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The arbuscular mycorrhizal fungus Rhizophagus irregularis affects arthropod colonization on sweet pepper in both the field and greenhouse

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Abstract

In the present study sweet pepper plants, Capsicum annuum, were planted in greenhouse and open field conditions to test the effect of the arbuscular mycorrhizal fungus (AMF) Rhizophagus irregularis on phytophagous and predatory arthropod populations. Furthermore, we tested the hypothesis that AMF may increase the crop yield (number of fruits and their weight) and activity level of polyphenol oxidase (PPO) and peroxidase (POD), enzymes that seemingly decrease infestation by arthropod pests. The most abundant arthropod species found were the peach-potato aphid, Myzus persicae, western flower thrips, Frankliniella occidentalis, and the seven-spot ladybird, Coccinella septempunctata. Sweet pepper mutualism with AMF significantly reduced colonization by the peach-potato aphid under greenhouse conditions. Aphid density increased, however, on two of four pepper varieties tested under open field conditions. The density of ladybird predators did not appear directly influenced by AMF under greenhouse conditions, whereas a significantly higher predator density was found on three out of four pepper plant varieties with fungal mutualism tested under field conditions. Crop yield was significantly higher on plants with AMF mutualism under greenhouse conditions, but no clear effects were detected under field conditions. Both PPO and POD activity increased significantly and remained higher than controls until day 14 of the experiment under mutualism with AMF, although only in the greenhouse. The results suggest that under greenhouse conditions, pepper plant mutualism with AMF can increase pepper yield by reducing the numbers of the key pest, peach-potato aphid.

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References

  • Amarawardana L, Bandara P, Kumar V et al (2007) Olfactory response of Myzus persicae (Homoptera: Aphididae) to volatiles from leek and chive: Potential for intercropping with sweet pepper. Acta Agric Scand Sect B Soil Plant Sci 57:87–91

    Google Scholar 

  • Argandoña VH, Chaman M, Cardemil L et al (2001) Ethylene production and peroxidase activity in aphid-infested barley. J Chem Ecol 27:53–68

    Article  PubMed  Google Scholar 

  • Bass C, Puinean AM, Zimmer CT, Denholm I, Field LM, Foster SP, Gutbrod O, Nauen R, Slater R, Williamson MS (2014) The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochem Mol 51:41–51

    Article  CAS  Google Scholar 

  • Bergey DR, Howe GA, Ryan CA (1996) Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. PNAS 93:12053–12058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackman R, Eastop V (2000) Aphids on the world’s crops: an identification and information guide, 2nd edn. Wiley, Chichester

    Google Scholar 

  • Bond AB (2007) The evolution of color polymorphism: crypticity, searching images, and apostatic selection. Annu Rev Ecol Syst 38:489–514

    Article  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48

    Article  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 7(72):248–254

    Article  Google Scholar 

  • Cheema S, Sommerhalter M (2015) Characterization of polyphenol oxidase activity in Ataulfo mango. Food Chem 15(171):382–387

    Article  Google Scholar 

  • Chen H, Wilkerson CG, Kuchar JA et al (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. PNAS 102:19237–19242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, New York, pp 253–270

    Chapter  Google Scholar 

  • Constabel CP, Bergey DR, Ryan CA (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. PNAS 92:407–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emden HFV, Harrington R (2007) Aphids as crop pests, 2nd edn. CABI, Wallingford

    Book  Google Scholar 

  • Engelmoer DJP, Behm JE, Toby Kiers E (2014) Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance. Mol Ecol 23:1584–1593

    Article  CAS  PubMed  Google Scholar 

  • Felton GW, Donato K, Vecchio RJD, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J Chem Ecol 15:2667–2694

    Article  CAS  PubMed  Google Scholar 

  • Felton GW, Donato KK, Broadway RM, Duffey SS (1992) Impact of oxidized plant phenolics on the nutritional quality of dietar protein to a noctuid herbivore, Spodoptera exigua. J Insect Physiol 38:277–285

    Article  CAS  Google Scholar 

  • Fontana A, Reichelt M, Hempel S et al (2009) The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez F, Tkaczuk C, Dinu M et al (2016) New opportunities for the integration of microorganisms into biological pest control systems in greenhouse crops. J Pest Sci 89(2):295–311

    Article  Google Scholar 

  • Hare JD, Sun JJ (2011) Production of induced volatiles by Datura wrightii in response to damage by insects: effect of herbivore species and time. J Chem Ecol 37:751–764

    Article  CAS  PubMed  Google Scholar 

  • Hempel S, Stein C, Unsicker SB et al (2009) Specific bottom–up effects of arbuscular mycorrhizal fungi across a plant–herbivore–parasitoid system. Oecologia 160:267–277

    Article  PubMed  PubMed Central  Google Scholar 

  • Hepper CM, Azcon-Aguilar C, Rosendahl S, Sen R (1988) Competition between three species of Glomus used as spatially separated introduced and indigenous mycorrhizal inocula for leek (Allium porrum L.). N Phytol 110:207–215

    Article  Google Scholar 

  • Hoballah ME, Turlings TCJ (2005) The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J Chem Ecol 31:2003–2018

    Article  CAS  PubMed  Google Scholar 

  • Howard RJ, Garland JA, Seaman WL (1994) Diseases and pests of vegetable crops in Canada. The Canadian Phytopathological Society and the Entomological Society of Canada, Ottawa, Canada, pp 1–54

  • Jarvis WR (1992) Managing diseases in greenhouse crops. Plant Dis 73(3):190–194

    Article  Google Scholar 

  • Jiang J-H, Lee Y-I, Cubeta MA, Chen L-C (2015) Characterization and colonization of endomycorrhizal Rhizoctonia fungi in the medicinal herb Anoectochilus formosanus (Orchidaceae). Mycorrhiza 25:431–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johansen NS, Vänninen I, Pinto DM (2011) In the light of new greenhouse technologies: 2. Direct effects of artificial lighting on arthropods and integrated pest management in greenhouse crops. Ann Appl Biol 159(1):1–27

    Article  Google Scholar 

  • Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209

    Article  CAS  PubMed  Google Scholar 

  • Lee J-H, Hong J-P, Oh S-K et al (2004) The ethylene-responsive factor like protein 1 (CaERFLP1) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with different binding affinities: possible biological roles of CaERFLP1 in response to pathogen infection and high salinity conditions in transgenic tobacco plants. Plant Mol Biol 55:61–81

    Article  CAS  PubMed  Google Scholar 

  • Malais M, Ravensberg WJ (2003) The biology of glasshouse pests and their natural enemies: knowing and recognizing. Koppert, B. V., Berkel en Rodenrijs

    Google Scholar 

  • Mutune B, Ekesi S, Niassy S et al (2016) Fungal endophytes as promising tools for the management of bean stem maggot Ophiomyia phaseoli on beans Phaseolus vulgaris. J Pest Sci 89(4):993–1001

    Article  Google Scholar 

  • Németh ZI, Pozsgai-Harsányi M, Badáczy D, Horváth A (2009) Stress sensitivity of correlation between POD and PPO activities in plants. Acta Silv Lign Hung 5:27–45

    Google Scholar 

  • Odebode AC, Salami AO (2004) Biochemical contents of pepper seedlings inoculated with phytophthora infestans and arbuscular mycorrhiza. J Agric Sci Belgrade 49:251–257

    Article  Google Scholar 

  • Portree J (1996) Greenhouse vegetable production guide for commercial growers. Province of British Columbia Ministry of Agriculture, Fisheries and Food

  • Ruscitti M, Arango M, Ronco M, Beltrano J (2011) Inoculation with mycorrhizal fungi modifies proline metabolism and increases chromium tolerance in pepper plants (Capsicum annuum L.). Braz J Plant Physiol 23:15–25

    Article  CAS  Google Scholar 

  • Selvakumar G, Thamizhiniyan P (2011) The effect of the arbuscular mycorrhizal (AM) fungus Glomus intraradices on the growth and yield of chilli (Capsicum annuum L.) under salinity stress. World Appl Sci J 14:1209–1214

    Google Scholar 

  • Silva AX, Bacigalupe LD, Luna-Rudloff M, Figueroa CC (2012) Insecticide resistance mechanisms in the green peach aphid Myzus persicae (Hemiptera: Aphididae). II. Costs and benefits. PLoS ONE 7:e36810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic Press, London

    Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org

  • Verdugo JA, Méndez T, Ortiz-Martínez SA et al (2012) Variation in resistance mechanisms to the green peach aphid among different Prunus persica commercial cultivars. J Econ Entomol 105:1844–1855

    Article  CAS  PubMed  Google Scholar 

  • War AR, Paulraj MG, Ahmad T et al (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang G, Chen M, Li L et al (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot erp214 60(13):3781–3796

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Italpollina SPA, Italy, for supplying the samples of R. irregularis used here. We also most sincerely thank the two anonymous referees for their valuable comments, which helped us improve the focus and clarity of the manuscript

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Correspondence to Adalbert Balog.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

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Communicated by S.T. Jaronski.

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Balog, A., Loxdale, H.D., Bálint, J. et al. The arbuscular mycorrhizal fungus Rhizophagus irregularis affects arthropod colonization on sweet pepper in both the field and greenhouse. J Pest Sci 90, 935–946 (2017). https://doi.org/10.1007/s10340-017-0844-1

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  • DOI: https://doi.org/10.1007/s10340-017-0844-1

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