Plant commensal type VII secretion system causes iron leakage from roots to promote colonization

Yunpeng Liu; Xia Shu; Lin Chen; Huihui Zhang; Haichao Feng; Xiting Sun; Qin Xiong; Guangqi Li; Weibing Xun; Zhihui Xu; Nan Zhang; Corné M.J. Pieterse; Qirong Shen; Ruifu Zhang

doi:10.1038/s41564-023-01402-1

Plant commensal type VII secretion system causes iron leakage from roots to promote colonization

Yunpeng Liu^*, Xia Shu, Lin Chen, Huihui Zhang, Haichao Feng, Xiting Sun, Qin Xiong, Guangqi Li, Weibing Xun, Zhihui Xu, Nan Zhang, Corné M.J. Pieterse, Qirong Shen, Ruifu Zhang^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Competition for iron is an important factor for microbial niche establishment in the rhizosphere. Pathogenic and beneficial symbiotic bacteria use various secretion systems to interact with their hosts and acquire limited resources from the environment. Bacillus spp. are important plant commensals that encode a type VII secretion system (T7SS). However, the function of this secretion system in rhizobacteria–plant interactions is unclear. Here we use the beneficial rhizobacterium Bacillus velezensis SQR9 to show that the T7SS and the major secreted protein YukE are critical for root colonization. In planta experiments and liposome-based experiments demonstrate that secreted YukE inserts into the plant plasma membrane and causes root iron leakage in the early stage of inoculation. The increased availability of iron promotes root colonization by SQR9. Overall, our work reveals a previously undescribed role of the T7SS in a beneficial rhizobacterium to promote colonization and thus plant–microbe interactions.

Original language	English
Pages (from-to)	1434-1449
Number of pages	16
Journal	Nature Microbiology
Volume	8
Issue number	8
Early online date	29 May 2023
DOIs	https://doi.org/10.1038/s41564-023-01402-1
Publication status	Published - Aug 2023

Bibliographical note

Publisher Copyright:
© 2023, The Author(s), under exclusive licence to Springer Nature Limited.

Funding

This work was funded by the National Natural Science Foundation of China (32070104, Y.L.), the National Natural Science Foundation of China (32172661, R.Z.), the National Key Research and Development Programme (2022YFF1001804, R.Z.), the National Key Research and Development Program (2021YFF1000400, Y.L. and R.Z.), the Central Public-interest Scientific Institution Basal Research Fund (No. Y2022QC15, Y.L.), and the Agricultural Science and Technology Innovation Program (CAAS-ZDRW202308, Y.L.). We thank H. Wei and J. Li of the Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, for providing the strains and plasmid used in the Agrobacterium -mediated transient expression experiment; and X. Shen of the College of Life Sciences, Northwest A&F University, for help with editing the manuscript. This work was funded by the National Natural Science Foundation of China (32070104, Y.L.), the National Natural Science Foundation of China (32172661, R.Z.), the National Key Research and Development Programme (2022YFF1001804, R.Z.), the National Key Research and Development Program (2021YFF1000400, Y.L. and R.Z.), the Central Public-interest Scientific Institution Basal Research Fund (No. Y2022QC15, Y.L.), and the Agricultural Science and Technology Innovation Program (CAAS-ZDRW202308, Y.L.). We thank H. Wei and J. Li of the Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, for providing the strains and plasmid used in the Agrobacterium-mediated transient expression experiment; and X. Shen of the College of Life Sciences, Northwest A&F University, for help with editing the manuscript.

Funders	Funder number
Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences
National Natural Science Foundation of China	32070104, 32172661
National Key Research and Development Program of China	2022YFF1001804, 2021YFF1000400
Agricultural Science and Technology Innovation Program	CAAS-ZDRW202308
Central Public-interest Scientific Institution Basal Research Fund, Chinese Academy of Fishery Sciences	Y2022QC15

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10.1038/s41564-023-01402-1

NatureMicrobiology-Liu-2023Final published version, 5.33 MBLicence: Taverne

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title = "Plant commensal type VII secretion system causes iron leakage from roots to promote colonization",

abstract = "Competition for iron is an important factor for microbial niche establishment in the rhizosphere. Pathogenic and beneficial symbiotic bacteria use various secretion systems to interact with their hosts and acquire limited resources from the environment. Bacillus spp. are important plant commensals that encode a type VII secretion system (T7SS). However, the function of this secretion system in rhizobacteria–plant interactions is unclear. Here we use the beneficial rhizobacterium Bacillus velezensis SQR9 to show that the T7SS and the major secreted protein YukE are critical for root colonization. In planta experiments and liposome-based experiments demonstrate that secreted YukE inserts into the plant plasma membrane and causes root iron leakage in the early stage of inoculation. The increased availability of iron promotes root colonization by SQR9. Overall, our work reveals a previously undescribed role of the T7SS in a beneficial rhizobacterium to promote colonization and thus plant–microbe interactions.",

author = "Yunpeng Liu and Xia Shu and Lin Chen and Huihui Zhang and Haichao Feng and Xiting Sun and Qin Xiong and Guangqi Li and Weibing Xun and Zhihui Xu and Nan Zhang and Pieterse, {Corn{\'e} M.J.} and Qirong Shen and Ruifu Zhang",

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year = "2023",

month = aug,

doi = "10.1038/s41564-023-01402-1",

language = "English",

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AU - Liu, Yunpeng

AU - Shu, Xia

AU - Chen, Lin

AU - Zhang, Huihui

AU - Feng, Haichao

AU - Sun, Xiting

AU - Xiong, Qin

AU - Li, Guangqi

AU - Xun, Weibing

AU - Xu, Zhihui

AU - Zhang, Nan

AU - Pieterse, Corné M.J.

AU - Shen, Qirong

AU - Zhang, Ruifu

PY - 2023/8

Y1 - 2023/8

N2 - Competition for iron is an important factor for microbial niche establishment in the rhizosphere. Pathogenic and beneficial symbiotic bacteria use various secretion systems to interact with their hosts and acquire limited resources from the environment. Bacillus spp. are important plant commensals that encode a type VII secretion system (T7SS). However, the function of this secretion system in rhizobacteria–plant interactions is unclear. Here we use the beneficial rhizobacterium Bacillus velezensis SQR9 to show that the T7SS and the major secreted protein YukE are critical for root colonization. In planta experiments and liposome-based experiments demonstrate that secreted YukE inserts into the plant plasma membrane and causes root iron leakage in the early stage of inoculation. The increased availability of iron promotes root colonization by SQR9. Overall, our work reveals a previously undescribed role of the T7SS in a beneficial rhizobacterium to promote colonization and thus plant–microbe interactions.

AB - Competition for iron is an important factor for microbial niche establishment in the rhizosphere. Pathogenic and beneficial symbiotic bacteria use various secretion systems to interact with their hosts and acquire limited resources from the environment. Bacillus spp. are important plant commensals that encode a type VII secretion system (T7SS). However, the function of this secretion system in rhizobacteria–plant interactions is unclear. Here we use the beneficial rhizobacterium Bacillus velezensis SQR9 to show that the T7SS and the major secreted protein YukE are critical for root colonization. In planta experiments and liposome-based experiments demonstrate that secreted YukE inserts into the plant plasma membrane and causes root iron leakage in the early stage of inoculation. The increased availability of iron promotes root colonization by SQR9. Overall, our work reveals a previously undescribed role of the T7SS in a beneficial rhizobacterium to promote colonization and thus plant–microbe interactions.

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Plant commensal type VII secretion system causes iron leakage from roots to promote colonization

Abstract

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