Root exudates drive the soil-borne legacy of aboveground pathogen infection
Abstract Background Plants are capable of building up beneficial rhizosphere communities as is evidenced by disease-suppressive soils. However, it is not known how and why soil bacterial communities are impacted by plant exposure to foliar pathogens and if such responses might improve plant performa...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2018-09-01
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| Series: | Microbiome |
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| Online Access: | http://link.springer.com/article/10.1186/s40168-018-0537-x |
| _version_ | 1819146745006784512 |
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| author | Jun Yuan Jun Zhao Tao Wen Mengli Zhao Rong Li Pim Goossens Qiwei Huang Yang Bai Jorge M. Vivanco George A. Kowalchuk Roeland L. Berendsen Qirong Shen |
| author_facet | Jun Yuan Jun Zhao Tao Wen Mengli Zhao Rong Li Pim Goossens Qiwei Huang Yang Bai Jorge M. Vivanco George A. Kowalchuk Roeland L. Berendsen Qirong Shen |
| author_sort | Jun Yuan |
| collection | DOAJ |
| description | Abstract Background Plants are capable of building up beneficial rhizosphere communities as is evidenced by disease-suppressive soils. However, it is not known how and why soil bacterial communities are impacted by plant exposure to foliar pathogens and if such responses might improve plant performance in the presence of the pathogen. Here, we conditioned soil by growing multiple generations (five) of Arabidopsis thaliana inoculated aboveground with Pseudomonas syringae pv tomato (Pst) in the same soil. We then examined rhizosphere communities and plant performance in a subsequent generation (sixth) grown in pathogen-conditioned versus control-conditioned soil. Moreover, we assessed the role of altered root exudation profiles in shaping the root microbiome of infected plants. Results Plants grown in conditioned soil showed increased levels of jasmonic acid and improved disease resistance. Illumina Miseq 16S rRNA gene tag sequencing revealed that both rhizosphere and bulk soil bacterial communities were altered by Pst infection. Infected plants exhibited significantly higher exudation of amino acids, nucleotides, and long-chain organic acids (LCOAs) (C > 6) and lower exudation levels for sugars, alcohols, and short-chain organic acids (SCOAs) (C ≤ 6). Interestingly, addition of exogenous amino acids and LCOA also elicited a disease-suppressive response. Conclusion Collectively, our data suggest that plants can recruit beneficial rhizosphere communities via modification of plant exudation patterns in response to exposure to aboveground pathogens to the benefit of subsequent plant generations. |
| first_indexed | 2024-12-22T13:18:48Z |
| format | Article |
| id | doaj.art-24d8e607c88a4d088b7b562668ae2b5c |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-22T13:18:48Z |
| publishDate | 2018-09-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-24d8e607c88a4d088b7b562668ae2b5c2022-12-21T18:24:31ZengBMCMicrobiome2049-26182018-09-016111210.1186/s40168-018-0537-xRoot exudates drive the soil-borne legacy of aboveground pathogen infectionJun Yuan0Jun Zhao1Tao Wen2Mengli Zhao3Rong Li4Pim Goossens5Qiwei Huang6Yang Bai7Jorge M. Vivanco8George A. Kowalchuk9Roeland L. Berendsen10Qirong Shen11Jiangsu Provincial Key Lab for Organic Solid Waste Utilization; National Engineering Research Center for Organic-based Fertilizers; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural UniversitySchool of Geography Science, Nanjing Normal UniversityJiangsu Provincial Key Lab for Organic Solid Waste Utilization; National Engineering Research Center for Organic-based Fertilizers; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural UniversityJiangsu Provincial Key Lab for Organic Solid Waste Utilization; National Engineering Research Center for Organic-based Fertilizers; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural UniversityJiangsu Provincial Key Lab for Organic Solid Waste Utilization; National Engineering Research Center for Organic-based Fertilizers; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural UniversityPlant-Microbe Interactions, Institute of Environmental Biology, Utrecht UniversityJiangsu Provincial Key Lab for Organic Solid Waste Utilization; National Engineering Research Center for Organic-based Fertilizers; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural UniversityState Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of ScienceDepartment of Horticulture and Landscape Architecture and Center for Rhizosphere Biology, Colorado State UniversityEcology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, Utrecht UniversityPlant-Microbe Interactions, Institute of Environmental Biology, Utrecht UniversityJiangsu Provincial Key Lab for Organic Solid Waste Utilization; National Engineering Research Center for Organic-based Fertilizers; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural UniversityAbstract Background Plants are capable of building up beneficial rhizosphere communities as is evidenced by disease-suppressive soils. However, it is not known how and why soil bacterial communities are impacted by plant exposure to foliar pathogens and if such responses might improve plant performance in the presence of the pathogen. Here, we conditioned soil by growing multiple generations (five) of Arabidopsis thaliana inoculated aboveground with Pseudomonas syringae pv tomato (Pst) in the same soil. We then examined rhizosphere communities and plant performance in a subsequent generation (sixth) grown in pathogen-conditioned versus control-conditioned soil. Moreover, we assessed the role of altered root exudation profiles in shaping the root microbiome of infected plants. Results Plants grown in conditioned soil showed increased levels of jasmonic acid and improved disease resistance. Illumina Miseq 16S rRNA gene tag sequencing revealed that both rhizosphere and bulk soil bacterial communities were altered by Pst infection. Infected plants exhibited significantly higher exudation of amino acids, nucleotides, and long-chain organic acids (LCOAs) (C > 6) and lower exudation levels for sugars, alcohols, and short-chain organic acids (SCOAs) (C ≤ 6). Interestingly, addition of exogenous amino acids and LCOA also elicited a disease-suppressive response. Conclusion Collectively, our data suggest that plants can recruit beneficial rhizosphere communities via modification of plant exudation patterns in response to exposure to aboveground pathogens to the benefit of subsequent plant generations.http://link.springer.com/article/10.1186/s40168-018-0537-xSoil-borne legacyFoliar pathogenMicrobiomeDisease-suppressive soilRoot exudates |
| spellingShingle | Jun Yuan Jun Zhao Tao Wen Mengli Zhao Rong Li Pim Goossens Qiwei Huang Yang Bai Jorge M. Vivanco George A. Kowalchuk Roeland L. Berendsen Qirong Shen Root exudates drive the soil-borne legacy of aboveground pathogen infection Microbiome Soil-borne legacy Foliar pathogen Microbiome Disease-suppressive soil Root exudates |
| title | Root exudates drive the soil-borne legacy of aboveground pathogen infection |
| title_full | Root exudates drive the soil-borne legacy of aboveground pathogen infection |
| title_fullStr | Root exudates drive the soil-borne legacy of aboveground pathogen infection |
| title_full_unstemmed | Root exudates drive the soil-borne legacy of aboveground pathogen infection |
| title_short | Root exudates drive the soil-borne legacy of aboveground pathogen infection |
| title_sort | root exudates drive the soil borne legacy of aboveground pathogen infection |
| topic | Soil-borne legacy Foliar pathogen Microbiome Disease-suppressive soil Root exudates |
| url | http://link.springer.com/article/10.1186/s40168-018-0537-x |
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