Seed-Transmitted Bacteria and Fungi Dominate Juvenile Plant Microbiomes.

David Johnston-Monje,Janneth P Gutiérrez,Luis Augusto Becerra Lopez-Lavalle

doi:10.3389/fmicb.2021.737616

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.

Highlights

Over hundreds of millions of years, angiosperms have coevolved with microbes that helped them acquire nutrients, resist stress, and combat pathogens
After collecting and sieving sand and soil (Figures 1A,B), soaking seeds from many different sources (Figure 1C), germinating seeds were planted in sealed jars with either sterile sand or field soil and left to grow for up to 2 months until they were harvested for DNA extraction
To compare the diversity in different samples using Bray-Curtis dissimilarity, we rarefied the data to 3,500 reads per shoot, 3,000 reads per root, and 6,500 reads per rhizosphere; operational taxonomic units (OTUs) counts were transformed to relative proportions, averaged across repetitions

Summary

Introduction

Over hundreds of millions of years, angiosperms have coevolved with microbes that helped them acquire nutrients, resist stress, and combat pathogens. Agriculture in some parts of the world has for many decades appreciated that other microbes may play important roles in plant growth and productivity; for example in the 1970s, stem-inhabiting bacterial endophytes were discovered in Brazil (principally coordinated by EMBRAPA Agrobiologia scientist Johanna Döbereiner) to be important in the nitrogen economy of graminaceous grasses (Baldani and Baldani, 2005) It was not until the advent of high-throughput sequencing technologies at the beginning of this new millennium, that the immense diversity of plant-associated microbes began to be understood by the broader scientific community, highlighting the potential to discover many new beneficial plant-associated bacteria and fungi. As this exciting frontier of agricultural science continues to unfold, rational microbiome engineering to improve crop resilience and productivity will only become possible if the rules of microbiome function, provenance, transmission, assembly, and inheritance are elucidated (Vandenkoornhuyse et al, 2015; Busby et al, 2017; Arif et al, 2020)

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