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The Role of Plant Growth Regulators in a Plant–Aphid–Parasitoid Tritrophic System

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Abstract

Plant growth regulators (PGRs) play important roles in regulating plant growth. Application of PGRs may conversely affect the tritrophic plant–herbivore–parasitoid interactions. To manipulate the growth of winter wheat for rearing the English grain aphid, Sitobion avenae, which is used to rear an aphid parasitoid, Aphidius gifuensis, we determined the effects of four commonly used PGRs, indole-3-acetic acid (IAA), naphthalene acetic acid (NAA), gibberellic acid (GA3), and one plant growth retardant paclobutrazol (PBZ), on winter wheat seedlings and their indirect effects on the aphids and the parasitoids. Foliar application of IAA, NAA, and GA3 to wheat seedlings significantly affected the growth of the winter wheat plants, promoted plant height and leaf length, and increased fresh and dry weights. In contrast, PBZ had a negative effect on wheat growth. The PGRs did not affect the development, but had negative effects on fecundity and intrinsic rates of natural increase of S. avenae. The PGRs also exhibited negative effects on the parasitoids by having lower parasitism, emergence rate, and proportion of females when the host (aphids) fed on the PGRs-treated winter wheat seedlings than on untreated wheat plants. In conclusion, the PGRs-mediated effects strongly impact not only plant growth, but also the herbivores and the parasitoids. Our results suggest that the PGRs should be cautiously used to regulate plant growth if aphid parasitoids are dominant natural enemies. The information should be useful for understanding potential consequences related to biological control of aphids via parasitoids when plant growth regulators are used on crops.

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References

  • Abdellaoui K, Halima-Kamel MB, Hamouda MHB (2009) Physiological effects of gibberellic acid on the reproductive potential of Locusta migratoria migratoria. Tunis J Plant Prot 4:67–76.

    Google Scholar 

  • Ahmad N, Rashdi SMMS, Rajput AA (2003) Efficacy of plant growth regulators to manage the insect pests of cotton. Asian J Plant Sci 2:544–547

    Article  Google Scholar 

  • Bhalla O, Robinson A (1968) Effects of chemosterilants and growth regulators on the pea aphid fed an artificial diet. J Econ Entomol 61:552–555

    Article  CAS  Google Scholar 

  • Blackman RL, Eastop VF (1984) Aphids on the world’s crops: an identification and information guide. John Wiley & Sons, Chichester

    Google Scholar 

  • Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego

    Google Scholar 

  • Carver M (1989) Biological control of aphids. In: Minks AK, Harrewijn P (eds) Aphids: their biology, natural enemies and control, vol 2B. Elsevier, Amsterdam, pp 141–161

    Google Scholar 

  • Chaudhary B, Sharma M, Shakya S, Gautam D (2006) Effect of plant growth regulators on growth, yield and quality of chilli (Capsicum annuum L.) at Rampur, Chitwan. J Inst Agric Anim Sci 27:65–68

    Google Scholar 

  • Cottrell TE, Wood BW, Ni X (2010) Application of plant growth regulators mitigates chlorotic foliar injury by the black pecan aphid (Hemiptera: Aphididae). Pest Manag Sci 66:1236–1242

    Article  CAS  PubMed  Google Scholar 

  • Dixon AFG (1997) Aphid ecology: an optimization approach: an optimization approach. 2nd edn. Springer, Netherlands

    Google Scholar 

  • Fan ZY, Chen Q, Liang YZ, Zhou XN, Wu YQ. (2011) Preliminary study on the community structure charateristics of wheat aphid and their natural enemies. Mod Agric Sci Tech 4:145–146

    Google Scholar 

  • Foster S, Denholm I, Harling Z, Moores G, Devonshire A (1998) Intensification of insecticide resistance in UK field populations of the peach-potato aphid, Myzus persicae (Hemiptera: Aphididae) in 1996. Bull Entomol Res 88:127–130

    Article  Google Scholar 

  • Gencsoylu I (2009) Effect of plant growth regulators on agronomic characteristics, lint quality, pests, and predators in cotton. J Plant Growth Regul 28:147–153

    Article  CAS  Google Scholar 

  • Gianfagna T (1995) Natural and synthetic growth regulators and their use in horticultural and agronomic crops. In: Davies P (ed) Plant hormones: physiology, biochemistry and molecular biology, Springer, New York, pp. 751–774

    Chapter  Google Scholar 

  • Giron D, Frago E, Glevarec G, Pieterse CM, Dicke M (2013) Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence. Funct Ecol 27:599–609

    Article  Google Scholar 

  • Harms CL, Oplinger ES (1988) Plant growth regulators: their use in crop production. Purdue Univ, Coop Ext Serv, North Central Region Ext Publ NCR303. Am Soc Agron, Madison, WI, pp. 1–6

  • Hawkins DM (1981) A new test for multivariate normality and homoscedasticity. Technometers 23:105–110

    Article  Google Scholar 

  • Honeyborne C (1969) Performance of Aphis fabae and Brevicoryne brassicae on plants treated with growth regulators. J Sci Food Agric 20:388–390

    Article  CAS  Google Scholar 

  • Jarosik V, Holy I, Lapchin L, Havelka J (2003) Sex ratio in the aphid parasitoid Aphidius colemani (Hymenoptera: Braconidae) in relation to host size. Bull Entomol Res 93:255–258

    Article  CAS  PubMed  Google Scholar 

  • Kaur R, Rup P (2003) Influence of four plant growth regulators on development of the melon fruit fly, Bactrocera cucurbitae (Coquillett). Int J Trop Insect Sci 23:121–125

    Article  CAS  Google Scholar 

  • Kumar B, Pandey D, Goswami C, Jain S (2001) Effect of growth regulators on photosynthesis, transpiration and related parameters in water stressed cotton. Biol Plant 44:475–478

    Article  CAS  Google Scholar 

  • Latimer JG, Oetting RD (1999) Conditioning treatments affect insect and mite populations on bedding plants in the greenhouse. HortSci 34:235–238

    Google Scholar 

  • Li L, Staden JV, Jäger A (1998) Effects of plant growth regulators on the antioxidant system in seedlings of two maize cultivars subjected to water stress. Plant Growth Regul 25:81–87

    Article  CAS  Google Scholar 

  • Li CX, Shang YL, Jiang LN, Liu P, Qiu ZB, Zhang X (2001a) Regulation of plant growth regulator on leaves senescence and yield constitutions of wheat. Acta Bot Boreal-Occident Sin 21:931–936

    CAS  Google Scholar 

  • Li XJ, Zhi MX, Wei XY (2001b) Effects of BA and GA on grain weight at different position of winter wheat. Acta Agron Sin 27:1017–1020

    Google Scholar 

  • Nauen R, Elbert A (2003) European monitoring of resistance to insecticides in Myzus persicae and Aphis gossypii (Hemiptera: Aphididae) with special reference to imidacloprid. Bull Entomol Res 93:47–54

    Article  CAS  PubMed  Google Scholar 

  • Pan MZ, Liu TX (2014a) Suitability of three aphid species for Aphidius gifuensis (Hymenoptera: Braconidae): parasitoid performance varies with hosts of origin. Biol Control 69:90–96

    Article  Google Scholar 

  • Pan MZ, Liu TX (2014b) Effects of winter wheat cultivars on the life history traits and olfactory response of Aphidius gifuensis. Biocontrol 59:539–546

    Article  CAS  Google Scholar 

  • Pandey G, Teotia T (1980) Laboratory studies on chemosterilization of Angoumois grain moth, Sitotroga cerealella (Oliv.): screening of 33 compounds by pupal treatments. Indian J Entomol 42:1–15

    Google Scholar 

  • Prado SG, Frank SD (2013) Tritrophic effects of plant growth regulators in an aphid-parasitoid system. Biol Control 66:72–76

    Article  CAS  Google Scholar 

  • Rajala A, Peltonen-Sainio P (2000) Manipulating yield potential in cereals by plant growth regulators. Growth regulators in crop production. Food Products Press, Binghamton, pp. 27–70

    Google Scholar 

  • Ren XJ, Gao ZL, Dang ZH, Li YF, Pan WL (2007) The species and distribution of Aphidiidae in wheat fields in Hebei Province. J Hebei Agric Sci 11:37–40

    Google Scholar 

  • Robinson AG (1960) Effect of maleic hydrazide and other plant-growth regulators on the pea aphid, Acyrthosiphon pissum (Macrosiphon pisi), caged on broad bean, Vicia faba. Can Entomol 92:494–499

    Article  CAS  Google Scholar 

  • Robinson AG (1961) Effects of amitrol, zytron, and other herbicides or plant-growth regulators on the pea aphid, Acyrthosiphon pisum [Macrosiphum pisi], caged on broad bean, Vicia faba. Can J Plant Sci 41:413–417

    Article  CAS  Google Scholar 

  • Rup PJ, Kaur R, Kaur J (1998) Effect of gibberellic acid (GA3) on the protein, lipid and carbohydrate contents of banana fruit fly, Zaprionus paravittiger larvae. Int J Trop Insect Sci 18:145–148

    Article  CAS  Google Scholar 

  • Sajid GM, Kaukab M, Ahmad Z (2009) Foliar application of plant growth regulators (PGRs) and nutrients for improvement of lily flowers. Pak J Bot 41:233–237

    CAS  Google Scholar 

  • Singer M, Smith B (1976) Use of the plant growth regulator chlormequat chloride to control the aphid Hyperomyzus lactucae on black currants. Ann Appl Biol 82:407–414

    Article  CAS  Google Scholar 

  • Sohal S, Rup P, Arora G (2006) Influence of cytokinine, a plant growth regulator (PGR) on the activity of some enzymes involved in metabolism, in the nymphs of Lipaphis erysimi (Kalt.). J Environ Biol 27:217

    CAS  Google Scholar 

  • Uçkan F, Tüven A, Er A, Ergin E (2008) Effects of gibberellic acid on biological parameters of the larval endoparasitoid Apanteles galleriae (Hymenoptera: Braconidae). Ann Entomol Soc Am 101:593–597

    Article  Google Scholar 

  • Uçkan F, Haftaci İ, Ergin E (2011a) Effects of indol-3-acetic acid on biological parameters of the larval endoparasitoid Apanteles galleriae (Hymenoptera: Braconidae). Ann Entomol Soc Am 104:77–82

    Article  Google Scholar 

  • Uçkan F, Öztürk Z, Altuntaş H, Ergin E (2011b) Effects of gibberellic acid (GA3) on biological parameters and hemolymph metabolites of the pupal endoparasitoid Pimpla turionellae (Hymenoptera: Ichneumonidae) and its host Galleria mellonella (Lepidoptera: Pyralidae). J Entomol Res Soc 13:1–14

    Google Scholar 

  • van Emden HF (1964) Effect of (2-chloroethyl) trimethylammonium chloride on the rate of increase of the cabbage aphid (Brevicoryne brassicae (L.). Nature 201:946–948

    Article  Google Scholar 

  • van Emden HF, (1969) Plant resistance to Myzus persicae induced by a plant regulator and measured by aphid relative growth rate. Entomol Exp Appl 12:125–131

    Article  Google Scholar 

  • van Lenteren JC (2000) A greenhouse without pesticides: fact or fantasy?. Crop Prot 19:375–384

    Article  Google Scholar 

  • Wei JN, Li TF, Kuang RP, Wang Y, Yin TS, Wu XF, Zou L, Zhao WY, Cao J, Deng JH (2003) Mass rearing of Aphidius gifuensis (Hymenoptera: Aphidiidae) for biological control of Myzus persicae (Homoptera: Aphididae). Biocontrol Sci Technol 13:87–97

    Article  Google Scholar 

  • Worthing C (1969) Use of growth retardants on chrysanthemums: effect on pest populations. J Sci Food Agric 20:394–397

    Article  CAS  Google Scholar 

  • Wyatt I, White P (1977) Simple estimation of intrinsic increase rates for aphids and tetranychid mites. J Appl Ecol 14:757–766

    Article  Google Scholar 

  • Yang S, Wei JN, Yang SY, Kuang RP (2011) Current status and future trends of augmentative release of Aphidius gifuensis for control of Myzus persicae in China’s Yunnan Province. J Entomol Res Soc 13:87–99

    Google Scholar 

  • Zummo G, Benedict J, Segers J (1984) Effect of the plant growth regulator mepiquat chloride on host plant resistance in cotton to bollworm (Lepidoptera: Noctuidae). J Econ Entomol 77:922–924

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful for the assistance of all staff and students in the Key Laboratory of Applied Entomology, Northwest A&F University at Yangling, Shaanxi, China. This work was supported by the Natural Science Foundation of China (31471819), National Basic Research Program of Ministry of Science and Technology, China (973 Programs, 2013CB127600) and China Agriculture Research System (CARS-25-B-06).

Author Contributions

Conceived and designed the experiments: HZ, TXL. Performed the experiments: HZ, HHC, MZP, YZS. Analyzed the data: HZ, HHC, TXL. Contributed reagents/materials/analysis tools: HZ, HHC, TXL. Wrote the paper: HZ, HHC, TXL.

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Correspondence to Tong-Xian Liu.

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Zhao, H., Cao, HH., Pan, MZ. et al. The Role of Plant Growth Regulators in a Plant–Aphid–Parasitoid Tritrophic System. J Plant Growth Regul 36, 868–876 (2017). https://doi.org/10.1007/s00344-017-9689-3

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  • DOI: https://doi.org/10.1007/s00344-017-9689-3

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