Ethylene signals through an ethylene receptor to modulate biofilm formation and root colonization in a beneficial plant-associated bacterium.

Ethylene is a plant hormone involved in many aspects of plant growth and development as well as responses to stress. The role of ethylene in plant-microbe interactions has been explored from the perspective of plants. However, only a small number of studies have examined the role of ethylene in micr...

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Main Authors: T Scott Carlew, Eric Brenya, Mahbuba Ferdous, Ishita Banerjee, Lauren Donnelly, Eric Heinze, Josie King, Briana Sexton, Randy F Lacey, Arkadipta Bakshi, Gladys Alexandre, Brad M Binder
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-02-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1011587
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author T Scott Carlew
Eric Brenya
Mahbuba Ferdous
Ishita Banerjee
Lauren Donnelly
Eric Heinze
Josie King
Briana Sexton
Randy F Lacey
Arkadipta Bakshi
Gladys Alexandre
Brad M Binder
author_facet T Scott Carlew
Eric Brenya
Mahbuba Ferdous
Ishita Banerjee
Lauren Donnelly
Eric Heinze
Josie King
Briana Sexton
Randy F Lacey
Arkadipta Bakshi
Gladys Alexandre
Brad M Binder
author_sort T Scott Carlew
collection DOAJ
description Ethylene is a plant hormone involved in many aspects of plant growth and development as well as responses to stress. The role of ethylene in plant-microbe interactions has been explored from the perspective of plants. However, only a small number of studies have examined the role of ethylene in microbes. We demonstrated that Azospirillum brasilense contains a functional ethylene receptor that we call Azospirillum Ethylene Response1 (AzoEtr1) after the nomenclature used in plants. AzoEtr1 directly binds ethylene with high affinity. Treating cells with ethylene or disrupting the receptor reduces biofilm formation and colonization of plant root surfaces. Additionally, RNA sequencing and untargeted metabolomics showed that ethylene causes wide-spread metabolic changes that affect carbon and nitrogen metabolism. One result is the accumulation of poly-hydroxybutyrate. Our data suggests a model in which ethylene from host plants alters the density of colonization by A. brasilense and re-wires its metabolism, suggesting that the bacterium implements an adaptation program upon sensing ethylene. These data provide potential new targets to regulate beneficial plant-microbe interactions.
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spelling doaj-art-86f0881dcd7f4c14b2f2a1bacac947f92025-08-20T02:57:02ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042025-02-01212e101158710.1371/journal.pgen.1011587Ethylene signals through an ethylene receptor to modulate biofilm formation and root colonization in a beneficial plant-associated bacterium.T Scott CarlewEric BrenyaMahbuba FerdousIshita BanerjeeLauren DonnellyEric HeinzeJosie KingBriana SextonRandy F LaceyArkadipta BakshiGladys AlexandreBrad M BinderEthylene is a plant hormone involved in many aspects of plant growth and development as well as responses to stress. The role of ethylene in plant-microbe interactions has been explored from the perspective of plants. However, only a small number of studies have examined the role of ethylene in microbes. We demonstrated that Azospirillum brasilense contains a functional ethylene receptor that we call Azospirillum Ethylene Response1 (AzoEtr1) after the nomenclature used in plants. AzoEtr1 directly binds ethylene with high affinity. Treating cells with ethylene or disrupting the receptor reduces biofilm formation and colonization of plant root surfaces. Additionally, RNA sequencing and untargeted metabolomics showed that ethylene causes wide-spread metabolic changes that affect carbon and nitrogen metabolism. One result is the accumulation of poly-hydroxybutyrate. Our data suggests a model in which ethylene from host plants alters the density of colonization by A. brasilense and re-wires its metabolism, suggesting that the bacterium implements an adaptation program upon sensing ethylene. These data provide potential new targets to regulate beneficial plant-microbe interactions.https://doi.org/10.1371/journal.pgen.1011587
spellingShingle T Scott Carlew
Eric Brenya
Mahbuba Ferdous
Ishita Banerjee
Lauren Donnelly
Eric Heinze
Josie King
Briana Sexton
Randy F Lacey
Arkadipta Bakshi
Gladys Alexandre
Brad M Binder
Ethylene signals through an ethylene receptor to modulate biofilm formation and root colonization in a beneficial plant-associated bacterium.
PLoS Genetics
title Ethylene signals through an ethylene receptor to modulate biofilm formation and root colonization in a beneficial plant-associated bacterium.
title_full Ethylene signals through an ethylene receptor to modulate biofilm formation and root colonization in a beneficial plant-associated bacterium.
title_fullStr Ethylene signals through an ethylene receptor to modulate biofilm formation and root colonization in a beneficial plant-associated bacterium.
title_full_unstemmed Ethylene signals through an ethylene receptor to modulate biofilm formation and root colonization in a beneficial plant-associated bacterium.
title_short Ethylene signals through an ethylene receptor to modulate biofilm formation and root colonization in a beneficial plant-associated bacterium.
title_sort ethylene signals through an ethylene receptor to modulate biofilm formation and root colonization in a beneficial plant associated bacterium
url https://doi.org/10.1371/journal.pgen.1011587
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