilience of the olive holobiont [26]. ...
Background
The complex and co-evolved interplay between plants and their microbiota is crucial for the health and fitness of the plant holobiont. However, the microbiota of the seeds is still relatively unexplored and no studies have been conducted with olive trees so far. In this study, we aimed to characterize the bacterial, fungal and archaeal communities present in seeds of ten olive genotypes growing in the same orchard through amplicon sequencing to test whether the olive genotype is a major driver in shaping the seed microbial community, and to identify the origin of the latter. Therefore, we have developed a methodology for obtaining samples from the olive seed’s endosphere under sterile conditions.
Results
A diverse microbiota was uncovered in olive seeds, the plant genotype being an important factor influencing the structure and composition of the microbial communities. The most abundant bacterial phylum was Actinobacteria , accounting for an average relative abundance of 41%. At genus level, Streptomyces stood out because of its potential influence on community structure. Within the fungal community, Basidiomycota and Ascomycota were the most abundant phyla, including the genera Malassezia , Cladosporium , and Mycosphaerella . The shared microbiome was composed of four bacterial ( Stenotrophomonas , Streptomyces , Promicromonospora and Acidipropionibacterium ) and three fungal ( Malassezia , Cladosporium and Mycosphaerella ) genera. Furthermore, a comparison between findings obtained here and earlier results from the root endosphere of the same trees indicated that genera such as Streptomyces and Malassezia were present in both olive compartments.
Conclusions
This study provides the first insights into the composition of the olive seed microbiota. The highly abundant fungal genus Malassezia and the bacterial genus Streptomyces reflect a unique signature of the olive seed microbiota. The genotype clearly shaped the composition of the seed’s microbial community, although a shared microbiome was found. We identified genera that may translocate from the roots to the seeds, as they were present in both organs of the same trees. These findings set the stage for future research into potential vertical transmission of olive endophytes and the role of specific microbial taxa in seed germination, development, and seedling survival.
... T he y are collecti v el y known as micr obemediated adaptation (Petipas et al. 2021 ). All these processes are suggested to be influenced by plant genotype and the environment, including the extent of anthropogenic impacts on the ecosystem (Menzel et al. 2017, Kusstatscher et al. 2021, Berg and Cernava 2022, Cosme 2023. Plants assemble their rhizosphere microbiome by recruiting bacteria from seeds and the surrounding environment (Abdelfattah et al. 2021, Wicaksono et al. 2022 ). ...
Rhizosphere microbiome assembly is essential for plant health, but the temporal dimension of this process remains unexplored. We used a chronosequence of 150 years of the retreating Hallstätter glacier (Dachstein, Austria) to disentangle this exemplarily for the rhizosphere of three pioneer alpine plants. Time of deglaciation was an important factor shaping the rhizosphere microbiome. Microbiome functions, i.e. nutrient uptake and stress protection, were carried out by ubiquitous and cosmopolitan bacteria. The rhizosphere succession along the chronosequence was characterized by decreasing microbial richness but increasing specificity of the plant-associated bacterial community. Environmental selection is a critical factor in shaping the ecosystem, particularly in terms of plant-driven recruitment from the available edaphic pool. A higher rhizosphere microbial richness during early succession compared to late succession can be explained by the occurrence of cold-acclimated bacteria recruited from the surrounding soils. These taxa might be sensitive to changing habitat conditions that occurred at the later stages. A stronger influence of the plant host on the rhizosphere microbiome assembly was observed with increased time since deglaciation. Overall, this study indicated that well-adapted, ubiquitous microbes potentially support pioneer plants to colonize new ecosystems, while plant-specific microbes may be associated with the long-term establishment of their hosts.
