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Stochastic Inoculum, Biotic Filtering and Species-Specific Seed Transmission Shape the Rare Microbiome of Plants

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 productivi...

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Autores principales: Johnston-Monje, David, Gutiérrez, Janneth P., Becerra Lopez-Lavalle, Luis Augusto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9506401/
https://www.ncbi.nlm.nih.gov/pubmed/36143410
http://dx.doi.org/10.3390/life12091372
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author Johnston-Monje, David
Gutiérrez, Janneth P.
Becerra Lopez-Lavalle, Luis Augusto
author_facet Johnston-Monje, David
Gutiérrez, Janneth P.
Becerra Lopez-Lavalle, Luis Augusto
author_sort Johnston-Monje, David
collection PubMed
description 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.
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spelling pubmed-95064012022-09-24 Stochastic Inoculum, Biotic Filtering and Species-Specific Seed Transmission Shape the Rare Microbiome of Plants Johnston-Monje, David Gutiérrez, Janneth P. Becerra Lopez-Lavalle, Luis Augusto Life (Basel) Article 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. MDPI 2022-09-02 /pmc/articles/PMC9506401/ /pubmed/36143410 http://dx.doi.org/10.3390/life12091372 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Johnston-Monje, David
Gutiérrez, Janneth P.
Becerra Lopez-Lavalle, Luis Augusto
Stochastic Inoculum, Biotic Filtering and Species-Specific Seed Transmission Shape the Rare Microbiome of Plants
title Stochastic Inoculum, Biotic Filtering and Species-Specific Seed Transmission Shape the Rare Microbiome of Plants
title_full Stochastic Inoculum, Biotic Filtering and Species-Specific Seed Transmission Shape the Rare Microbiome of Plants
title_fullStr Stochastic Inoculum, Biotic Filtering and Species-Specific Seed Transmission Shape the Rare Microbiome of Plants
title_full_unstemmed Stochastic Inoculum, Biotic Filtering and Species-Specific Seed Transmission Shape the Rare Microbiome of Plants
title_short Stochastic Inoculum, Biotic Filtering and Species-Specific Seed Transmission Shape the Rare Microbiome of Plants
title_sort stochastic inoculum, biotic filtering and species-specific seed transmission shape the rare microbiome of plants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9506401/
https://www.ncbi.nlm.nih.gov/pubmed/36143410
http://dx.doi.org/10.3390/life12091372
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