Seed microbiota revealed by a large-scale meta-analysis including 50 plant species

Seed microbiota revealed by a large-scale meta-analysis including 50 plant species June 8, 2021

Seed microbiota revealed by a large-scale meta-analysis including 50 plant species​

Authors: Marie Simonin, Martial Briand, Guillaume Chesneau, Aude Rochefort, Coralie Marais, Alain Sarniguet, Matthieu Barret

doi: https://doi.org/10.1101/2021.06.08.447541

ABSTRACT​

Seed microbiota constitutes a primary inoculum for plants that is gaining attention due to its role for plant health and productivity. Here, we performed a meta-analysis on 63 seed microbiota studies covering 50 plant species to synthesize knowledge on the diversity of this habitat. Seed microbiota are diverse and extremely variable, with taxa richness varying from one to thousands of taxa. Hence, seed microbiota presents a variable (i.e flexible) microbial fraction but we also identified a stable (i.e. core) fraction across samples. Around 30 bacterial and fungal taxa are present in most plant species and in samples from all over the world. Core taxa, such as Pantoea agglomerans, Pseudomonas viridiflava, P. fluorescens, Cladosporium perangustum and Alternaria sp., are dominant seed taxa. The characterization of the core and flexible seed microbiota provided here will help uncover seed microbiota roles for plant health and design effective microbiome engineering.

INTRODUCTION​

Seeds are key components of plant fitness and are central to the sustainability of the agri-food system. Seed consumption is the foundation of human food security with wheat, rice and maize seeds providing 42.5 % of the world’s food calorie supply1. Moreover, the transition of seed to seedling represents a major bottleneck for both plant fitness and seed microbiota with large implications in agricultural systems and for the maintenance of plant biodiversity in natural ecosystems24. Both seed quality for food consumption and seed vigour in agricultural settings can be influenced by the microorganisms living inside and on the surface of seeds (i.e. the seed microbiota)5,6. Knowledge regarding seed microbiota has been long lagging behind that of other plant compartments, like the rhizosphere, phyllosphere and endosphere7. However, recently a renewed attention to reproductive tissues (seeds, flowers) and plant early life stages have emerged to better understand the dynamic and assembly processes of plant microbiota 810.
Seed microbiota constitutes a primary microbial inoculum for the plant microbiota with potential long-term impacts on plant fitness. Seed-associated microorganisms can be acquired either horizontally from various environments (e.g. air, water, insects, seed processing) or vertically from the mother plant and transmitted across multiple generations 1113. The prevalence of pathogens on seeds has been extensively studied but the occurrence and role of other commensal or mutualistic microorganisms constituting the majority of seed microbiota are mostly unknown 1416. Currently, limited attempts have been made to characterize the seed core microbiota of a specific plant species or shared across multiple plant species at a large scale 17,18. Here, the definition of the core microbiota used, corresponds to the “common core” (sensu Risely 202019) that represents the component of the microbiota that is found across a considerable proportion of hosts. The identification of the core and flexible microbiota of a plant habitat can help identify microbial taxa and functions that may be particularly important for host fitness20. This identification can be achieved by large-scale data synthesis efforts (e.g. meta-analysis) but such efforts remain to be done for seed microbiota.
A global analysis of seed microbial diversity appears even more timely as seeds appear as a key vector of solutions to promote sustainable agriculture. Seeds can play a double role: i) as a source of innovations with seed-borne microorganisms representing key biotechnological resources21; and ii) as carriers of microbial biostimulants or biocontrol solutions that greatly reduces the surface and volume of treatment applied to fields, thus decreasing application costs and potential negative impacts on the environment 2224. A synthesized knowledge on seed microbiota will accelerate discoveries and will help future practices promoting the presence of important seed microorganisms for plant health and productivity.
In this context, we performed a meta-analysis on available seed microbiota studies to synthesize the current knowledge on the diversity of this habitat and to constitute an open database for the research community. This data synthesis effort enabled us to address the following questions:
  1. How diverse is the seed microbiota?
  2. Which taxonomic groups compose the seed microbiota?
  3. Can we find the evidence for a seed core microbiota shared across plant species?
  4. Do we detect specific patterns in seed microbiota composition and diversity by plant species?
These questions were addressed through a meta-analysis gathering a total of 63 seed microbiota studies yielding 3,190 seed samples from 50 plant species collected in 28 countries. This study shows that the overall seed microbiota composition is highly variable from one seed sample to another but most seeds share a core microbiota composed of few dominant bacterial and fungal taxa.

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