Multiple toxins and a protease contribute to the aphid-killing ability of Pseudomonas fluorescens PpR24.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
Apr 2024
Apr 2024
Historique:
received:
20
09
2023
accepted:
23
02
2024
medline:
2
4
2024
pubmed:
2
4
2024
entrez:
2
4
2024
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 38561900
doi: 10.1111/1462-2920.16604
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e16604Subventions
Organisme : University of Reading
Organisme : Bayer Crop Science
Organisme : BBSRC
ID : BB/P006272/1
Organisme : UKRI, Defra, and the Scottish Government, under the Strategic Priorities Fund Plant Bacterial Diseases programme
ID : BB/T010568/1
Organisme : BBSRC funded Growing Health
ID : BB/X010953/1
Organisme : Soils to Nutrition
ID : BBS/E/C/000I0310
Organisme : Institute Strategic Programmes
Organisme : NERC Biomolecular Analysis Facility Liverpool via award
ID : NBAF794
Informations de copyright
© 2024 The Authors. Environmental Microbiology published by John Wiley & Sons Ltd.
Références
Abe, A. (2009) Bacterial secretion systems: their function and contribution to disease process. Kansenshogaku Zasshi, 83, 94–100.
Alsohim, A.S., Taylor, T.B., Barrett, G.A., Gallie, J., Zhang, X.X., Altamirano‐Junqueira, A.E. et al. (2014) The biosurfactant viscosin produced by Pseudomonas fluorescens SBW25 aids spreading motility and plant growth promotion. Environmental Microbiology, 16, 2267–2281.
Amich, J., Schafferer, L., Haas, H. & Krappmann, S. (2013) Regulation of sulphur assimilation is essential for virulence and affects iron homeostasis of the human‐pathogenic mould Aspergillus fumigatus. PLoS Pathogens, 9, e1003573.
Bahlai, C.A., Xue, Y., Mccreary, C.M., Schaafsma, A.W. & Hallett, R.H. (2010) Choosing organic pesticides over synthetic pesticides may not effectively mitigate environmental risk in soybeans. PLoS One, 5, e11250.
Bansal, R., Mian, M.A.R., Mittapalli, O. & Michel, A.P. (2014) RNA‐Seq reveals a xenobiotic stress response in the soybean aphid, Aphis glycines, when fed aphid‐resistant soybean. BMC Genomics, 15, 972.
Bass, C., Puinean, A.M., Zimmer, C.T., Denholm, I., Field, L.M., Foster, S.P. et al. (2014) The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochemistry and Molecular Biology, 51, 41–51.
Basset, A., Tzou, P., Lemaitre, B. & Boccard, F. (2003) A single gene that promotes interaction of a phytopathogenic bacterium with its insect vector, Drosophila melanogaster. EMBO Reports, 4, 205–209.
Blackman R.L. & Eastop, E.L. (1994) Aphids on the world's crops: an identification and information guide, 2nd Edition, Wallingford: CAB International in association with the Natural History Museum.
Bowen, D., Rocheleau, T.A., Blackburn, M., Andreev, O., Golubeva, E., Bhartia, R. et al. (1998) Insecticidal toxins from the bacterium Photorhabdus luminescens. Science, 280, 2129–2132.
Boyd, E.F. & Hartl, D.L. (1998) Salmonella virulence plasmid. Modular acquisition of the spv virulence region by an F‐plasmid in Salmonella enterica subspecies I and insertion into the chromosome of subspecies II, IIIa, IV and VII isolates. Genetics, 149, 1183–1190.
Bronstein, P.A., Filiatrault, M.J., Myers, C.R., Rutzke, M., Schneider, D.J. & Cartinhour, S.W. (2008) Global transcriptional responses of Pseudomonas syringae DC3000 to changes in iron bioavailability in vitro. BMC Microbiology, 8, 209.
Brugirard‐Ricaud, K., Duchaud, E., Givaudan, A., Girard, P.A., Kunst, F., Boemare, N. et al. (2005) Site‐specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization. Cellular Microbiology, 7, 363–371.
Casilag, F., Lorenz, A., Krueger, J., Klawonn, F., Weiss, S. & Häussler, S. (2015) The LasB elastase of Pseudomonas aeruginosa acts in concert with alkaline protease apra to prevent flagellin‐mediated immune recognition. Infection and Immunity, 84, 162–171.
Chen, L., Zou, Y., She, P. & Wu, Y. (2015) Composition, function, and regulation of T6SS in Pseudomonas aeruginosa. Microbiological Research, 172, 19–25.
Choi, Y.S., Shin, D.H., Chung, I.Y., Kim, S.H., Heo, Y.J. & Cho, Y.H. (2007) Identification of Pseudomonas aeruginosa genes crucial for hydrogen peroxide resistance. Journal of Microbiology and Biotechnology, 17, 1344–1352.
Conesa, A. & Götz, S. (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics, 2008, 619832.
Cornelis, P., Wei, Q., Andrews, S.C. & Vinckx, T. (2011) Iron homeostasis and management of oxidative stress response in bacteria. Metallomics, 3, 540–549.
Cornelissen, C.N. (2003) Transferrin‐iron uptake by gram‐negative bacteria. Frontiers in Bioscience, 8, d836–d847.
Correa, V.R., Majerczak, D.R., Ammar El, D., Merighi, M., Pratt, R.C., Hogenhout, S.A. et al. (2012) The bacterium Pantoea stewartii uses two different type III secretion systems to colonize its plant host and insect vector. Applied and Environmental Microbiology, 78, 6327–6336.
Costechareyre, D., Balmand, S., Condemine, G. & Rahbé, Y. (2012) Dickeya dadantii, a plant pathogenic bacterium producing Cyt‐like entomotoxins, causes septicemia in the pea aphid Acyrthosiphon pisum. PLoS One, 7, e30702.
Cristofoletti, P.T., De Sousa, F.A.M., Rahbé, Y. & Terra, W.R. (2006) Characterization of a membrane‐bound aminopeptidase purified from Acyrthosiphon pisum midgut cells. A major binding site for toxic mannose lectins. The FEBS Journal, 273, 5574–5588.
Cristofoletti, P.T., Ribeiro, A.F., Deraison, C., Rahbé, Y. & Terra, W.R. (2003) Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. Journal of Insect Physiology, 49, 11–24.
Davis, M.M. & Engström, Y. (2012) Immune response in the barrier epithelia: lessons from the fruit fly Drosophila melanogaster. Journal of Innate Immunity, 4, 273–283.
De Gregorio, E., Spellman, P.T., Rubin, G.M. & Lemaitre, B. (2001) Genome‐wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proceedings of the National Academy of Sciences of the United States of America, 98, 12590–12595.
Dedryver, C.‐A., Le Ralec, A. & Fabre, F. (2010) The conflicting relationships between aphids and men: a review of aphid damage and control strategies. Comptes Rendus Biologies, 333, 539–553.
Duchaud, E., Rusniok, C., Frangeul, L., Buchrieser, C., Givaudan, A., Taourit, S. et al. (2003) The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nature Biotechnology, 21, 1307–1313.
Dutta, S., Yu, S.M., Jeong, S.C. & Lee, Y.H. (2020) High‐throughput analysis of genes involved in biocontrol performance of Pseudomonas fluorescens NBC275 against Gray mold. Journal of Applied Microbiology, 128, 265–279.
Filloux, A. (2011) Protein secretion systems in Pseudomonas aeruginosa: an essay on diversity, evolution, and function. Frontiers in Microbiology, 2, 155.
Flury, P., Aellen, N., Ruffner, B., Péchy‐Tarr, M., Fataar, S., Metla, Z. et al. (2016) Insect pathogenicity in plant‐beneficial pseudomonads: phylogenetic distribution and comparative genomics. The ISME Journal, 10, 2527–2542.
Flury, P., Vesga, P., Dominguez‐Ferreras, A., Tinguely, C., Ullrich, C.I., Kleespies, R.G. et al. (2019) Persistence of root‐colonizing Pseudomonas protegens in herbivorous insects throughout different developmental stages and dispersal to new host plants. The ISME Journal, 13, 860–872.
Flury, P., Vesga, P., Péchy‐Tarr, M., Aellen, N., Dennert, F., Hofer, N. et al. (2017) Antimicrobial and insecticidal: cyclic lipopeptides and hydrogen cyanide produced by plant‐beneficial pseudomonas strains CHA0, CMR12a, and PCL1391 contribute to insect killing. Frontiers in Microbiology, 8, 100.
Gallagher, L.A. & Manoil, C. (2001) Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. Journal of Bacteriology, 183, 6207–6214.
Garrido‐Sanz, D., Vesga, P., Heiman, C.M., Altenried, A., Keel, C. & Vacheron, J. (2023) Relation of pest insect‐killing and soilborne pathogen‐inhibition abilities to species diversification in environmental Pseudomonas protegens. The ISME Journal, 17, 1369–1381.
Gerardo, N.M., Altincicek, B., Anselme, C., Atamian, H., Barribeau, S.M., De Vos, M. et al. (2010) Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biology, 11, R21.
Gotoh, H., Okada, N., Kim, Y.‐G., Shiraishi, K., Hirami, N., Haneda, T. et al. (2003) Extracellular secretion of the virulence plasmid‐encoded ADP‐ribosyltransferase SpvB in Salmonella. Microbial Pathogenesis, 34, 227–238.
Guo, J., Jing, X., Peng, W.‐L., Nie, Q., Zhai, Y., Shao, Z. et al. (2016) Comparative genomic and functional analyses: unearthing the diversity and specificity of nematicidal factors in Pseudomonas putida strain 1A00316. Scientific Reports, 6, 29211.
Haas, D. & Défago, G. (2005) Biological control of soil‐borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology, 3, 307–319.
Haas, D. & Keel, C. (2003) Regulation of antibiotic production in root‐colonizing Peudomonas spp. and relevance for biological control of plant disease. Annual Review of Phytopathology, 41, 117–153.
Hassett, D.J., Howell, M.L., Sokol, P.A., Vasil, M.L. & Dean, G.E. (1997) Fumarase C activity is elevated in response to iron deprivation and in mucoid, alginate‐producing Pseudomonas aeruginosa: cloning and characterization of fumC and purification of native fumC. Journal of Bacteriology, 179, 1442–1451.
Hillyer, J.F. (2016) Insect immunology and hematopoiesis. Developmental and Comparative Immunology, 58, 102–118.
Hou, Y.‐J., Banerjee, R., Thomas, B., Nathan, C., García‐Sastre, A., Ding, A. et al. (2013) SARM is required for neuronal injury and cytokine production in response to central nervous system viral infection. Journal of Immunology (Baltimore, MD: 1950), 191, 875–883.
Horton, R.M., Cai, Z., Ho, S.M. & Pease, L.R. (1990) Gene splicing by overlap extension: tailor‐made genes using the polymerase chain reaction. Biotechniques, 8(5), 528–535.
Huang, X., Dai, J., Fournier, J., Ali, A.M., Zhang, Q. & Frenkel, K. (2002) Ferrous ion autoxidation and its chelation in iron‐loaded human liver HepG2 cells. Free Radical Biology and Medicine, 32, 84–92.
Irving, P., Troxler, L., Heuer, T.S., Belvin, M., Kopczynski, C., Reichhart, J.M. et al. (2001) A genome‐wide analysis of immune responses in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 98, 15119–15124.
Jackson, A.P., Thomas, G.H., Parkhill, J. & Thomson, N.R. (2009) Evolutionary diversification of an ancient gene family (rhs) through C‐terminal displacement. BMC Genomics, 10, 584.
Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., Mcginnis, S. & Madden, T.L. (2008) NCBI BLAST: a better web interface. Nucleic Acids Research, 36, W5–W9.
Jousset, A., Rochat, L., Lanoue, A., Bonkowski, M., Keel, C. & Scheu, S. (2011) Plants respond to pathogen infection by enhancing the antifungal gene expression of root‐associated bacteria. Molecular Plant‐Microbe Interactions, 24, 352–358.
Kamilova, F., Validov, S., Azarova, T., Mulders, I. & Lugtenberg, B. (2005) Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environmental Microbiology, 7, 1809–1817.
Kammler, M., Schön, C. & Hantke, K. (1993) Characterization of the ferrous iron uptake system of Escherichia coli. Journal of Bacteriology, 175, 6212–6219.
Kang, Y.‐S., Lee, Y., Jung, H., Jeon, C.O., Madsen, E.L. & Park, W. (2007) Overexpressing antioxidant enzymes enhances naphthalene biodegradation in Pseudomonas sp. strain As1. Microbiology, 153, 3246–3254.
Kawakami, T., Kuroki, M., Ishii, M., Igarashi, Y. & Arai, H. (2009) Differential expression of multiple terminal oxidases for aerobic respiration in Pseudomonas aeruginosa. Environmental Microbiology, 12(6), 1399–1412.
Keel, C. (2016) A look into the toolbox of multi‐talents: insect pathogenicity determinants of plant‐beneficial pseudomonads. Environmental Microbiology, 18, 3207–3209.
King, E.O., Ward, M.K. & Raney, D.E. (1954) Two simple media for the demonstration of pyocyanin and fluorescin. The Journal of Laboratory and Clinical Medicine, 44, 301–307.
Kunert, G. & Weisser, W.W. (2003) The interplay between density‐ and trait‐mediated effects in predator‐prey interactions: a case study in aphid wing polymorphism. Oecologia, 135, 304–312.
Kutsukake, M., Shibao, H., Nikoh, N., Morioka, M., Tamura, T., Hoshino, T. et al. (2004) Venomous protease of aphid soldier for colony defense. Proceedings of the National Academy of Sciences of the United States of America, 101, 11338–11343.
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. (2009) Ultrafast and memory‐efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25.
Liehl, P., Blight, M., Vodovar, N., Boccard, F. & Lemaitre, B. (2006) Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model. PLoS Pathogens, 2, e56.
Lim, C.K., Hassan, K.A., Tetu, S.G., Loper, J.E. & Paulsen, I.T. (2012) The effect of iron limitation on the transcriptome and proteome of Pseudomonas fluorescens Pf‐5. PLoS One, 7, e39139.
Lin, X., Ruiz, J., Bajraktari, I., Ohman, R., Banerjee, S., Gribble, K. et al. (2014) Z‐disc‐associated, alternatively spliced, PDZ motif‐containing protein (ZASP) mutations in the actin‐binding domain cause disruption of skeletal muscle actin filaments in myofibrillar myopathy. The Journal of Biological Chemistry, 289, 13615–13626.
Liu, K., Knabel, S.J. & Dudley, E.G. (2009) rhs genes are potential markers for multilocus sequence typing of Escherichia coli O157:H7 strains. Applied and Environmental Microbiology, 75, 5853–5862.
Loper, J.E., Henkels, M.D., Rangel, L.I., Olcott, M.H., Walker, F.L., Bond, K.L. et al. (2016) Rhizoxin analogs, orfamide A and chitinase production contribute to the toxicity of Pseudomonas protegens strain Pf‐5 to Drosophila melanogaster. Environmental Microbiology, 18, 3509–3521.
Lugtenberg, B. & Kamilova, F. (2009) Plant‐growth‐promoting rhizobacteria. Annual Review of Microbiology, 63, 541–556.
Ma, J.F., Ochsner, U.A., Klotz, M.G., Nanayakkara, V.K., Howell, M.L., Johnson, Z. et al. (1999) Bacterioferritin A modulates catalase A (KatA) activity and resistance to hydrogen peroxide in Pseudomonas aeruginosa. Journal of Bacteriology, 181, 3730–3742.
Marmaras, V.J., Bournazos, S.N., Katsoris, P.G. & Lambropoulou, M. (1993) Defense mechanisms in insects: certain integumental proteins and tyrosinase are responsible for nonself‐recognition and immobilization of Escherichia coli in the cuticle of developing Ceratitis capitata. Archives of Insect Biochemistry and Physiology, 23, 169–180.
Mercado‐Blanco, J. & Bakker, P.A. (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek, 92, 367–389.
Merlin, C., Mcateer, S. & Masters, M. (2002) Tools for characterization of Escherichia coli genes of unknown function. Journal of Bacteriology, 184, 4573–4581.
Miller, J.H. (1972) Experiments in molecular genetics. Cold Spring Harbor: Cold Spring Harbor Laboratory.
Miyata, S., Casey, M., Frank, D.W., Ausubel, F.M. & Drenkard, E. (2003) Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infection and Immunity, 71, 2404–2413.
Moir, M.L., Renton, M., Hoffmann, B.D., Leng, M.C. & Lach, L. (2018) Development and testing of a standardized method to estimate honeydew production. PLoS One, 13, e0201845.
Morel, V., Lepicard, S., Rey, A., Parmentier, M.‐L. & Schaeffer, L. (2014) Drosophila Nesprin‐1 controls glutamate receptor density at neuromuscular junctions. Cellular and Molecular Life Sciences, 71, 3363–3379.
Nappi, A.J. & Vass, E. (2000) Iron, metalloenzymes and cytotoxic reactions. Cellular and Molecular Biology (Noisy‐le‐Grand, France), 46, 637–647.
Nehme, N.T., Liégeois, S., Kele, B., Giammarinaro, P., Pradel, E., Hoffmann, J.A. et al. (2007) A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathogens, 3, e173.
Noinaj, N., Buchanan, S.K. & Cornelissen, C.N. (2012) The transferrin‐iron import system from pathogenic Neisseria species. Molecular Microbiology, 86, 246–257.
Ochsner, U.A., Vasil, M.L., Alsabbagh, E., Parvatiyar, K. & Hassett, D.J. (2000) Role of the Pseudomonas aeruginosa oxyR‐recG operon in oxidative stress defense and DNA repair: OxyR‐dependent regulation of katB‐ankb, ahpb, and ahpC‐ahpF. Journal of Bacteriology, 182, 4533–4544.
Olcott, M.H., Henkels, M.D., Rosen, K.L., Walker, F.L., Sneh, B., Loper, J.E. et al. (2010) Lethality and developmental delay in Drosophila melanogaster larvae after ingestion of selected Pseudomonas fluorescens strains. PLoS One, 5, e12504.
Pal, S., Wu, J. & Wu, L.P. (2008) Microarray analyses reveal distinct roles for Rel proteins in the Drosophila immune response. Developmental and Comparative Immunology, 32, 50–60.
Paliwal, D., Hamilton, A.J., Barrett, G.A., Alberti, F., Van Emden, H., Monteil, C.L. et al. (2022) Identification of novel aphid‐killing bacteria to protect plants. Microbial Biotechnology, 15, 1203–1220.
Palma, M., Worgall, S. & Quadri, L.E.N. (2003) Transcriptome analysis of the Pseudomonas aeruginosa response to iron. Archives of Microbiology, 180, 374–379.
Paulsen, I.T., Press, C.M., Ravel, J., Kobayashi, D.Y., Myers, G.S.A., Mavrodi, D.V. et al. (2005) Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf‐5. Nature Biotechnology, 23, 873–878.
Polack, B.T., Dacheux, D., Delic‐Attree, I., Toussaint, B. & Vignais, P.M. (1996) The Pseudomonas aeruginosa fumcandsoda genes belong to an iron‐responsive operon. Biochemical and Biophysical Research Communications, 226, 555–560.
Preston, G.M., Bertrand, N. & Rainey, P.B. (2001) Type III secretion in plant growth‐promoting Pseudomonas fluorescens SBW25. Molecular Microbiology, 41, 999–1014.
Puca, L. & Brou, C. (2014) α‐Arrestins – new players in Notch and GPCR signaling pathways in mammals. Journal of Cell Science, 127, 1359–1367.
Raaijmakers, J.M., De Bruijn, I., Nybroe, O. & Ongena, M. (2010) Natural functions of lipopeptides from Bacillusi and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiology Reviews, 34, 1037–1062.
Rispe, C., Kutsukake, M., Doublet, V., Hudaverdian, S., Legeai, F., Simon, J.C. et al. (2007) Large gene family expansion and variable selective pressures for cathepsin B in aphids. Molecular Biology and Evolution, 25, 5–17.
Ruffner, B., Péchy‐Tarr, M., Höfte, M., Bloemberg, G., Grunder, J., Keel, C. et al. (2015) Evolutionary patchwork of an insecticidal toxin shared between plant‐associated pseudomonads and the insect pathogens Photorhabdus and Xenorhabdus. BMC Genomics, 16, 609.
Sapountzis, P., Duport, G., Balmand, S., Gaget, K., Jaubert‐Possamai, S., Febvay, G. et al. (2014) New insight into the RNA interference response against cathepsin‐L gene in the pea aphid, Acyrthosiphon pisum: molting or gut phenotypes specifically induced by injection or feeding treatments. Insect Biochemistry and Molecular Biology, 51, 20–32.
Sarwan, K. (2019) Aphid‐plant interactions: implications for pest management. In: Manuel, T.O., Feyza, C. & Anabela, F.‐S. (Eds.) Plant communities and their environment. Rijeka: IntechOpen.
Schmidt, M.H., Lauer, A., Purtauf, T., Thies, C., Schaefer, M. & Tscharntke, T. (2003) Relative importance of predators and parasitoids for cereal aphid control. Proceedings of the Royal Society of London Series B–Biological Sciences, 270, 1905–1909.
Spink, J.M., Pullinger, G.D., Wood, M.W. & Lax, A.J. (1994) Regulation of spvr, the positive regulatory gene of Salmonella plasmid virulence genes. FEMS Microbiology Letters, 116, 113–121.
Stavrinides, J., Mccloskey, J.K. & Ochman, H. (2009) Pea aphid as both host and vector for the phytopathogenic bacterium Pseudomonas syringae. Applied and Environmental Microbiology, 75, 2230–2235.
Stavrinides, J., No, A. & Ochman, H. (2010) A single genetic locus in the phytopathogen Pantoea stewartiii enables gut colonization and pathogenicity in an insect host. Environmental Microbiology, 12, 147–155.
Touati, D. (2000) Iron and oxidative stress in bacteria. Archives of Biochemistry and Biophysics, 373, 1–6.
Town, J., Cui, N., Audy, P., Boyetchko, S. & Dumonceaux, T.J. (2016) Improved high‐quality draft genome sequence of Pseudomonas fluorescens KENGFT3. Genome Announcements, 4, e00428‐16.
Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., Van Baren, M.J. et al. (2010) Transcript assembly and quantification by RNA‐Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28, 511–515.
Vacheron, J., Péchy‐Tarr, M., Brochet, S., Heiman, C.M., Stojiljkovic, M., Maurhofer, M. et al. (2019) T6SS contributes to gut microbiome invasion and killing of an herbivorous pest insect by plant‐beneficial Pseudomonas protegens. The ISME Journal, 13, 1318–1329.
Van Emden, H.F. & Wild, E.A. (2020) A fully defined artificial diet for Myzus persicae – the detailed technical manual. Entomologia Experimentalis et Applicata, 168, 582–586.
Vesga, P., Augustiny, E., Keel, C., Maurhofer, M. & Vacheron, J. (2021) Phylogenetically closely related pseudomonads isolated from arthropods exhibit differential insect‐killing abilities and genetic variations in insecticidal factors. Environmental Microbiology, 23, 5378–5394.
Vesga, P., Flury, P., Vacheron, J., Keel, C., Croll, D. & Maurhofer, M. (2020) Transcriptome plasticity underlying plant root colonization and insect invasion by Pseudomonas protegens. The ISME Journal, 14, 2766–2782.
Vodovar, N., Vallenet, D., Cruveiller, S., Rouy, Z., Barbe, V., Acosta, C. et al. (2006) Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila. Nature Biotechnology, 24, 673–679.
Vodovar, N., Vinals, M., Liehl, P., Basset, A., Degrouard, J., Spellman, P. et al. (2005) Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proceedings of the National Academy of Sciences of the United States of America, 102, 11414–11419.
Von Morgen, P., Hořejší, Z. & Macurek, L. (2015) Substrate recognition and function of the R2TP complex in response to cellular stress. Frontiers in Genetics, 6, 69.
Walker, K.A., Maltez, V.I., Hall, J.D., Vitko, N.P. & Miller, V.L. (2013) A phenotype at last: essential role for the Yersinia enterocolitica Ysa type III secretion system in a Drosophila melanogaster S2 cell model. Infection and Immunity, 81, 2478–2487.
Wang, L.F., Chai, L.Q., He, H.J., Wang, Q., Wang, J.X. & Zhao, X.F. (2010) A cathepsin L‐like proteinase is involved in moulting and metamorphosis in Helicoverpa armigera. Insect Molecular Biology, 19, 99–111.
Waterfield, N.R., Bowen, D.J., Fetherston, J.D., Perry, R.D. & Ffrench‐Constant, R.H. (2001) The tc genes of Photorhabdus: a growing family. Trends in Microbiology, 9, 185–191.
Waterhouse, R.M., Povelones, M. & Christophides, G.K. (2010) Sequence‐structure‐function relations of the mosquito leucine‐rich repeat immune proteins. BMC Genomics, 11, 531.
Yan, Q., Philmus, B., Chang, J.H. & Loper, J.E. (2017) Novel mechanism of metabolic co‐regulation coordinates the biosynthesis of secondary metabolites in Pseudomonas protegens. eLife, 6, e22835.
Yang, G. & Waterfield, N.R. (2013) The role of TcdB and TccC subunits in secretion of the Photorhabdus Tcd toxin complex. PLoS Pathogens, 9, e1003644.
Yao, H., Jepkorir, G., Lovell, S., Nama, P.V., Weeratunga, S., Battaile, K.P. et al. (2011) Two distinct ferritin‐like molecules in Pseudomonas aeruginosa: the product of the bfrA gene is a bacterial ferritin (FtnA) and not a bacterioferritin (Bfr). Biochemistry, 50, 5236–5248.
Ye, X.‐D., Su, Y.‐L., Zhao, Q.‐Y., Xia, W.‐Q., Liu, S.‐S. & Wang, X.‐W. (2014) Transcriptomic analyses reveal the adaptive features and biological differences of guts from two invasive whitefly species. BMC Genomics, 15, 370.
Zerbino, D.R. (2010) Using the Velvet de novo assembler for short‐read sequencing technologies. Current Protocols in Bioinformatics Chapter 11, Unit 11.5. https://doi.org/10.1002/0471250953.bi1105s31