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Integrated Microbiome and Metabolomic Analysis Reveal Responses of Rhizosphere Bacterial Communities and Root exudate Composition to Drought and Genotype in Rice (Oryza sativa L.)

BACKGROUND: As climate change events become more frequent, drought is an increasing threat to agricultural production and food security. Crop rhizosphere microbiome and root exudates are critical regulators for drought adaptation, yet our understanding on the rhizosphere bacterial communities and ro...

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Autores principales: Li, Gege, Wang, Kexin, Qin, Qun, Li, Qi, Mo, Fei, Nangia, Vinay, Liu, Yang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10090257/
https://www.ncbi.nlm.nih.gov/pubmed/37039929
http://dx.doi.org/10.1186/s12284-023-00636-1
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author Li, Gege
Wang, Kexin
Qin, Qun
Li, Qi
Mo, Fei
Nangia, Vinay
Liu, Yang
author_facet Li, Gege
Wang, Kexin
Qin, Qun
Li, Qi
Mo, Fei
Nangia, Vinay
Liu, Yang
author_sort Li, Gege
collection PubMed
description BACKGROUND: As climate change events become more frequent, drought is an increasing threat to agricultural production and food security. Crop rhizosphere microbiome and root exudates are critical regulators for drought adaptation, yet our understanding on the rhizosphere bacterial communities and root exudate composition as affected by drought stress is far from complete. In this study, we performed 16S rRNA gene amplicon sequencing and widely targeted metabolomic analysis of rhizosphere soil and root exudates from two contrasting rice genotypes (Nipponbare and Luodao 998) exposed to drought stress. RESULTS: A reduction in plant phenotypes was observed under drought, and the inhibition was greater for roots than for shoots. Additionally, drought exerted a negligible effect on the alpha diversity of rhizosphere bacterial communities, but obviously altered their composition. In particular, drought led to a significant enrichment of Actinobacteria but a decrease in Firmicutes. We also found that abscisic acid in root exudates was clearly higher under drought, whereas lower jasmonic acid and L-cystine concentrations. As for plant genotypes, variations in plant traits of the drought-tolerant genotype Luodao 998 after drought were smaller than those of Nipponbare. Interestingly, drought triggered an increase in Bacillus, as well as an upregulation of most organic acids and a downregulation of all amino acids in Luodao 998. Notably, both Procrustes analysis and Mantel test demonstrated that rhizosphere microbiome and root exudate metabolomic profiles were highly correlated. A number of differentially abundant genera responded to drought and genotype, including Streptomyces, Bacillus and some members of Actinobacteria, were significantly associated with organic acid and amino acid contents in root exudates. Further soil incubation experiments showed that Streptomyces was regulated by abscisic acid and jasmonic acid under drought. CONCLUSIONS: Our results reveal that both drought and genotype drive changes in the compositions of rice rhizosphere bacterial communities and root exudates under the greenhouse condition, and that organic acid exudation and suppression of amino acid exudation to select specific rhizosphere bacterial communities may be an important strategy for rice to cope with drought. These findings have important implications for improving the adaptability of rice to drought from the perspective of plant–microbe interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12284-023-00636-1.
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spelling pubmed-100902572023-04-13 Integrated Microbiome and Metabolomic Analysis Reveal Responses of Rhizosphere Bacterial Communities and Root exudate Composition to Drought and Genotype in Rice (Oryza sativa L.) Li, Gege Wang, Kexin Qin, Qun Li, Qi Mo, Fei Nangia, Vinay Liu, Yang Rice (N Y) Research BACKGROUND: As climate change events become more frequent, drought is an increasing threat to agricultural production and food security. Crop rhizosphere microbiome and root exudates are critical regulators for drought adaptation, yet our understanding on the rhizosphere bacterial communities and root exudate composition as affected by drought stress is far from complete. In this study, we performed 16S rRNA gene amplicon sequencing and widely targeted metabolomic analysis of rhizosphere soil and root exudates from two contrasting rice genotypes (Nipponbare and Luodao 998) exposed to drought stress. RESULTS: A reduction in plant phenotypes was observed under drought, and the inhibition was greater for roots than for shoots. Additionally, drought exerted a negligible effect on the alpha diversity of rhizosphere bacterial communities, but obviously altered their composition. In particular, drought led to a significant enrichment of Actinobacteria but a decrease in Firmicutes. We also found that abscisic acid in root exudates was clearly higher under drought, whereas lower jasmonic acid and L-cystine concentrations. As for plant genotypes, variations in plant traits of the drought-tolerant genotype Luodao 998 after drought were smaller than those of Nipponbare. Interestingly, drought triggered an increase in Bacillus, as well as an upregulation of most organic acids and a downregulation of all amino acids in Luodao 998. Notably, both Procrustes analysis and Mantel test demonstrated that rhizosphere microbiome and root exudate metabolomic profiles were highly correlated. A number of differentially abundant genera responded to drought and genotype, including Streptomyces, Bacillus and some members of Actinobacteria, were significantly associated with organic acid and amino acid contents in root exudates. Further soil incubation experiments showed that Streptomyces was regulated by abscisic acid and jasmonic acid under drought. CONCLUSIONS: Our results reveal that both drought and genotype drive changes in the compositions of rice rhizosphere bacterial communities and root exudates under the greenhouse condition, and that organic acid exudation and suppression of amino acid exudation to select specific rhizosphere bacterial communities may be an important strategy for rice to cope with drought. These findings have important implications for improving the adaptability of rice to drought from the perspective of plant–microbe interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12284-023-00636-1. Springer US 2023-04-11 /pmc/articles/PMC10090257/ /pubmed/37039929 http://dx.doi.org/10.1186/s12284-023-00636-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/ Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research
Li, Gege
Wang, Kexin
Qin, Qun
Li, Qi
Mo, Fei
Nangia, Vinay
Liu, Yang
Integrated Microbiome and Metabolomic Analysis Reveal Responses of Rhizosphere Bacterial Communities and Root exudate Composition to Drought and Genotype in Rice (Oryza sativa L.)
title Integrated Microbiome and Metabolomic Analysis Reveal Responses of Rhizosphere Bacterial Communities and Root exudate Composition to Drought and Genotype in Rice (Oryza sativa L.)
title_full Integrated Microbiome and Metabolomic Analysis Reveal Responses of Rhizosphere Bacterial Communities and Root exudate Composition to Drought and Genotype in Rice (Oryza sativa L.)
title_fullStr Integrated Microbiome and Metabolomic Analysis Reveal Responses of Rhizosphere Bacterial Communities and Root exudate Composition to Drought and Genotype in Rice (Oryza sativa L.)
title_full_unstemmed Integrated Microbiome and Metabolomic Analysis Reveal Responses of Rhizosphere Bacterial Communities and Root exudate Composition to Drought and Genotype in Rice (Oryza sativa L.)
title_short Integrated Microbiome and Metabolomic Analysis Reveal Responses of Rhizosphere Bacterial Communities and Root exudate Composition to Drought and Genotype in Rice (Oryza sativa L.)
title_sort integrated microbiome and metabolomic analysis reveal responses of rhizosphere bacterial communities and root exudate composition to drought and genotype in rice (oryza sativa l.)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10090257/
https://www.ncbi.nlm.nih.gov/pubmed/37039929
http://dx.doi.org/10.1186/s12284-023-00636-1
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