Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids

Serteyn, Laurent; Quaghebeur, Céleste; Ongena, Marc; Cabrera, Nuri; Barrera, Andrea; Molina-Montenegro, Marco; Francis, Frédéric; Ramirez, Claudio

doi:10.3390/insects11040234

Article (Scientific journals)

Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids

Serteyn, Laurent; Quaghebeur, Céleste; Ongena, Marc et al.

2020 • In Insects, 11 (4)

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/248420

DOI
10.3390/insects11040234

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Serteyn et al. 2020 - PGPR ISR A. pisum.pdf

Publisher postprint (1.9 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Acyrthosiphon pisum; Bacillus amyloliquefaciens; electropenetrography; Hamiltonella defensa; interactions; plant growth-promoting rhizobacteria; Vicia faba

Abstract :

[en] The effects of microorganisms on plant-insect interactions have usually been underestimated. While plant growth-promoting rhizobacteria (PGPR) are known to induce plant defenses, endosymbiotic bacteria hosted by herbivorous insects are often beneficial to the host. Here, we aimed to assess whether PGPR-induced defenses in broad bean plants impact the pea aphid, depending on its genotype and the presence of endosymbionts. We estimated aphid reproduction, quantified defense- and growth-related phytohormones by GC-MS, and measured different plant growth and physiology parameters, after PGPR treatment. In addition, we recorded the feeding behavior of aphids by electropenetrography. We found that the PGPR treatment of broad bean plants reduced the reproduction of one of the pea aphid clones. We highlighted a phenomenon of PGPR-induced plant defense priming, but no noticeable plant growth promotion. The main changes in aphid probing behavior were related to salivation events into phloem sieve elements. We suggest that the endosymbiont Hamiltonella defensa played a key role in plant-insect interactions, possibly helping aphids to counteract plant-induced resistance and allowing them to develop normally on PGPR-treated plants. Our results imply that plant- and aphid-associated microorganisms add greater complexity to the outcomes of aphid-plant interactions.

Disciplines :

Entomology & pest control

Author, co-author :

Serteyn, Laurent ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Quaghebeur, Céleste

Ongena, Marc ; Université de Liège - ULiège > Département GxABT > Microbial, food and biobased technologies

Cabrera, Nuri

Barrera, Andrea

Molina-Montenegro, Marco

Francis, Frédéric ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Ramirez, Claudio

Language :

English

Title :

Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids

Publication date :

08 April 2020

Journal title :

Insects

eISSN :

2075-4450

Publisher :

Multidisciplinary Digital Publishing Institute (MDPI), Switzerland

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.mdpi.com/2075-4450/11/4/234?utm_source=releaseissue&utm_medium=email&utm_campaign=releaseissue_insects&utm_term=doilink30

Available on ORBi :

since 11 June 2020

Statistics

Number of views

118 (28 by ULiège)

Number of downloads

89 (16 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Hartmann, A.; Rothballer, M.; Schmid, M. Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 2008, 312, 7-14.
Dardanelli, M.S.; Medeot, D.B.; Paulucci, N.S.; Bueno, M.A.; Vicario, J.C.; García, M.; Bensi, N.H.; Niebylski, A.M. Biochemical Processes of Rhizobacteria and Their Application in Biotechnology; Malik, A., Grohmann, E., Eds.; Springer: Berlin/Heidelberg, Germany, 2012; ISBN 9789400715912.
Kloepper, J.W.; Rodríguez-Kábana, R.; Zehnder, G.W.; Murphy, J.F.; Sikora, E.; Fernández, C. Plant root-bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Australas. Plant Pathol. 1999, 28, 21-26.
Ramamoorthy, V.; Viswanathan, R.; Raguchander, T.; Prakasam, V.; Samiyappan, R. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Prot. 2001, 20, 1-11.
Walters, D.; Heil, M. Costs and trade-offs associated with induced resistance. Physiol. Mol. Plant Pathol. 2007, 71, 3-17.
Ongena, M.; Jacques, P. Bacillus lipopeptides: Versatile weapons for plant disease biocontrol. Trends Microbiol.2008, 16, 115-125.
Fan, B.; Blom, J.; Klenk, H.P.; Borriss, R. Bacillus amyloliquefaciens, Bacillus velezensis, and Bacillus siamensis form an “Operational group B. amyloliquefaciens” within the B. subtilis species complex. Front. Microbiol.2017, 8, 1-15.
Matilla, M.; Krell, T. Plant growth promotion and biocontrol mediated by plant-associated bacteria BT. In Plant Microbiome: Stress Response; Egamberdieva, D., Ahmad, P., Eds.; Springer: Berlin/Heidelberg, Germany, 2018; pp. 45-80.
Chowdhury, S.P.; Hartmann, A.; Gao, X.W.; Borriss, R. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42-A review. Front. Microbiol. 2015, 6, 1-11.
Zehnder, G.; Kloepper, J.; Tuzun, S.; Yao, C.;Wei, G.; Chambliss, O.; Shelby, R. Insect feeding on cucumber mediated by rhizobacteria-induced plant resistance. Entomol. Exp. Appl. 1997, 83, 81-85.
Van der Ent, S.; Van Wees, S.C.M.; Pieterse, C.M.J. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 2009, 70, 1581-1588.
Song, G.C.; Ryu, C.M. Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int. J. Mol. Sci. 2013, 14, 9803-9819.
Conrath, U.; Pieterse, C.M.J.; Mauch-mani, B. Priming in plant-pathogen interactions. Trends Plant Sci. 2002, 7, 210-216.
Choudhary, D.K.; Johri, B.N. Interactions of Bacillus spp. and plants-With special reference to induced systemic resistance (ISR). Microbiol. Res. 2009, 164, 493-513.
Van Peer, R.; Niemann, G.J.; Schippers, B. Induced resistance and phytoalexin accumulation in biological control of Fusarium Wilt of Carnation by Pseudomonas sp. Strain WCS417r. Phytopathology 1991, 81, 728-734.
Pastor, V.; Luna, E.; Mauch-Mani, B.; Ton, J.; Flors, V. Primed plants do not forget. Environ. Exp. Bot. 2012, 94, 46-56.
Fahimi, A.; Ashouri, A.; Ahmadzadeh, M.; Hoseini Naveh, V.; Asgharzadeh, A.; Maleki, F.; Felton, G.W. Effect of PGPR on population growth parameters of cotton aphid. Arch. Phytopathol. Plant Prot. 2014, 47, 1274-1285.
Disi, J.O.; Zebelo, S.; Kloepper, J.W.; Fadamiro, H. Seed inoculation with beneficial rhizobacteria affects European corn borer (Lepidoptera: Pyralidae) oviposition on maize plants. Entomol. Sci. 2018, 21, 48-58.
Hogenhout, S.A.; Ammar, E.-D.; Whitfield, A.E.; Redinbaugh, M.G. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 2008, 46, 327-359.
Peccoud, J.; Figueroa, C.C.; Silva, A.X.; Ramirez, C.C.; Mieuzet, L.; Bonhomme, J.; Stoeckel, S.; Plantagenest, M.; Simon, J.-C. Host range expansion of an introduced insect pest through multiple colonizations of specialized clones. Mol. Ecol. 2008, 17, 4608-4618.
Guyomar, C.; Legeai, F.; Jousselin, E.; Mougel, C.; Lemaitre, C.; Simon, J.C. Multi-scale characterization of symbiont diversity in the pea aphid complex through metagenomic approaches. Microbiome 2018, 6, 1-21.
Guo, J.; Hatt, S.; He, K.; Chen, J.; Francis, F.;Wang, Z. Nine facultative endosymbionts in aphids. A review. J. Asia Pac. Entomol. 2017, 20, 794-801.
Su, Q.; Oliver, K.M.; Xie, W.; Wu, Q.; Wang, S.; Zhang, Y. The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato. Funct. Ecol. 2015, 29, 1007-1018.
Oliver, K.M.; Degnan, P.H.; Hunter, M.S.; Moran, N.A. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science (80-) 2009, 325, 992-994.
Frago, E.; Mala, M.; Weldegergis, B.T.; Yang, C.; McLean, A.; Godfray, H.C.J.; Gols, R.; Dicke, M. Symbionts protect aphids from parasitic wasps by attenuating herbivore-induced plant volatiles. Nat. Commun. 2017, 8, 1-9.
Angelella, G.; Nalam, V.; Nachappa, P.; White, J.; Kaplan, I. Endosymbionts differentially alter exploratory probing behavior of a nonpersistent plant virus vector. Microb. Ecol. 2018, 76, 453-458.
Hackett, S.C.; Karley, A.J.; Bennett, A.E. Unpredicted impacts of insect endosymbionts on interactions between soil organisms, plants and aphids. Proc. R. Soc. B Biol. Sci. 2013, 280, 20131275.
Dunlap, C.A.; Kim, S.J.; Kwon, S.W.; Rooney, A.P. Bacillus velezensis is not a later heterotypic synonym of Bacillus amyloliquefaciens; Bacillus methylotrophicus, Bacillus amyloliquefaciens subsp. Plantarum and ‘Bacillus oryzicola’ are later heterotypic synonyms of Bacillus velezensis based on phylogenom. Int. J. Syst. Evol. Microbiol.2016, 66, 1212-1217.
Schuelke, M. An economic method for the fluorescent labeling of PCR fragments. Nat. Biotechnol. 2000, 18, 233-234.
Borodovsky, M.; McIninch, J. GenMark: Parallel gene recognition for both DNA strands. Comput. Chem.1993, 17, 123-133.
Peccoud, J.; Bonhomme, J.; Mahéo, F.; de la Huerta, M.; Cosson, O.; Simon, J.C. Inheritance patterns of secondary symbionts during sexual reproduction of pea aphid biotypes. Insect Sci. 2014, 21, 291-300.
Ramos, P.; Rivas, N.; Pollmann, S.; Casati, P.; Molina-Montenegro, M.A. Hormonal and physiological changes driven by fungal endophytes increase Antarctic plant performance under UV-B radiation. Fungal Ecol. 2018, 34, 76-82.
Carrasco Loba, V.; Pérez Alonso, M.-M.; Pollmann, S. Monitoring of crosstalk between jasmonate and auxin in the framework of plant stress responses of roots. In Auxins and Cytokinins in Plant Biology: Methods and Protocols; Dandekar, T., Naseem, M., Eds.; Humana Press: New York, NY, USA, 2017; pp. 175-185, ISBN 978-1-4939-6829-9.
Manschadi, A.M.; Sauerborn, J.; Stützel, H.; Göbel,W.; Saxena, M.C. Simulation of faba bean (Vicia faba L.) root system development under Mediterranean conditions. Eur. J. Agron. 1998, 9, 259-272.
Adasme-Carreño, F.; Muñoz-Gutiérrez, C.; Salinas-Cornejo, J.; Ramírez, C.C. A2EPG: A new software for the analysis of electrical penetration graphs to study plant probing behaviour of hemipteran insects. Comput. Electron. Agric. 2015, 113, 128-135.
Sarria, E.; Cid, M.; Garzo, E.; Fereres, A. ExcelWorkbook for automatic parameter calculation of EPG data. Comput. Electron. Agric. 2009, 67, 35-42.
Buensanteai, N.; Yuen, G.Y.; Prathuangwong, S. Priming, signaling, and protein production associated with induced resistance by Bacillus amyloliquefaciens KPS46. World J. Microbiol. Biotechnol. 2009, 25, 1275-1286.
Beris, D.; Theologidis, I.; Skandalis, N.; Vassilakos, N. Bacillus amyloliquefaciens strain MBI600 induces salicylic acid dependent resistance in tomato plants against Tomato spotted wilt virus and Potato virus y. Sci. Rep.2018, 8, 1-11.
Asari, S.; Ongena, M.; Debois, D.; De Pauw, E.; Chen, K.; Bejai, S.; Meijer, J. Insights into the molecular basis of biocontrol of Brassica pathogens by Bacillus amyloliquefaciens UCMB5113 lipopeptides. Ann. Bot. 2017, 120, 551-562.
Brock, A.K.; Berger, B.; Schreiner, M.; Ruppel, S.; Mewis, I. Plant growth-promoting bacteria Kosakonia radicincitans mediate anti-herbivore defense in Arabidopsis thaliana. Planta 2018, 248, 1383-1392.
Xie, S.; Jiang, H.; Ding, T.; Xu, Q.; Chai, W.; Cheng, B. Bacillus amyloliquefaciens FZB42 represses plant miR846 to induce systemic resistance via a jasmonic acid-dependent signalling pathway. Mol. Plant Pathol. 2018, 19, 1612-1623.
Kloth, K.J.; Wiegers, G.L.; Busscher-Lange, J.; Van Haarst, J.C.; Kruijer, W.; Bouwmeester, H.J.; Dicke, M.; Jongsma, M.A. AtWRKY22 promotes susceptibility to aphids and modulates salicylic acid and jasmonic acid signalling. J. Exp. Bot. 2016, 67, 3383-3396.
Herman, M.A.B.; Nault, B.A.; Smart, C.D. Effects of plant growth-promoting rhizobacteria on bell pepper production and green peach aphid infestations in New York. Crop Prot. 2008, 27, 996-1002.
Boutard-Hunt, C.; Smart, C.D.; Thaler, J.; Nault, B.A. Impact of plant growth-promoting rhizobacteria and natural enemies on Myzus persicae (Hemiptera: Aphididae) infestations in pepper. J. Econ. Entomol. 2009, 102, 2183-2191.
Martinuz, A.; Schouten, A.; Menjivar, R.D.; Sikora, R.A. Effectiveness of systemic resistance toward Aphis gossypii (Hom., Aphididae) as induced by combined applications of the endophytes Fusarium oxysporum Fo162 and Rhizobium etli G12. Biol. Control 2012, 62, 206-212.
Gadhave, K.R.; Gange, A.C. Plant-associated Bacillus spp. alter life-history traits of the specialist insect Brevicoryne brassicae L. Agric. For. Entomol. 2016, 18, 35-42.
Naeem, M.; Aslam, Z.; Khaliq, A.; Ahmed, J.N.; Nawaz, A.; Hussain, M. Plant growth promoting rhizobacteria reduce aphid population and enhance the productivity of bread wheat. Braz. J. Microbiol. 2018, 49, 9-14.
Pineda, A.; Zheng, S.J.; van Loon, J.J.A.; Dicke, M. Rhizobacteria modify plant-aphid interactions: A case of induced systemic susceptibility. Plant Biol. 2012, 14, 83-90.
Blubaugh, C.K.; Carpenter-Boggs, L.; Reganold, J.P.; Schaeffer, R.N.; Snyder,W.E. Bacteria and competing herbivores weaken top-down and bottom-up aphid suppression. Front. Plant Sci. 2018, 9, 1-10.
Stewart, S.A.; Hodge, S.; Bennett, M.; Mansfield, J.W.; Powell, G. Aphid induction of phytohormones in Medicago truncatula is dependent upon time post-infestation, aphid density and the genotypes of both plant and insect. Arthropod Plant Interact. 2016, 10, 41-53.
Oliver, K.M.; Higashi, C.H. Variations on a protective theme: Hamiltonella defensa infections in aphids variably impact parasitoid success. Curr. Opin. Insect Sci. 2019, 32, 1-7.
Sochard, C.; Morlière, S.; Toussaint, G.; Outreman, Y.; Sugio, A.; Simon, J.C. Examination of the success rate of secondary symbiont manipulation by microinjection methods in the pea aphid system. Entomol. Exp. Appl.2020, 1-10.
Blakeslee, J.J.; Spatola Rossi, T.; Kriechbaumer, V. Auxin biosynthesis: Spatial regulation and adaptation to stress. J. Exp. Bot. 2019, 70, 5041-5049.
Kurepin, L.V.; Park, J.M.; Lazarovits, G.; Bernards, M.A. Burkholderia phytofirmans-induced shoot and root growth promotion is associated with endogenous changes in plant growth hormone levels. Plant Growth Regul.2014, 75, 199-207.
Kumar, A.; Patel, J.S.; Meena, V.S.; Ramteke, P.W. Plant growth-promoting rhizobacteria: Strategies to improve abiotic stresses under sustainable agriculture. J. Plant Nutr. 2019, 42, 1402-1415.
Kumar, A.; Patel, J.S.; Meena, V.S.; Srivastava, R. Recent advances of PGPR based approaches for stress tolerance in plants for sustainable agriculture. Biocatal. Agric. Biotechnol. 2019, 20, 101271.
He, L.; Li, C.; Liu, R. Indirect interactions between arbuscular mycorrhizal fungi and Spodoptera exigua alter photosynthesis and plant endogenous hormones. Mycorrhiza 2017, 27, 525-535.
Bhattacharyya, P.N.; Jha, D.K. Plant growth-promoting rhizobacteria (PGPR): Emergence in agriculture. World J. Microbiol. Biotechnol. 2012, 28, 1327-1350.
Radwan, S.S.; Dashti, N.; El-Nemr, I.M. Enhancing the growth of Vicia faba plants by microbial inoculation to improve their phytoremediation potential for oily desert areas. Int. J. Phytoremed. 2005, 7, 19-32.
Elbadry, M.; Taha, R.M.; Eldougdoug, K.A.; Gamal-Eldin, H. Induction of systemic resistance in faba bean (Vicia faba L.) to bean yellow mosaic potyvirus (BYMV) via seed bacterization with plant growth promoting rhizobacteria. J. Plant Dis. Prot. 2006, 113, 247-251.
Nalam, V.; Louis, J.; Shah, J. Plant defense against aphids, the pest extraordinaire. Plant Sci. 2019, 279, 96-107.
Alvarez, A.E.; Tjallingii,W.F.; Garzo, E.; Vleeshouwers, V.; Dicke, M.; Vosman, B. Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to the aphid Myzus persicae. Entomol. Exp. Appl.2006, 121, 145-157.
Le Roux, V.; Dugravot, S.; Brunissen, L.; Vincent, C.; Pelletier, Y.; Giordanengo, P. Antixenosis phloem-based resistance to aphids: Is it the rule? Ecol. Entomol. 2010, 35, 407-416.
Will, T.; Kornemann, S.R.; Furch, A.C.U.; Tjallingii, W.F.; van Bel, A.J.E. Aphid watery saliva counteracts sieve-tube occlusion: A universal phenomenon? J. Exp. Biol. 2009, 212, 3305-3312.
Paprocka, M.; Gliszczyńska, A.; Dancewicz, K.; Gabryś, B. Novel hydroxy- and epoxy-cis-jasmone and dihydrojasmone derivatives affect the foraging activity of the peach potato aphid Myzus persicae (Sulzer) (Homoptera: Aphididae). Molecules 2018, 23, 2362.
Wang, W.; Dai, H.; Zhang, Y.; Chandrasekar, R.; Luo, L.; Hiromasa, Y.; Sheng, C.; Peng, G.; Chen, S.; Tomich, J.M.; et al. Armet is an effector protein mediating aphid-plant interactions. FASEB J. 2015, 29, 2032-2045.
Wang, W.; Luo, L.; Lu, H.; Chen, S.; Kang, L.; Cui, F. Angiotensin-converting enzymes modulate aphid-plant interactions. Sci. Rep. 2015, 5, 1-9.
Will, T.; Tjallingii, W.F.; Thonnessen, A.; van Bel, A.J.E. Molecular sabotage of plant defense by aphid saliva. Proc. Natl. Acad. Sci. USA 2007, 104, 10536-10541.
Naessens, E.; Dubreuil, G.; Giordanengo, P.; Baron, O.L.; Minet-Kebdani, N.; Keller, H.; Coustau, C. A secreted MIF cytokine enables aphid feeding and represses plant immune responses. Curr. Biol. 2015, 25, 1898-1903.