RESUMO
A plant's health and productivity is influenced by its associated microbes. Although the common/core microbiome is often thought to be the most influential, significant numbers of rare or uncommon microbes (e.g., specialized endosymbionts) may also play an important role in the health and productivity of certain plants in certain environments. To help identify rare/specialized bacteria and fungi in the most important angiosperm plants, we contrasted microbiomes of the seeds, spermospheres, shoots, roots and rhizospheres of Arabidopsis, Brachypodium, maize, wheat, sugarcane, rice, tomato, coffee, common bean, cassava, soybean, switchgrass, sunflower, Brachiaria, barley, sorghum and pea. Plants were grown inside sealed jars on sterile sand or farm soil. Seeds and spermospheres contained some uncommon bacteria and many fungi, suggesting at least some of the rare microbiome is vertically transmitted. About 95% and 86% of fungal and bacterial diversity inside plants was uncommon; however, judging by read abundance, uncommon fungal cells are about half of the mycobiome, while uncommon bacterial cells make up less than 11% of the microbiome. Uncommon-seed-transmitted microbiomes consisted mostly of Proteobacteria, Firmicutes, Bacteriodetes, Ascomycetes and Basidiomycetes, which most heavily colonized shoots, to a lesser extent roots, and least of all, rhizospheres. Soil served as a more diverse source of rare microbes than seeds, replacing or excluding the majority of the uncommon-seed-transmitted microbiome. With the rarest microbes, their colonization pattern could either be the result of stringent biotic filtering by most plants, or uneven/stochastic inoculum distribution in seeds or soil. Several strong plant-microbe associations were observed, such as seed transmission to shoots, roots and/or rhizospheres of Sarocladium zeae (maize), Penicillium (pea and Phaseolus), and Curvularia (sugarcane), while robust bacterial colonization from cassava field soil occurred with the cyanobacteria Leptolyngbya into Arabidopsis and Panicum roots, and Streptomyces into cassava roots. Some abundant microbes such as Sakaguchia in rice shoots or Vermispora in Arabidopsis roots appeared in no other samples, suggesting that they were infrequent, stochastically deposited propagules from either soil or seed (impossible to know based on the available data). Future experiments with culturing and cross-inoculation of these microbes between plants may help us better understand host preferences and their role in plant productivity, perhaps leading to their use in crop microbiome engineering and enhancement of agricultural production.
RESUMO
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.