Modulation of the Tomato Rhizosphere Microbiome via Changes in Root Exudation Mediated by the Ethylene Receptor NR

Plant hormones have been recently shown to exert an indirect influence on the recruitment of plant-associated microbiomes. However, it remains unclear the extent to which the disruption of the ethylene (ET) signaling pathway affects the assembly and functioning of plant-root microbiomes. In this stu...

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Main Authors: Ruixin Fu, Haichao Feng, Francisco Dini-Andreote, Zhen Wang, Chunbin Bo, Wenhui Cao, Keming Yang, Mingchun Liu, Tianjie Yang, Qirong Shen, Yangchun Xu, Zhong Wei
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/9/12/2456
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author Ruixin Fu
Haichao Feng
Francisco Dini-Andreote
Zhen Wang
Chunbin Bo
Wenhui Cao
Keming Yang
Mingchun Liu
Tianjie Yang
Qirong Shen
Yangchun Xu
Zhong Wei
author_facet Ruixin Fu
Haichao Feng
Francisco Dini-Andreote
Zhen Wang
Chunbin Bo
Wenhui Cao
Keming Yang
Mingchun Liu
Tianjie Yang
Qirong Shen
Yangchun Xu
Zhong Wei
author_sort Ruixin Fu
collection DOAJ
description Plant hormones have been recently shown to exert an indirect influence on the recruitment of plant-associated microbiomes. However, it remains unclear the extent to which the disruption of the ethylene (ET) signaling pathway affects the assembly and functioning of plant-root microbiomes. In this study, the Never-ripe tomato mutant (<i>Nr</i>) was profiled for differences compared to the wild type (control). Tomato plants were subjected to root exudate profiling and the characterization of bacterial and fungal communities. Compared to the control, <i>Nr</i> revealed differences in the composition of root exudates, including lower amounts of esculetin, gallic acid, L-fucose, eicosapentaenoic acid, and higher amounts of β-aldehyde. Interestingly, <i>Nr</i> significantly differed in the composition and functioning of the rhizosphere bacterial community. We also identified the taxa that occurred at relatively higher abundances in <i>Nr</i>, including the genus <i>Lysobacter</i>, which displayed a significant negative correlation with changes in eicosapentaenoic acid and esculetin, and a significant positive correlation with changes in β-aldehyde. Taken together, our study provides evidence that a mutation in the ET receptor exerts predictable changes in the root-associated microbial taxa of tomato plants. These indirect effects can potentially be explored towards new strategies to engineer beneficial plant microbiomes via targeted changes in plant genetics and physiology.
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spelling doaj.art-350638a1cd224114939a84fde9e55a012023-11-23T09:38:15ZengMDPI AGMicroorganisms2076-26072021-11-01912245610.3390/microorganisms9122456Modulation of the Tomato Rhizosphere Microbiome via Changes in Root Exudation Mediated by the Ethylene Receptor NRRuixin Fu0Haichao Feng1Francisco Dini-Andreote2Zhen Wang3Chunbin Bo4Wenhui Cao5Keming Yang6Mingchun Liu7Tianjie Yang8Qirong Shen9Yangchun Xu10Zhong Wei11Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaDepartment of Plant Science and Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16801, USAJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, ChinaJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-Based Fertilizers, Nanjing Agricultural University, Nanjing 210095, ChinaPlant hormones have been recently shown to exert an indirect influence on the recruitment of plant-associated microbiomes. However, it remains unclear the extent to which the disruption of the ethylene (ET) signaling pathway affects the assembly and functioning of plant-root microbiomes. In this study, the Never-ripe tomato mutant (<i>Nr</i>) was profiled for differences compared to the wild type (control). Tomato plants were subjected to root exudate profiling and the characterization of bacterial and fungal communities. Compared to the control, <i>Nr</i> revealed differences in the composition of root exudates, including lower amounts of esculetin, gallic acid, L-fucose, eicosapentaenoic acid, and higher amounts of β-aldehyde. Interestingly, <i>Nr</i> significantly differed in the composition and functioning of the rhizosphere bacterial community. We also identified the taxa that occurred at relatively higher abundances in <i>Nr</i>, including the genus <i>Lysobacter</i>, which displayed a significant negative correlation with changes in eicosapentaenoic acid and esculetin, and a significant positive correlation with changes in β-aldehyde. Taken together, our study provides evidence that a mutation in the ET receptor exerts predictable changes in the root-associated microbial taxa of tomato plants. These indirect effects can potentially be explored towards new strategies to engineer beneficial plant microbiomes via targeted changes in plant genetics and physiology.https://www.mdpi.com/2076-2607/9/12/2456ethylenenever-ripe (<i>Nr</i>)rhizospheremicrobiomeroot exudation
spellingShingle Ruixin Fu
Haichao Feng
Francisco Dini-Andreote
Zhen Wang
Chunbin Bo
Wenhui Cao
Keming Yang
Mingchun Liu
Tianjie Yang
Qirong Shen
Yangchun Xu
Zhong Wei
Modulation of the Tomato Rhizosphere Microbiome via Changes in Root Exudation Mediated by the Ethylene Receptor NR
Microorganisms
ethylene
never-ripe (<i>Nr</i>)
rhizosphere
microbiome
root exudation
title Modulation of the Tomato Rhizosphere Microbiome via Changes in Root Exudation Mediated by the Ethylene Receptor NR
title_full Modulation of the Tomato Rhizosphere Microbiome via Changes in Root Exudation Mediated by the Ethylene Receptor NR
title_fullStr Modulation of the Tomato Rhizosphere Microbiome via Changes in Root Exudation Mediated by the Ethylene Receptor NR
title_full_unstemmed Modulation of the Tomato Rhizosphere Microbiome via Changes in Root Exudation Mediated by the Ethylene Receptor NR
title_short Modulation of the Tomato Rhizosphere Microbiome via Changes in Root Exudation Mediated by the Ethylene Receptor NR
title_sort modulation of the tomato rhizosphere microbiome via changes in root exudation mediated by the ethylene receptor nr
topic ethylene
never-ripe (<i>Nr</i>)
rhizosphere
microbiome
root exudation
url https://www.mdpi.com/2076-2607/9/12/2456
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