Specialized microbiomes facilitate natural rhizosphere microbiome interactions counteracting high salinity stress in plants

•Specialized microbiome transfers increased plant growth at higher salinities.•Rice field microbiome is better suited to support plant growth.•Halotolerant microbiome promoted similar network structures between salinities.•Plant growth at high salinities was linked to denser and more complex network...

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Published inEnvironmental and experimental botany Vol. 186; p. 104430
Main Authors Santos, Susana Silva, Rask, Klara Andrés, Vestergård, Mette, Johansen, Jesper Liengaard, Priemé, Anders, Frøslev, Tobias Guldberg, González, Ana M. Martín, He, Huan, Ekelund, Flemming
Format Journal Article
LanguageEnglish
Published Elsevier B.V 01.06.2021
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Abstract •Specialized microbiome transfers increased plant growth at higher salinities.•Rice field microbiome is better suited to support plant growth.•Halotolerant microbiome promoted similar network structures between salinities.•Plant growth at high salinities was linked to denser and more complex networks.•Potential keystone taxa tolerant to salinity were identified. The root microbiota is crucial for plant productivity and stress tolerance. Still, our understanding of the factors that structure these microbial communities is limited, and we lack a theoretical framework to predict their assemblage and interactions. Here, we used rice as a model system to explore the hypothesis that microbiomes from specific environments enhance plant tolerance to salinity. We used 16S rRNA sequencing to track salinity-induced changes in microbiomes of plants inoculated with either a rice field microbiome, or a halotolerant microbiome, compared to only the seed microbiome. We found that, at salinities higher than 1.1 % plant growth was severely impeded. Nevertheless, at 0.11 % and 0.35 % salinity, plants inoculated with rice field and halotolerant microbiomes displayed enhanced shoot and root biomass, when compared to plants surviving only with the seed microbiome. Rice field microbiome had the highest plant growth-promoting effect and was the only treatment that promoted growth at 0.35 % salinity. The salinity effects on bacterial composition and alpha diversity were more pronounced for plants that relied only on the seed microbiome. The root-associated compartments harboured distinct microbiomes, but salinity explained most of the variation observed. Rice plants interacted with the rice field and halotolerant microbiomes to shape rhizosphere microbial community composition and the co-occurrence patterns, supporting plant growth at higher salinity. Assemblages of the halotolerant microbiome promoted similar network structures between the different salinity treatments, when compared to the other inoculations. Moreover, salinity responsive and keystone bacteria were taxonomically diverse and responded in guilds of taxa to the salinity levels. We conclude that both specialized inoculations differ greatly in how they influence the plant microbiome and that plant growth at higher salinity levels was associated with a denser and more complex root microbial community.
AbstractList The root microbiota is crucial for plant productivity and stress tolerance. Still, our understanding of the factors that structure these microbial communities is limited, and we lack a theoretical framework to predict their assemblage and interactions. Here, we used rice as a model system to explore the hypothesis that microbiomes from specific environments enhance plant tolerance to salinity. We used 16S rRNA sequencing to track salinity-induced changes in microbiomes of plants inoculated with either a rice field microbiome, or a halotolerant microbiome, compared to only the seed microbiome. We found that, at salinities higher than 1.1 % plant growth was severely impeded. Nevertheless, at 0.11 % and 0.35 % salinity, plants inoculated with rice field and halotolerant microbiomes displayed enhanced shoot and root biomass, when compared to plants surviving only with the seed microbiome. Rice field microbiome had the highest plant growth-promoting effect and was the only treatment that promoted growth at 0.35 % salinity. The salinity effects on bacterial composition and alpha diversity were more pronounced for plants that relied only on the seed microbiome. The root-associated compartments harboured distinct microbiomes, but salinity explained most of the variation observed. Rice plants interacted with the rice field and halotolerant microbiomes to shape rhizosphere microbial community composition and the co-occurrence patterns, supporting plant growth at higher salinity. Assemblages of the halotolerant microbiome promoted similar network structures between the different salinity treatments, when compared to the other inoculations. Moreover, salinity responsive and keystone bacteria were taxonomically diverse and responded in guilds of taxa to the salinity levels. We conclude that both specialized inoculations differ greatly in how they influence the plant microbiome and that plant growth at higher salinity levels was associated with a denser and more complex root microbial community.
•Specialized microbiome transfers increased plant growth at higher salinities.•Rice field microbiome is better suited to support plant growth.•Halotolerant microbiome promoted similar network structures between salinities.•Plant growth at high salinities was linked to denser and more complex networks.•Potential keystone taxa tolerant to salinity were identified. The root microbiota is crucial for plant productivity and stress tolerance. Still, our understanding of the factors that structure these microbial communities is limited, and we lack a theoretical framework to predict their assemblage and interactions. Here, we used rice as a model system to explore the hypothesis that microbiomes from specific environments enhance plant tolerance to salinity. We used 16S rRNA sequencing to track salinity-induced changes in microbiomes of plants inoculated with either a rice field microbiome, or a halotolerant microbiome, compared to only the seed microbiome. We found that, at salinities higher than 1.1 % plant growth was severely impeded. Nevertheless, at 0.11 % and 0.35 % salinity, plants inoculated with rice field and halotolerant microbiomes displayed enhanced shoot and root biomass, when compared to plants surviving only with the seed microbiome. Rice field microbiome had the highest plant growth-promoting effect and was the only treatment that promoted growth at 0.35 % salinity. The salinity effects on bacterial composition and alpha diversity were more pronounced for plants that relied only on the seed microbiome. The root-associated compartments harboured distinct microbiomes, but salinity explained most of the variation observed. Rice plants interacted with the rice field and halotolerant microbiomes to shape rhizosphere microbial community composition and the co-occurrence patterns, supporting plant growth at higher salinity. Assemblages of the halotolerant microbiome promoted similar network structures between the different salinity treatments, when compared to the other inoculations. Moreover, salinity responsive and keystone bacteria were taxonomically diverse and responded in guilds of taxa to the salinity levels. We conclude that both specialized inoculations differ greatly in how they influence the plant microbiome and that plant growth at higher salinity levels was associated with a denser and more complex root microbial community.
ArticleNumber 104430
Author Santos, Susana Silva
Vestergård, Mette
Rask, Klara Andrés
Ekelund, Flemming
Frøslev, Tobias Guldberg
González, Ana M. Martín
Priemé, Anders
Johansen, Jesper Liengaard
He, Huan
Author_xml – sequence: 1
  givenname: Susana Silva
  orcidid: 0000-0001-7014-4999
  surname: Santos
  fullname: Santos, Susana Silva
  email: suss@agro.au.dk
  organization: Department of Biology, University of Copenhagen, Universitetsparken 15, Copenhagen, Denmark
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  givenname: Klara Andrés
  orcidid: 0000-0003-0872-1083
  surname: Rask
  fullname: Rask, Klara Andrés
  organization: Department of Biology, University of Copenhagen, Universitetsparken 15, Copenhagen, Denmark
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  givenname: Mette
  orcidid: 0000-0002-0054-4855
  surname: Vestergård
  fullname: Vestergård, Mette
  organization: Department of Agroecology, Aarhus University, Forsøgsvej 1, Slagelse, Denmark
– sequence: 4
  givenname: Jesper Liengaard
  orcidid: 0000-0001-7602-316X
  surname: Johansen
  fullname: Johansen, Jesper Liengaard
  organization: Department of Biology, University of Copenhagen, Universitetsparken 15, Copenhagen, Denmark
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  givenname: Anders
  surname: Priemé
  fullname: Priemé, Anders
  organization: Department of Biology, University of Copenhagen, Universitetsparken 15, Copenhagen, Denmark
– sequence: 6
  givenname: Tobias Guldberg
  surname: Frøslev
  fullname: Frøslev, Tobias Guldberg
  organization: Section for Geogenetics, GLOBE Institute, University of Copenhagen, Øster Voldgade 5-7, 1350, Copenhagen, Denmark
– sequence: 7
  givenname: Ana M. Martín
  orcidid: 0000-0001-9429-7180
  surname: González
  fullname: González, Ana M. Martín
  organization: Pacific Ecoinformatics and Computational Ecology Lab, Berkeley, CA, USA
– sequence: 8
  givenname: Huan
  surname: He
  fullname: He, Huan
  organization: Department of Biology, University of Copenhagen, Universitetsparken 15, Copenhagen, Denmark
– sequence: 9
  givenname: Flemming
  surname: Ekelund
  fullname: Ekelund, Flemming
  email: fekelund@bio.ku.dk
  organization: Department of Biology, University of Copenhagen, Universitetsparken 15, Copenhagen, Denmark
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Keywords Seed endophytes
Rhizosphere effects
Microbiome transfer
Rice
Halotolerant crops
16S rRNA gene
Language English
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Snippet •Specialized microbiome transfers increased plant growth at higher salinities.•Rice field microbiome is better suited to support plant growth.•Halotolerant...
The root microbiota is crucial for plant productivity and stress tolerance. Still, our understanding of the factors that structure these microbial communities...
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StartPage 104430
SubjectTerms 16S rRNA gene
biomass
community structure
Halotolerant crops
microbial communities
microbiome
Microbiome transfer
paddies
phytobiome
plant growth
rhizosphere
Rhizosphere effects
Rice
salinity
salt stress
salt tolerance
Seed endophytes
species diversity
stress tolerance
Title Specialized microbiomes facilitate natural rhizosphere microbiome interactions counteracting high salinity stress in plants
URI https://dx.doi.org/10.1016/j.envexpbot.2021.104430
https://www.proquest.com/docview/2540497682
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