Root-associated bacterial communities and root metabolite composition are linked to nitrogen use efficiency in sorghum
ABSTRACTThe development of cereal crops with high nitrogen use efficiency (NUE) is a priority for worldwide agriculture. In addition to conventional plant breeding and genetic engineering, the use of the plant microbiome offers another approach to improving crop NUE. To gain insight into the bacteri...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2024-01-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01190-23 |
| _version_ | 1797348305585307648 |
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| author | Yen Ning Chai Yunhui Qi Emily Goren Dawn Chiniquy Amy M. Sheflin Susannah G. Tringe Jessica E. Prenni Peng Liu Daniel P. Schachtman |
| author_facet | Yen Ning Chai Yunhui Qi Emily Goren Dawn Chiniquy Amy M. Sheflin Susannah G. Tringe Jessica E. Prenni Peng Liu Daniel P. Schachtman |
| author_sort | Yen Ning Chai |
| collection | DOAJ |
| description | ABSTRACTThe development of cereal crops with high nitrogen use efficiency (NUE) is a priority for worldwide agriculture. In addition to conventional plant breeding and genetic engineering, the use of the plant microbiome offers another approach to improving crop NUE. To gain insight into the bacterial communities associated with sorghum lines that differ in NUE, a field experiment was designed comparing 24 diverse Sorghum bicolor lines under sufficient and deficient nitrogen (N). Amplicon sequencing and untargeted gas chromatography–mass spectrometry were used to characterize the bacterial communities and the root metabolome associated with sorghum genotypes varying in sensitivity to low N. We demonstrated that N stress and sorghum type (energy, sweet, and grain sorghum) significantly impacted the root-associated bacterial communities and root metabolite composition of sorghum. We found a positive correlation between sorghum NUE and bacterial richness and diversity in the rhizosphere. The greater alpha diversity in high NUE lines was associated with the decreased abundance of a dominant bacterial taxon, Pseudomonas. Multiple strong correlations were detected between root metabolites and rhizosphere bacterial communities in response to low N stress. This indicates that the shift in the sorghum microbiome due to low N is associated with the root metabolites of the host plant. Taken together, our findings suggest that host genetic regulation of root metabolites plays a role in defining the root-associated microbiome of sorghum genotypes differing in NUE and tolerance to low N stress.IMPORTANCEThe development of crops that are more nitrogen use-efficient (NUE) is critical for the future of the enhanced sustainability of agriculture worldwide. This objective has been pursued mainly through plant breeding and plant molecular engineering, but these approaches have had only limited success. Therefore, a different strategy that leverages soil microbes needs to be fully explored because it is known that soil microbes improve plant growth through multiple mechanisms. To design approaches that use the soil microbiome to increase NUE, it will first be essential to understand the relationship among soil microbes, root metabolites, and crop productivity. Using this approach, we demonstrated that certain key metabolites and specific microbes are associated with high and low sorghum NUE in a field study. This important information provides a new path forward for developing crop genotypes that have increased NUE through the positive contribution of soil microbes. |
| first_indexed | 2024-03-08T12:02:54Z |
| format | Article |
| id | doaj.art-acbca23da8894cff9bbd0474d1371a0e |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-08T12:02:54Z |
| publishDate | 2024-01-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-acbca23da8894cff9bbd0474d1371a0e2024-01-23T14:00:49ZengAmerican Society for MicrobiologymSystems2379-50772024-01-019110.1128/msystems.01190-23Root-associated bacterial communities and root metabolite composition are linked to nitrogen use efficiency in sorghumYen Ning Chai0Yunhui Qi1Emily Goren2Dawn Chiniquy3Amy M. Sheflin4Susannah G. Tringe5Jessica E. Prenni6Peng Liu7Daniel P. Schachtman8Department of Agronomy and Horticulture, Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, Nebraska, USADepartment of Statistics, Iowa State University, Ames, Iowa, USADepartment of Statistics, Iowa State University, Ames, Iowa, USAEnvironmental Genomics and System Biology, Lawrence Berkeley National Laboratory, Berkeley, California, USADepartment of Horticulture and Landscape Architecture, Colorado State University, Colorado State University, Fort Collins, Colorado, USAEnvironmental Genomics and System Biology, Lawrence Berkeley National Laboratory, Berkeley, California, USADepartment of Horticulture and Landscape Architecture, Colorado State University, Colorado State University, Fort Collins, Colorado, USADepartment of Statistics, Iowa State University, Ames, Iowa, USADepartment of Agronomy and Horticulture, Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, Nebraska, USAABSTRACTThe development of cereal crops with high nitrogen use efficiency (NUE) is a priority for worldwide agriculture. In addition to conventional plant breeding and genetic engineering, the use of the plant microbiome offers another approach to improving crop NUE. To gain insight into the bacterial communities associated with sorghum lines that differ in NUE, a field experiment was designed comparing 24 diverse Sorghum bicolor lines under sufficient and deficient nitrogen (N). Amplicon sequencing and untargeted gas chromatography–mass spectrometry were used to characterize the bacterial communities and the root metabolome associated with sorghum genotypes varying in sensitivity to low N. We demonstrated that N stress and sorghum type (energy, sweet, and grain sorghum) significantly impacted the root-associated bacterial communities and root metabolite composition of sorghum. We found a positive correlation between sorghum NUE and bacterial richness and diversity in the rhizosphere. The greater alpha diversity in high NUE lines was associated with the decreased abundance of a dominant bacterial taxon, Pseudomonas. Multiple strong correlations were detected between root metabolites and rhizosphere bacterial communities in response to low N stress. This indicates that the shift in the sorghum microbiome due to low N is associated with the root metabolites of the host plant. Taken together, our findings suggest that host genetic regulation of root metabolites plays a role in defining the root-associated microbiome of sorghum genotypes differing in NUE and tolerance to low N stress.IMPORTANCEThe development of crops that are more nitrogen use-efficient (NUE) is critical for the future of the enhanced sustainability of agriculture worldwide. This objective has been pursued mainly through plant breeding and plant molecular engineering, but these approaches have had only limited success. Therefore, a different strategy that leverages soil microbes needs to be fully explored because it is known that soil microbes improve plant growth through multiple mechanisms. To design approaches that use the soil microbiome to increase NUE, it will first be essential to understand the relationship among soil microbes, root metabolites, and crop productivity. Using this approach, we demonstrated that certain key metabolites and specific microbes are associated with high and low sorghum NUE in a field study. This important information provides a new path forward for developing crop genotypes that have increased NUE through the positive contribution of soil microbes.https://journals.asm.org/doi/10.1128/msystems.01190-23sorghumroot metabolitesbacterial communitiesnitrogen use efficiencynitrogen stressbiomass |
| spellingShingle | Yen Ning Chai Yunhui Qi Emily Goren Dawn Chiniquy Amy M. Sheflin Susannah G. Tringe Jessica E. Prenni Peng Liu Daniel P. Schachtman Root-associated bacterial communities and root metabolite composition are linked to nitrogen use efficiency in sorghum mSystems sorghum root metabolites bacterial communities nitrogen use efficiency nitrogen stress biomass |
| title | Root-associated bacterial communities and root metabolite composition are linked to nitrogen use efficiency in sorghum |
| title_full | Root-associated bacterial communities and root metabolite composition are linked to nitrogen use efficiency in sorghum |
| title_fullStr | Root-associated bacterial communities and root metabolite composition are linked to nitrogen use efficiency in sorghum |
| title_full_unstemmed | Root-associated bacterial communities and root metabolite composition are linked to nitrogen use efficiency in sorghum |
| title_short | Root-associated bacterial communities and root metabolite composition are linked to nitrogen use efficiency in sorghum |
| title_sort | root associated bacterial communities and root metabolite composition are linked to nitrogen use efficiency in sorghum |
| topic | sorghum root metabolites bacterial communities nitrogen use efficiency nitrogen stress biomass |
| url | https://journals.asm.org/doi/10.1128/msystems.01190-23 |
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