Seed-Transmitted Bacteria and Fungi Dominate Juvenile Plant Microbiomes

Abstract

Plant microbiomes play an important role in agricultural productivity, but there is still much to learn about their provenance, diversity, and organization. In order to study the role of vertical transmission in establishing the bacterial and fungal populations of juvenile plants, we used high-throughput sequencing to survey the microbiomes of seeds, spermospheres, rhizospheres, roots, and shoots of the monocot crops maize (B73), rice (Nipponbare), switchgrass (Alamo), Brachiaria decumbens, wheat, sugarcane, barley, and sorghum; the dicot crops tomato (Heinz 1706), coffee (Geisha), common bean (G19833), cassava, soybean, pea, and sunflower; and the model plants Arabidopsis thaliana (Columbia-0) and Brachypodium distachyon (Bd21). Unsterilized seeds were planted in either sterile sand or farm soil inside hermetically sealed jars, and after as much as 60 days of growth, DNA was extracted to allow for amplicon sequence-based profiling of the bacterial and fungal populations that developed. Seeds of most plants were dominated by Proteobacteria and Ascomycetes, with all containing operational taxonomic units (OTUs) belonging to Pantoea and Enterobacter. All spermospheres also contained DNA belonging to Pseudomonas, Bacillus, and Fusarium. Despite having only seeds as a source of inoculum, all plants grown on sterile sand in sealed jars nevertheless developed rhizospheres, endospheres, and phyllospheres dominated by shared Proteobacteria and diverse fungi. Compared to sterile sand-grown seedlings, growth on soil added new microbial diversity to the plant, especially to rhizospheres; however, all 63 seed-transmitted bacterial OTUs were still present, and the most abundant bacteria (Pantoea, Enterobacter, Pseudomonas, Klebsiella, and Massilia) were the same dominant seed-transmitted microbes observed in sterile sand-grown plants. While most plant mycobiome diversity was observed to come from soil, judging by read abundance, the dominant fungi (Fusarium and Alternaria) were also vertically transmitted. Seed-transmitted fungi and bacteria appear to make up the majority of juvenile crop plant microbial populations by abundance, and based on occupancy, there seems to be a pan-angiosperm seed-transmitted core bacterial microbiome. Further study of these seed-transmitted microbes will be important to understand their role in plant growth and health, as well as their fate during the plant life cycle and may lead to innovations for agricultural inoculant development.

Cultivable Endophytic Bacteria in Seeds of Dongxiang Wild Rice and Their Role in Plant-Growth Promotion

“…Apart from Bacillus, the Actinobacterial Microbacterium and Curtobacterium were the prevalent genera (Table 2), as also reported for mature seeds of rice varieties cultivated in the Philippines and Japan [51,52]. The core microbiome of Bacillus and Microbacterium from seeds is consistent with our previous results from Dongxiang wild rice [35], and is supported by the recent finding that most seed transmitted bacteria are part of a core plant microbiome [17]. Some seed-borne pathogenic endophytes, such as Burkholderia spp.…”

“…Previous studies 2 of 15 have reported that seed microbes may originate from the earliest stages of seed development on the parent plant and then are able to establish early in soil grown seedlings [14,15]. Evidence has also indicated that vertical or seed transmission can significantly contribute to the plant microbiome [16,17]. Indeed, endophytic seed microbes have been previously shown to have potential to promote plant growth or control plant diseases [11,18,19].…”

Histochemical Evidence for Nitrogen-Transfer Endosymbiosis in Non-Photosynthetic Cells of Leaves and Inflorescence Bracts of Angiosperms

“…More work is needed to fully resolve the question of where nitrogenous chemicals detected around bacteria are actually fixed. As reported recently [ 38 ], many of these bacteria (including Pantoea , Pseudomonas , and Klebsiella ) appear to be taxonomically similar to a pan-angiosperm seed-transmitted microbiome with an otherwise poorly understood function within the plant. These bacteria are able to become internalized at meristems when leaf cells are forming.…”

“…Ample evidence over the past several decades suggests that all plants internalize microbes into their cells and tissues [ 13 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 ]. The obvious benefits to microbes are nutrients and protection when living inside the plant; plants also benefit from atmospheric nitrogen fixed by endophytic microbes [ 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 ]. The mechanisms for the transfer of fixed nitrogen from bacteria to plant tissues are largely unknown.…”

Bacterial Communities in the Embryo of Maize Landraces: Relation with Susceptibility to Fusarium Ear Rot

“…While it has been held for a long time that healthy plant tissues were sterile, the presence of complex communities of microorganisms inside every plant tissue has been proven [19,20]. These microorganisms, called endophytes, can have beneficial, neutral, or harmful effects on the host.…”