A Genome-Wide Screen Identifies Genes in Rhizosphere-Associated <italic toggle="yes">Pseudomonas</italic> Required to Evade Plant Defenses

ABSTRACT Pseudomonas fluorescens and related plant root (“rhizosphere”)-associated species contribute to plant health by modulating defenses and facilitating nutrient uptake. To identify bacterial fitness determinants in the rhizosphere of the model plant Arabidopsis thaliana, we performed a high-th...

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Autores principales: Zhexian Liu, Polina Beskrovnaya, Ryan A. Melnyk, Sarzana S. Hossain, Sophie Khorasani, Lucy R. O’Sullivan, Christina L. Wiesmann, Jen Bush, Joël D. Richard, Cara H. Haney
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:c60a8f4c47db4d34ad973715154addeb2021-11-15T15:52:19ZA Genome-Wide Screen Identifies Genes in Rhizosphere-Associated <italic toggle="yes">Pseudomonas</italic> Required to Evade Plant Defenses10.1128/mBio.00433-182150-7511https://doaj.org/article/c60a8f4c47db4d34ad973715154addeb2018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00433-18https://doaj.org/toc/2150-7511ABSTRACT Pseudomonas fluorescens and related plant root (“rhizosphere”)-associated species contribute to plant health by modulating defenses and facilitating nutrient uptake. To identify bacterial fitness determinants in the rhizosphere of the model plant Arabidopsis thaliana, we performed a high-throughput transposon sequencing (Tn-Seq) screen using the biocontrol and growth-promoting strain Pseudomonas sp. WCS365. The screen, which was performed in parallel on wild-type and immunocompromised Arabidopsis plants, identified 231 genes that increased fitness in the rhizosphere of wild-type plants. A subset of these genes decreased fitness in the rhizosphere of immunocompromised plants. We hypothesized that these genes might be involved in avoiding plant defenses and verified 7 Pseudomonas sp. WCS365 candidate genes by generating clean deletions. We found that two of these deletion mutants, ΔmorA (encoding a putative diguanylate cyclase/phosphodiesterase) and ΔspuC (encoding a putrescine aminotransferase), formed enhanced biofilms and inhibited plant growth. We found that mutants ΔspuC and ΔmorA induced pattern-triggered immunity (PTI) as measured by induction of an Arabidopsis PTI reporter and FLS2/BAK1-dependent inhibition of plant growth. We show that MorA acts as a phosphodiesterase to inhibit biofilm formation, suggesting a possible role in biofilm dispersal. We found that both putrescine and its precursor arginine promote biofilm formation that is enhanced in the ΔspuC mutant, which cannot break down putrescine, suggesting that putrescine might serve as a signaling molecule in the rhizosphere. Collectively, this work identified novel bacterial factors required to evade plant defenses in the rhizosphere. IMPORTANCE While rhizosphere bacteria hold the potential to improve plant health and fitness, little is known about the bacterial genes required to evade host immunity. Using a model system consisting of Arabidopsis and a beneficial Pseudomonas sp. isolate, we identified bacterial genes required for both rhizosphere fitness and for evading host immune responses. This work advances our understanding of how evasion of host defenses contributes to survival in the rhizosphere.Zhexian LiuPolina BeskrovnayaRyan A. MelnykSarzana S. HossainSophie KhorasaniLucy R. O’SullivanChristina L. WiesmannJen BushJoël D. RichardCara H. HaneyAmerican Society for MicrobiologyarticleArabidopsisPseudomonaspattern-triggered immunityphosphodiesteraseputrescinerhizosphereMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution DOAJ
collection DOAJ
language EN
topic Arabidopsis
Pseudomonas
pattern-triggered immunity
phosphodiesterase
putrescine
rhizosphere
Microbiology
QR1-502
spellingShingle Arabidopsis
Pseudomonas
pattern-triggered immunity
phosphodiesterase
putrescine
rhizosphere
Microbiology
QR1-502
Zhexian Liu
Polina Beskrovnaya
Ryan A. Melnyk
Sarzana S. Hossain
Sophie Khorasani
Lucy R. O’Sullivan
Christina L. Wiesmann
Jen Bush
Joël D. Richard
Cara H. Haney
A Genome-Wide Screen Identifies Genes in Rhizosphere-Associated <italic toggle="yes">Pseudomonas</italic> Required to Evade Plant Defenses
description ABSTRACT Pseudomonas fluorescens and related plant root (“rhizosphere”)-associated species contribute to plant health by modulating defenses and facilitating nutrient uptake. To identify bacterial fitness determinants in the rhizosphere of the model plant Arabidopsis thaliana, we performed a high-throughput transposon sequencing (Tn-Seq) screen using the biocontrol and growth-promoting strain Pseudomonas sp. WCS365. The screen, which was performed in parallel on wild-type and immunocompromised Arabidopsis plants, identified 231 genes that increased fitness in the rhizosphere of wild-type plants. A subset of these genes decreased fitness in the rhizosphere of immunocompromised plants. We hypothesized that these genes might be involved in avoiding plant defenses and verified 7 Pseudomonas sp. WCS365 candidate genes by generating clean deletions. We found that two of these deletion mutants, ΔmorA (encoding a putative diguanylate cyclase/phosphodiesterase) and ΔspuC (encoding a putrescine aminotransferase), formed enhanced biofilms and inhibited plant growth. We found that mutants ΔspuC and ΔmorA induced pattern-triggered immunity (PTI) as measured by induction of an Arabidopsis PTI reporter and FLS2/BAK1-dependent inhibition of plant growth. We show that MorA acts as a phosphodiesterase to inhibit biofilm formation, suggesting a possible role in biofilm dispersal. We found that both putrescine and its precursor arginine promote biofilm formation that is enhanced in the ΔspuC mutant, which cannot break down putrescine, suggesting that putrescine might serve as a signaling molecule in the rhizosphere. Collectively, this work identified novel bacterial factors required to evade plant defenses in the rhizosphere. IMPORTANCE While rhizosphere bacteria hold the potential to improve plant health and fitness, little is known about the bacterial genes required to evade host immunity. Using a model system consisting of Arabidopsis and a beneficial Pseudomonas sp. isolate, we identified bacterial genes required for both rhizosphere fitness and for evading host immune responses. This work advances our understanding of how evasion of host defenses contributes to survival in the rhizosphere.
format article
author Zhexian Liu
Polina Beskrovnaya
Ryan A. Melnyk
Sarzana S. Hossain
Sophie Khorasani
Lucy R. O’Sullivan
Christina L. Wiesmann
Jen Bush
Joël D. Richard
Cara H. Haney
author_facet Zhexian Liu
Polina Beskrovnaya
Ryan A. Melnyk
Sarzana S. Hossain
Sophie Khorasani
Lucy R. O’Sullivan
Christina L. Wiesmann
Jen Bush
Joël D. Richard
Cara H. Haney
author_sort Zhexian Liu
title A Genome-Wide Screen Identifies Genes in Rhizosphere-Associated <italic toggle="yes">Pseudomonas</italic> Required to Evade Plant Defenses
title_short A Genome-Wide Screen Identifies Genes in Rhizosphere-Associated <italic toggle="yes">Pseudomonas</italic> Required to Evade Plant Defenses
title_full A Genome-Wide Screen Identifies Genes in Rhizosphere-Associated <italic toggle="yes">Pseudomonas</italic> Required to Evade Plant Defenses
title_fullStr A Genome-Wide Screen Identifies Genes in Rhizosphere-Associated <italic toggle="yes">Pseudomonas</italic> Required to Evade Plant Defenses
title_full_unstemmed A Genome-Wide Screen Identifies Genes in Rhizosphere-Associated <italic toggle="yes">Pseudomonas</italic> Required to Evade Plant Defenses
title_sort genome-wide screen identifies genes in rhizosphere-associated <italic toggle="yes">pseudomonas</italic> required to evade plant defenses
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/c60a8f4c47db4d34ad973715154addeb
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