Engineering plant microbiomes by integrating eco-evolutionary principles into current strategies.

Engineering plant microbiomes has the potential to improve plant health in a rapid and sustainable way. Rapidly changing climates and relatively long timelines for plant breeding make microbiome engineering an appealing approach to improving food security. However, approaches that have shown promise in the lab have not resulted in wide-scale implementation in the field. Here, we suggest the use of an integrated approach, combining mechanistic molecular and genetic knowledge, with ecological and evolutionary theory, to target knowledge gaps in plant microbiome engineering that may facilitate translatability of approaches into the field. We highlight examples where understanding microbial community ecology is essential for a holistic understanding of the efficacy and consequences of microbiome engineering. We also review examples where understanding plant-microbe evolution could facilitate the design of plants able to recruit specific microbial communities. Finally, we discuss possible trade-offs in plant-microbiome interactions that should be considered during microbiome engineering efforts so as not to introduce off-target negative effects. We include classic and emergent approaches, ranging from microbial inoculants to plant breeding to host-driven microbiome engineering, and address areas that would benefit from multidisciplinary approaches.

Assembly and potential transmission of the Lens culinaris seed microbiome.

Soil is an important source of bacteria and fungi for the plant, but seeds can also provide microbial inocula through heritable or stochastic assembly. Seed-associated microbial communities can potentially interact with the host plant through multiple generations. Here, we assessed the impact of two different soil types on the seed microbiome assembly of seven lentil (Lens culinaris) genotypes under environmentally controlled conditions and examined the vertical transmission of bacterial communities from seed to seed across two generations. Bulk soil microbiomes and seed microbiomes were characterized using high-throughput amplicon sequencing of the bacterial 16S rRNA gene. Our results revealed that bacterial communities in the two soils differed significantly and that bacterial communities associated with seeds were significantly impacted by genotype (15%) in one of the soils. Co-occurrence of amplicon sequence variants between generations suggests that members of the genera Cutibacterium, Methylobacterium, Sphingomonas, Streptococcus and Tepidimonas are transmitted and preserved in lentil genotypes irrespective of the soil in which they were grown. Increasing our knowledge of how microbial communities carried by seeds are assembled, transmitted and preserved offers a promising way for future breeding programs to consider microbial communities when selecting for more resilient and productive cultivars.

Crop, genotype, and field environmental conditions shape bacterial and fungal seed epiphytic microbiomes.

Seeds are reproductive structures able to carry and transfer microorganisms that play an important role in plant fitness. Genetic and external factors are reported to be partly responsible for the plant microbiome assemblage, but their contribution in seeds is poorly understood. In this study, wheat, canola, and lentil seeds were analyzed to characterize diversity, structure, and persistence of seed-associated microbial communities. Five lines and 2 generations of each crop were subjected to high-throughput amplicon sequencing of the 16S rRNA and internal transcribed spacer (ITS) regions. Bacterial and fungal communities differed most by crop type (30% and 47% of the variance), while generation explained an additional 10% and 15% of the variance. The offspring (i.e., generation harvested in 2016 at the same location) exhibited a higher number of common amplicon sequence variants (ASVs) and less variability in microbial composition. Additionally, in every sample analyzed, a "core microbiome" was detected consisting of 5 bacterial and 12 fungal ASVs. Our results suggest that crop, genotype, and field environmental conditions contributed to the seed-associated microbial assemblage. These findings not only expand our understanding of the factors influencing the seed microbiome but may also help us to manipulate and exploit the microbiota naturally carried by seeds.