Multiple toxins and a protease contribute to the aphid-killing ability of Pseudomonas fluorescens PpR24

Deepa Paliwal; Mojgan Rabiey; Tim H. Mauchline; Keywan Hassani-Pak; Ralf Nauen; Carol Wagstaff; Simon Andrews; Chris Bass; Robert Jackson

doi:10.1111/1462-2920.16604

Multiple toxins and a protease contribute to the aphid-killing ability of Pseudomonas fluorescens PpR24

Deepa Paliwal, Mojgan Rabiey^*, Tim H. Mauchline, Keywan Hassani-Pak, Ralf Nauen, Carol Wagstaff, Simon Andrews, Chris Bass, Robert Jackson^*

^*Corresponding author for this work

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Abstract

Aphids are globally important pests causing damage to a broad range of crops. Due to insecticide resistance, there is an urgent need to develop alternative control strategies. In our previous work, we found Pseudomonas fluorescens PpR24 can orally infect and kill the insecticide-resistant green-peach aphid (Myzus persicae). However, the genetic basis of the insecticidal capability of PpR24 remains unclear. Genome sequencing of PpR24 confirmed the presence of various insecticidal toxins such as Tc (toxin complexes), Rhs (rearrangement hotspot) elements, and other insect-killing proteases. Upon aphids infection with PpR24, RNA-Seq analysis revealed 193 aphid genes were differentially expressed with down-regulation of 16 detoxification genes. In addition, 1325 PpR24 genes (542 were upregulated and 783 downregulated) were subject to differential expression, including genes responsible for secondary metabolite biosynthesis, the iron-restriction response, oxidative stress resistance, and virulence factors. Single and double deletion of candidate virulence genes encoding a secreted protease (AprX) and four toxin components (two TcA-like; one TcB-like; one TcC-like insecticidal toxins) showed that all five genes contribute significantly to aphid killing, particularly AprX. This comprehensive host–pathogen transcriptomic analysis provides novel insight into the molecular basis of bacteria-mediated aphid mortality and the potential of PpR24 as an effective biocontrol agent.

Original language	English
Article number	e16604
Number of pages	19
Journal	Environmental Microbiology
Volume	26
Issue number	4
DOIs	https://doi.org/10.1111/1462-2920.16604
Publication status	Published - 1 Apr 2024

Bibliographical note

Funding:
D.P. was funded by the University of Reading and Bayer Crop Science. We acknowledge funding for M.R. and R.W.J. from BBSRC (BB/P006272/1) and a jointly funded grant from UKRI, Defra, and the Scottish Government, under the Strategic Priorities Fund Plant Bacterial Diseases programme (BB/T010568/1). T.H.M. acknowledges the BBSRC funded ‘Growing Health’ (BB/X010953/1) and ‘Soils to Nutrition’ (BBS/E/C/000I0310) Institute Strategic Programmes. An initial RNA seq experiment was carried out using the NERC Biomolecular Analysis Facility Liverpool via award NBAF794.

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10.1111/1462-2920.16604Licence: Creative Commons: Attribution (CC BY)

PaliwalD2024MultipleFinal published version, 1.61 MBLicence: Creative Commons: Attribution (CC BY)

Predicting the emergence of host-adapted bacterial phytopathogens
Jackson, R.
Biotechnology & Biological Sciences Research Council
1/09/20 → 31/03/24
Project: Research Councils

Cite this

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title = "Multiple toxins and a protease contribute to the aphid-killing ability of Pseudomonas fluorescens PpR24",

abstract = "Aphids are globally important pests causing damage to a broad range of crops. Due to insecticide resistance, there is an urgent need to develop alternative control strategies. In our previous work, we found Pseudomonas fluorescens PpR24 can orally infect and kill the insecticide-resistant green-peach aphid (Myzus persicae). However, the genetic basis of the insecticidal capability of PpR24 remains unclear. Genome sequencing of PpR24 confirmed the presence of various insecticidal toxins such as Tc (toxin complexes), Rhs (rearrangement hotspot) elements, and other insect-killing proteases. Upon aphids infection with PpR24, RNA-Seq analysis revealed 193 aphid genes were differentially expressed with down-regulation of 16 detoxification genes. In addition, 1325 PpR24 genes (542 were upregulated and 783 downregulated) were subject to differential expression, including genes responsible for secondary metabolite biosynthesis, the iron-restriction response, oxidative stress resistance, and virulence factors. Single and double deletion of candidate virulence genes encoding a secreted protease (AprX) and four toxin components (two TcA-like; one TcB-like; one TcC-like insecticidal toxins) showed that all five genes contribute significantly to aphid killing, particularly AprX. This comprehensive host–pathogen transcriptomic analysis provides novel insight into the molecular basis of bacteria-mediated aphid mortality and the potential of PpR24 as an effective biocontrol agent.",

author = "Deepa Paliwal and Mojgan Rabiey and Mauchline, {Tim H.} and Keywan Hassani-Pak and Ralf Nauen and Carol Wagstaff and Simon Andrews and Chris Bass and Robert Jackson",

note = "Funding: D.P. was funded by the University of Reading and Bayer Crop Science. We acknowledge funding for M.R. and R.W.J. from BBSRC (BB/P006272/1) and a jointly funded grant from UKRI, Defra, and the Scottish Government, under the Strategic Priorities Fund Plant Bacterial Diseases programme (BB/T010568/1). T.H.M. acknowledges the BBSRC funded {\textquoteleft}Growing Health{\textquoteright} (BB/X010953/1) and {\textquoteleft}Soils to Nutrition{\textquoteright} (BBS/E/C/000I0310) Institute Strategic Programmes. An initial RNA seq experiment was carried out using the NERC Biomolecular Analysis Facility Liverpool via award NBAF794.",

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AU - Paliwal, Deepa

AU - Rabiey, Mojgan

AU - Mauchline, Tim H.

AU - Hassani-Pak, Keywan

AU - Nauen, Ralf

AU - Wagstaff, Carol

AU - Andrews, Simon

AU - Bass, Chris

AU - Jackson, Robert

N1 - Funding: D.P. was funded by the University of Reading and Bayer Crop Science. We acknowledge funding for M.R. and R.W.J. from BBSRC (BB/P006272/1) and a jointly funded grant from UKRI, Defra, and the Scottish Government, under the Strategic Priorities Fund Plant Bacterial Diseases programme (BB/T010568/1). T.H.M. acknowledges the BBSRC funded ‘Growing Health’ (BB/X010953/1) and ‘Soils to Nutrition’ (BBS/E/C/000I0310) Institute Strategic Programmes. An initial RNA seq experiment was carried out using the NERC Biomolecular Analysis Facility Liverpool via award NBAF794.

PY - 2024/4/1

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N2 - Aphids are globally important pests causing damage to a broad range of crops. Due to insecticide resistance, there is an urgent need to develop alternative control strategies. In our previous work, we found Pseudomonas fluorescens PpR24 can orally infect and kill the insecticide-resistant green-peach aphid (Myzus persicae). However, the genetic basis of the insecticidal capability of PpR24 remains unclear. Genome sequencing of PpR24 confirmed the presence of various insecticidal toxins such as Tc (toxin complexes), Rhs (rearrangement hotspot) elements, and other insect-killing proteases. Upon aphids infection with PpR24, RNA-Seq analysis revealed 193 aphid genes were differentially expressed with down-regulation of 16 detoxification genes. In addition, 1325 PpR24 genes (542 were upregulated and 783 downregulated) were subject to differential expression, including genes responsible for secondary metabolite biosynthesis, the iron-restriction response, oxidative stress resistance, and virulence factors. Single and double deletion of candidate virulence genes encoding a secreted protease (AprX) and four toxin components (two TcA-like; one TcB-like; one TcC-like insecticidal toxins) showed that all five genes contribute significantly to aphid killing, particularly AprX. This comprehensive host–pathogen transcriptomic analysis provides novel insight into the molecular basis of bacteria-mediated aphid mortality and the potential of PpR24 as an effective biocontrol agent.

AB - Aphids are globally important pests causing damage to a broad range of crops. Due to insecticide resistance, there is an urgent need to develop alternative control strategies. In our previous work, we found Pseudomonas fluorescens PpR24 can orally infect and kill the insecticide-resistant green-peach aphid (Myzus persicae). However, the genetic basis of the insecticidal capability of PpR24 remains unclear. Genome sequencing of PpR24 confirmed the presence of various insecticidal toxins such as Tc (toxin complexes), Rhs (rearrangement hotspot) elements, and other insect-killing proteases. Upon aphids infection with PpR24, RNA-Seq analysis revealed 193 aphid genes were differentially expressed with down-regulation of 16 detoxification genes. In addition, 1325 PpR24 genes (542 were upregulated and 783 downregulated) were subject to differential expression, including genes responsible for secondary metabolite biosynthesis, the iron-restriction response, oxidative stress resistance, and virulence factors. Single and double deletion of candidate virulence genes encoding a secreted protease (AprX) and four toxin components (two TcA-like; one TcB-like; one TcC-like insecticidal toxins) showed that all five genes contribute significantly to aphid killing, particularly AprX. This comprehensive host–pathogen transcriptomic analysis provides novel insight into the molecular basis of bacteria-mediated aphid mortality and the potential of PpR24 as an effective biocontrol agent.

U2 - 10.1111/1462-2920.16604

DO - 10.1111/1462-2920.16604

M3 - Article

C2 - 38561900

SN - 1462-2912

VL - 26

JO - Environmental Microbiology

JF - Environmental Microbiology

IS - 4

M1 - e16604

ER -

Multiple toxins and a protease contribute to the aphid-killing ability of Pseudomonas fluorescens PpR24

Abstract

Bibliographical note

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Projects

Predicting the emergence of host-adapted bacterial phytopathogens

Cite this