Temporal dynamics of bacterial communities during seed development and maturation

Abstract

Seed microbiota acts as a starting point for the assembly of the plant microbiota and contributes to successful plant establishment. To date, the order and timing of microbial taxa immigration during seed development and maturation remained unknown. We investigated the temporal dynamics of seed bacterial communities in bean and radish. A high phylogenetic turnover was observed for both plant species with few taxa associated with all seed developmental stages. Greater heterogeneity in community structure within each stage was observed for radish. While about one-third of radish seed bacterial taxa were detected in buds, flowers and fruits, very few taxa seem to be transmitted by the floral route in bean. In the latter species, bacterial populations belonging to the P. fluorescens species complex were found either in buds, flowers and fruits or in seeds. The relative phylogenetic proximity of these bacterial populations combined with their habitat specificity led us to explore the genetic determinants involved in successful seed transmission in bean. Comparative genomic analyses of representatives bacterial strains revealed dozens of coding sequences specifically associated with seed-transmitted strains. This study provided a first glimpse on processes involved in seed microbiota assembly, which could be used for designing plant-beneficial microbial consortia.

Endophytic microbiome variation at the level of a single plant seed

“…Because multiple legume seeds within a pod develop as a result of a single flower pollination, one simple hypothesis is that the individual seeds within a pod may harbor a highly similar microbiome if the floral pathway of assembly is prominent. However, recent work has suggested that the endophytic seed microbiome of green bean varieties of common bean likely colonize predominantly via the internal vascular pathway, and not the floral pathway (Chesneau et al 2020), which may result in more homogeneity among seed microbiomes of the same plant. Our data support this finding, as seeds from the same plant (and therefore a common vascular pathway across pods) had relatively low microbiome variability, especially as compared across plants.…”

“…There are many challenges in analyzing the microbiome of seeds generally and of a single seed in particular, which may be why cultivation-independent studies of single seeds are few (Abdelfattah et al 2021). Previous studies showed that seeds have low microbial biomass and diversity (Adam et al 2018; Chesneau et al 2020; Rezki et al 2016), especially relative to other plant compartments or soil. Therefore, many studies pool seeds to analyze the aggregated microbiome of many seeds and to get enough microbial biomass for metagenomic DNA extraction (Latz et al 2021; Bergna et al 2018; Wassermann et al 2019; Adam et al 2018; Johnston-Monje and Raizada 2011; Klaedtke et al 2016).…”

“…Therefore, nucleic acid extractions may attempt minimal disturbance of the plant tissue that is that target of microbiome investigation; for example, grinding tissues to include in the extraction will result in higher plant DNA contamination than separating microbial biomass from intact tissue. For seeds in particular, it is known that seeds can exude both antimicrobials and attractants to select for particular microbial members early in microbiome assembly of the germinated seed and emerging seedling (Chesneau et al 2020; Meldau et al 2012), and there is an active zone of plant and microbiome activity at the seed-soil-interface of a germinating seed (the spermosphere, e.g., Schiltz et al 2015). Therefore, to target the native endophytic seed microbiome without also allowing for the plant’s potential selection for or filtering against particular members, it is important to use dormant seeds and also to minimally disrupt the seed compartment during extraction.…”

Microbial effects on plant phenology and fitness

“…Further, few studies considered flower-inhabiting microbes, which manipulate the attraction of pollinators (Rering et al, 2018;Tsuji and Fukami, 2018;Cellini et al, 2019;Russell and Ashman, 2019). Floral microbes can be mutualistic or pathogenic, and some species can migrate to the vascular bundles, becoming systemic and even passing on to seeds (Piqué et al, 2015;Kim et al, 2019;Chesneau et al, 2020). Thus, they have high potential for downstream consequences on plant traits, such as the timing of floral senescence and fruiting.…”

Quality of Immature and Mature Pepper (Capsicum annuum L.) Seeds in Relation to Bio-Priming with Endophytic Pseudomonas and Bacillus spp.

“…Whereas some studies have focused on the effect of seed microbiota on germination and emergence [43][44][45][46], bacterial communities' influence on seed enhancement possibilities of differentially matured lots is currently unknown [47,48]. Therefore, the aim of the present study was to evaluate the effects of four different endophytic bacteria, Pseudomonas fluorescens strain L5b, Pseudomonas gessardii strain L13, Bacillus subtilis strain Bs1 and Bacillus mojavensis strain ApBm, on immature and mature pepper seeds by the meaning of quality.…”