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Fungal community composition and richness of seeds of sessile oak collected in the canopy and on the ground. (a) PCoA plot of compositional dissimilarities among fungal communities associated with seeds, canopy (leaves and twigs) and ground materials (litter and upper soil). Dissimilarities among samples were estimated using binary Jaccard distance. Fungal community composition differed significantly among the four sample types (PERMANOVA on Jaccard qualitative index; F = 4.8, P < 0.001; PERMANOVA on Jaccard quantitative index; F = 4.3, P < 0.001). (b) Richness (log‐transformed) of seed fungal communities, defined as the number of amplicon sequence variants (ASVs) per sample. The lower and upper edges of each box correspond to the 25th and 75th percentiles, respectively, while the whiskers correspond to the 10th and 90th percentiles. Dots indicate outliers. A horizontal line indicates the median value. Richness was significantly higher (*) in seeds on the ground according to GLM results (Table 3).
Source publication
The tree seed mycobiome has received little attention despite its potential role in forest regeneration and health. The aim of the present study was to analyze the processes shaping the composition of seed fungal communities in natural forests as seeds transition from the mother plant to the ground for establishment.
We used metabarcoding approache...
Citations
... The host genetics of parental lines may play a crucial role in determining the seed phenotype, affecting features such as seed anatomy, immune response, and chemical composition. These characteristics, in turn, can influence the assembly of the seed microbiome (12,13). In addition to plant genotype, several environmental factors such as climatic conditions and soil characteristics can affect seed endophytic microbiomes (14). ...
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.
... Recently, a meta-analysis conducted by Simonin and colleagues [4] has stressed the fact that most of the available studies exploring and unveiling the seed microbiome have been focused on herbaceous plants. In contrast, and despite their economic, social and ecological relevance in a range of agroforestry ecosystems, the seed microbiome of woody plants has been poorly investigated [22][23][24][25]. In the case of the olive tree, there is currently no data available related to its seed microbiome [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.
... Although Gnomoniopsis paraclavulata (En61-1) was isolated from grapevine leaves, this species is best known from Quercus spp. in the US and Europe, where it is found in the stems, wood, asymptomatic leaves, overwintering leaves, leaf litter, and acorns [56,[102][103][104]. The most dominant species isolated from asymptomatic and diseased stems of Quercus robur in Poland included G. paraclavulata (and, incidentally, D. eres and C. fioriniae) [62,105]. ...
... Therefore, the senescent and overwintered leaves and wood of both grapevines and other distantly related plant hosts may serve as inoculum for new infections. Vertical transmission of endophytes is also possible in some cases; for example, as demonstrated or suggested in Diaporthe, Ramularia, and G. paraclavulata [103,146,147]. ...
Plant diseases and pests reduce crop yields, accounting for global crop losses of 30% to 50%. In conventional agricultural production systems, these losses are typically controlled by applying chemical pesticides. However, public pressure is mounting to curtail agrochemical use. In this context, employing beneficial endophytic microorganisms is an increasingly attractive alternative to the use of conventional chemical pesticides in agriculture. A multitude of fungal endophytes are naturally present in plants, producing enzymes, small peptides, and secondary metabolites due to their bioactivity, which can protect hosts from pathogens, pests, and abiotic stresses. The use of beneficial endophytic microorganisms in agriculture is an increasingly attractive alternative to conventional pesticides. The aim of this study was to characterize fungal endophytes isolated from apparently healthy, feral wine grapes in eastern Canada that have grown without agrochemical inputs for decades. Host plants ranged from unknown seedlings to long-lost cultivars not widely propagated since the 1800s. HPLC-MS was used to identify unique endophyte-derived chemical compounds in the host plants, while dual-culture competition assays showed a range in endophytes’ ability to suppress the mycelial growth of Botrytis, which is typically controlled in viticulture with pesticides. Twelve of the most promising fungal endophytes isolated were identified using multilocus sequencing and morphology, while DNA barcoding was employed to identify some of their host vines. These fungal endophyte isolates, which consisted of both known and putative novel strains, belonged to seven genera in six families and five orders of Ascomycota. Exploring the fungal endophytes in these specimens may yield clues to the vines’ survival and lead to the discovery of novel biocontrol agents.
... Plants interact with a community of symbiotic microorganisms, known as the microbiome, which can influence germination, establishment, and adaptation of species in the ecosystem (Hassani et al. 2018;Fuentes et al. 2020). Interactions with microorganisms occur in all plant organs, including the surface of aboveground biomass (phyllosphere), the soil affected by root metabolism (rhizosphere), and the internal tissues of roots and aerial organs (plant endosphere) (Leveau 2019;Qu et al. 2020;Compant et al. 2021). Recent evidence has shown that endophytic microorganisms can be useful in promoting plant growth and tolerance to abiotic and biotic stresses in land plants Tran et al. 2022). ...
... Even exposure of seeds to soilborne fungi appears to affect the diversity of seed-associated microorganisms (Zalamea et al. 2021). These studies show that external factors, including environmental conditions, microbial diversity within the plant rhizosphere, and specific biotic interactions, can collectively shape the microbial diversity transferred to tree seeds (Fort et al. 2021;Bastías et al., 2022). These mechanisms provide valuable insights to explain the differences observed in seed-associated endophytes among N. obliqua trees growing within the sampling area. ...
Symbiotic microorganisms are essential for promoting plant growth and establishment from the early stages of plant development. However, the diversity of seed-associated endophytes in native Andean trees and their role in growth promotion and seedling establishment have scarcely been studied. This study aimed to characterize the microbial diversity associated with seeds of Nothofagus obliqua (Mirb.) Oerst. Viable seeds were collected from healthy young trees in a section of the Nahuelbuta Mountains, south-central Chile. Then, they were processed to characterize total microbial diversity using a 16S rRNA gene and an internal transcribed spacer (ITS) region metabarcoding approach. The diversity of culturable bacteria was determined and tested for plant growth-promoting effects. Effects on seed germination, seedling development, and plantlet establishment were evaluated by in vivo inoculations. Seed-associated microbial diversity was dominated by Ascomycota and Proteobacteria, with Diaphorte and Pantoea being the most abundant genera. Five different strains of culturable bacteria were identified, with Rahnella aquatilis being the strain with the most traits that promote plant growth. Bioaugmentation with R. aquatilis improved seed germination, plantlet growth, and establishment of N. obliqua plantlets in the field. Specifically, bioaugmentation with R. aquatilis stimulated height (+ 52%), stem cross-sectional area (+ 89%), stomatal conductance to water vapor (+ 25%), and leaf mass area (+ 29%). These results provide evidence for the beneficial properties of seed-associated bacteria that can support the establishment of native forest tree species in the southern Andes.
... Previous studies suggest that both vertical and horizontal factors contribute to the formation of seed mycobiomes [7,8]. Despite limited research outside of model plant species, a growing body of evidence supports the bene cial nature of certain fruit-associated fungi in which they directly or indirectly bene t diverse physiological processes of the hosts [9,10]. The fact that the seed mycobiome can affect a successive microbial recruitment of seedlings [9] has underlined the need to better understand not only composition but also function of the seed-associated mycobiome. ...
... Despite limited research outside of model plant species, a growing body of evidence supports the bene cial nature of certain fruit-associated fungi in which they directly or indirectly bene t diverse physiological processes of the hosts [9,10]. The fact that the seed mycobiome can affect a successive microbial recruitment of seedlings [9] has underlined the need to better understand not only composition but also function of the seed-associated mycobiome. ...
Objective
Endophytic mycobiomes are present in all studied plant compartments, including fruits and seeds, but a transmission of the mycobiome between generations is largely unknown. Our objectives were to examine mycobiome transfer via seed wings (samaras) of European ash (Fraxinus excelsior), and to test whether these mycobiomes differ among trees. To achieve this, we used ITS1-based amplicon sequencing and two genotypes of F. excelsior as a model to compare the mycobiome of mother trees and their samaras.
Results
We profiled the mycobiome of 57 seed stalks and seed wings (samaras) collected from two genotypes of F. excelsior using three ramets of each genotype. Alpha diversity indices (Observed OTUs and ACE) suggested a higher richness of the mycobiome associated with seed wing than seed stalk within each genotype. However, there was neither significant differences in diversity between the mycobiomes from the two tissue types nor the two genotypes. PERMANOVA analysis revealed significant differences in the mycobiome composition between seed wings, but not between seed stalks, of the two genotypes. Our results suggest that Fraxinus excelsior mother trees disperse different sets of mycobiomes with their samaras, which may be important for germination and seedling establishment – especially in the light of ash dieback.
... All plant species carry FECs, which may include hundreds and even thousands of fungal variants (31)(32)(33)(34). Certain groups in the FEC, such as mycorrhizae and endophytic Epichloë and Serendipita species, form mutualistic relationships that benefit their hosts. ...
The native microbiome in a given plant must be considered when evaluating the effect of a single taxon or synthetic community. The pre-existing microbiome can interact with artificially added microbial cargo, which affects the final outcome. Such issues can be at least partially solved by the use of endophyte-free plants, which provide a clean background that should be useful in determining the effect of a single taxon, taxa combinations, or the entire microbiome on plant performance. Previous reports regarded plants as endophyte-free or axenic by the lack of fungal growth on culture media or the generation of plants from tissue cultures. We showed here that while fungi could not be isolated from fungicide-treated or tissue culture-regenerated plants, nevertheless, all plants contained rich fungal endophyte communities; namely, it was impossible to create fungi-free wheat plants. Our results call for rethinking fundamental microbiome-related concepts, such as core taxa, transmission mode, and functional species.
... In the lifecycle of plants, the seed plays a crucial role by linking one generation to the next. 1,2 Seeds also provide an exclusive microhabitat for microorganisms. 3,4 Unlike microorganisms in other microhabitats of plants, seed endophytes can be vertically transmitted to offspring seeds and may evolve with the host plants. ...
Though the evidence for antibiotic resistance spread via plant microbiome is mounting, studies regarding antibiotic resistome in the plant seed, a reproductive organ and important food resource, are still in their infancy. This study investigated the effects of long-term organic fertilization on seed bacterial endophytes, resistome, and their intergenerational transfer in the microcosm. A total of 99 antibiotic resistance genes (ARGs) and 26 mobile genetic elements (MGEs) were detected by high-throughput quantitative PCR. The amount of organic fertilizer applied was positively correlated to the number and relative abundance of seed-associated ARGs and MGEs. Moreover, the transmission of ARGs from the rhizosphere to the seed was mainly mediated by the shared bacteria and MGEs. Notably, the rhizosphere of progeny seedlings derived from seeds harboring abundant ARGs was found to have a higher relative abundance of ARGs. Using structural equation models, we further revealed that seed resistome and MGEs were key factors affecting the ARGs in the progeny rhizosphere, implying the seed was a potential resistome reservoir for rhizosphere soil. This study highlights the overlooked role of seed endophytes in the dissemination of resistome in the soil-plant continuum, and more attention should be paid to plant seeds as vectors of ARGs within the “One-Health” framework.
... However, it is notable that Kernaghan, Mayerhofer and Griffin [16] did not report any Diaporthe endophytes in wild and hybrid Vitis leaves sampled from wild grapes and vineyards in eastern Canada. Although pathogenicity experiments were not conducted in this study, the virulence of En20-4 and En01-1 should be assessed in the future, especially considering the identification of the phytotoxin nectriapyrone in Although Gnomoniopsis paraclavulata (En61-1) was isolated from grapevine leaves, this species is best known from Quercus spp. in the US and Europe, where it is found in the stems, wood, asymptomatic leaves, overwintering leaves, leaf litter, and acorns [55][56][57][58]. The most dominant species isolated from asymptomatic and diseased stems of Quercus robur in Poland included G. paraclavulata (and, incidentally, D. eres and C. fioriniae) [59,60]. ...
... Therefore, the senescent and overwintered leaves and wood of both grapevine and other distantly related plant hosts may serve as inoculum for new infections. Vertical transmission of endophytes is also possible in some cases, for example, as demonstrated or suggested in Diaporthe, Ramularia, and G. paraclavulata [57,108,109]. ...
Plant diseases and pests reduce crop yields, accounting for global crop losses of 30% to 50%. In conventional agricultural production systems, these losses are typically controlled by applying chemical pesticides. However, public pressure is mounting to curtail agrochemical use. In this context, employing beneficial endophytic microorganisms is an increasingly attractive alternative to the use of conventional chemical pesticides in agriculture. A multitude of fungal endophytes are naturally present in plants, producing enzymes, small peptides and secondary metabolites due to their bioactivity, can protect hosts from pathogens, pests and abiotic stresses. The use of beneficial endophytic microorganisms in agriculture is an increasingly attractive alternative to conventional pesticides. The aim of this study was to characterize fungal endophytes isolated from apparently healthy, feral wine grapes in eastern Canada that have grown without agrochemical inputs for decades. Host plants ranged from unknown seedlings to long-lost cultivars not widely propagated since the 1800s. HPLC-MS was used to identify unique endophyte-derived chemical compounds in the host plants, while dual-culture competition assays showed a range in endophytes’ ability to suppress the mycelial growth of Botrytis, which is typically controlled in viticulture with pesticides. Twelve of the most promising fungal endophytes isolated were identified using multilocus sequencing and morphology, while DNA barcoding was employed to identify some of their host vines. These fungal endophyte isolates, which consisted of both known and putative novel strains, belonged to seven genera in six families and five orders of Ascomycota. Exploring the fungal endophytes in these specimens may yield clues to the vines’ survival and lead to the discovery of novel biocontrol agents.
... 'Maternal effects' can shape seed fungal communities. In particular, the maternal source of a seed explained a larger part of the variation in seed community composition than environment in Quercus petraea (Fort et al. 2021). ...
Context Given the effort and resources that go into collecting and maintaining seed collections, it is crucial that we maximise their usefulness. Conservation, restoration and research rely heavily on good quality collections in order to establish new populations, create habitat, minimise extinction and address scientific questions. Aims Although seed viability, excellent metadata and genetic representativeness make for good quality collections, we provide 10 detailed reasons why the maintenance of separate maternal lines further increases the quality and usefulness of seed collections. Key results Maternal line seed collections can accommodate new information, this is especially important given the increasing longevity of seed collections. For example, maintaining separate maternal lines facilitates accommodation of taxonomic changes, minimises the impact of erroneous plant identifications, and facilitates separation of polyploid races, hybrids and inappropriate lineages. Separate maternal line collections also facilitate better estimates of the genetic diversity captured, and consequently better inform conservation translocations and the establishment of conservation gardens and seed orchards. Separate maternal line collections can also expedite breeding for specific traits, such as disease resistance or other selective challenges that impact on biodiversity conservation. New seed microbiome data show how only some maternal lines contain pathogenic fungi, reminding seed collectors and collections managers that contamination can be better contained by keeping each maternal line separate. Conclusions and implications Maintaining separate maternal lines is a simple and effective way to increase the value of seed collections for multiple applications.
... Phyllosphere microbiome assembly starts during seed germination through microbial inheritance [8,[10][11][12]. During seed germination, a specific set of microorganisms migrate from the seed to the phyllosphere [10]. ...
Background:
The effect of soil on the plant microbiome is well-studied. However, less is known about the impact of the soil microbiome in multitrophic systems. Here we examined the effect of soil on plant and aphid microbiomes, and the reciprocal effect of aphid herbivory on the plant and soil microbiomes. We designed microcosms, which separate below and aboveground compartments, to grow oak seedlings with and without aphid herbivory in soils with three different microbiomes. We used amplicon sequencing and qPCR to characterize the bacterial and fungal communities in soils, phyllospheres, and aphids.
Results:
Soil microbiomes significantly affected the microbial communities of phyllospheres and, to a lesser extent, aphid microbiomes, indicating plant-mediated assembly processes from soil to aphids. While aphid herbivory significantly decreased microbial diversity in phyllospheres independent of soil microbiomes, the effect of aphid herbivory on the community composition in soil varied among the three soils.
Conclusions:
This study provides experimental evidence for the reciprocal influence of soil, plant, and aphid microbiomes, with the potential for the development of new microbiome-based pest management strategies.
