Insecticide Resistance Mechanisms in the Green Peach Aphid Myzus Persicae (Hemiptera: Aphididae) II: Costs and Benefits

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2012 Jun 12

PMID 22685539

Citations 19

Authors

Andrea X Silva

Leonardo D Bacigalupe

Manuela Luna-Rudloff

Christian C Figueroa

Affiliations

Soon will be listed here.

Abstract

Background: Among herbivorous insects that have exploited agro-ecosystems, the peach-potato aphid, Myzus persicae, is recognized as one of the most important agricultural pests worldwide. Uses over 400 plant species and has evolved different insecticides resistance mechanisms. As M. persicae feeds upon a huge diversity of hosts, it has been exposed to a wide variety of plant allelochemicals, which probably have promoted a wide range of detoxification systems.

Methodology/principal Findings: In this work we (i) evaluated whether insecticide resistance mutations (IRM) in M. persicae can give an advantage in terms of reproductive fitness when aphids face two hosts, pepper (Capsicum annuum) a suitable host and radish (Raphanus sativus) the unfavorable host and (ii) examined the transcriptional expression of six genes that are known to be up-regulated in response to insecticides. Our results show a significant interaction between host and IRM on the intrinsic rate of increase (r(m)). Susceptible genotypes (not carrying insensitivity mutations) had a higher r(m) on pepper, and the transcriptional levels of five genes increased on radish. The r(m) relationship was reversed on the unfavorable host; genotypes with multiple IRM exhibited higher r(m), without altering the transcriptional levels of the studied genes. Genotypes with one IRM kept a similar r(m) on both hosts, but they increased the transcriptional levels of two genes.

Conclusions/significance: Although we have studied only nine genotypes, overall our results are in agreement with the general idea that allelochemical detoxification systems could constitute a pre-adaptation for the development of insecticide resistance. Genotypes carrying IRM exhibited a higher r(m) than susceptible genotypes on radish, the more unfavorable host. Susceptible genotypes should be able to tolerate the defended host by up-regulating some metabolic genes that are also responding to insecticides. Hence, our results suggest that the trade-off among resistance mechanisms might be quite complex, with a multiplicity of costs and benefits depending on the environment.

Citing Articles

Host plant flooding stress in soybeans differentially impacts avirulent and virulent soybean aphid (Aphis glycines) biotypes.

Lewis M, Poelstra J, Michel A Sci Rep. 2025; 15(1):4897.

PMID: 39929874 PMC: 11811272. DOI: 10.1038/s41598-025-87561-z.

Comparative transcriptome analysis reveals differences in gene expression in whitefly following individual or combined applications of Akanthomyces attenuatus (Zare & Gams) and matrine.

Wu J, Sun T, Bashir M, Qiu B, Wang X, Ali S BMC Genomics. 2022; 23(1):808.

PMID: 36474158 PMC: 9727895. DOI: 10.1186/s12864-022-09048-9.

Transcriptome and population structure of glassy-winged sharpshooters (Homalodisca vitripennis) with varying insecticide resistance in southern California.

Ettinger C, Byrne F, Souza Pacheco I, Brown D, Walling L, Atkinson P BMC Genomics. 2022; 23(1):721.

PMID: 36273137 PMC: 9587601. DOI: 10.1186/s12864-022-08939-1.

Silencing a Myzus persicae Macrophage Inhibitory Factor by Plant-Mediated RNAi Induces Enhanced Aphid Mortality Coupled with Boosted RNAi Efficacy in Transgenic Potato Lines.

Murtaza S, Tabassum B, Tariq M, Riaz S, Yousaf I, Jabbar B Mol Biotechnol. 2022; 64(10):1152-1163.

PMID: 35460447 DOI: 10.1007/s12033-022-00498-w.

Virus Diseases of Cereal and Oilseed Crops in Australia: Current Position and Future Challenges.

Jones R, Sharman M, Trebicki P, Maina S, Congdon B Viruses. 2021; 13(10).

PMID: 34696481 PMC: 8539440. DOI: 10.3390/v13102051.

References

Foster S, Denholm I, Thompson R, Poppy G, Powell W . Reduced response of insecticide-resistant aphids and attraction of parasitoids to aphid alarm pheromone; a potential fitness trade-off. Bull Entomol Res. 2005; 95(1):37-46. DOI: 10.1079/ber2004336. View

Cristofoletti P, Ribeiro A, Deraison C, Rahbe Y, Terra W . Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol. 2003; 49(1):11-24. DOI: 10.1016/s0022-1910(02)00222-6. View

Xie W, Wang S, Wu Q, Feng Y, Pan H, Jiao X . Induction effects of host plants on insecticide susceptibility and detoxification enzymes of Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manag Sci. 2010; 67(1):87-93. DOI: 10.1002/ps.2037. View

Li X, Schuler M, Berenbaum M . Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol. 2006; 52:231-53. DOI: 10.1146/annurev.ento.51.110104.151104. View

Foster S, Kift N, Baverstock J, Sime S, Reynolds K, Jones J . Association of MACE-based insecticide resistance in Myzus persicae with reproductive rate, response to alarm pheromone and vulnerability to attack by Aphidius colemani. Pest Manag Sci. 2003; 59(11):1169-78. DOI: 10.1002/ps.751. View

Yoshimi T, Odagiri K, Hiroshige Y, Yokobori S, Takahashi Y, Sugaya Y . Induction profile of HSP70-cognate genes by environmental pollutants in Chironomidae. Environ Toxicol Pharmacol. 2011; 28(2):294-301. DOI: 10.1016/j.etap.2009.05.008. View

Bjorling-Poulsen M, Andersen H, Grandjean P . Potential developmental neurotoxicity of pesticides used in Europe. Environ Health. 2008; 7:50. PMC: 2577708. DOI: 10.1186/1476-069X-7-50. View

Li X, Berenbaum M, Schuler M . Molecular cloning and expression of CYP6B8: a xanthotoxin-inducible cytochrome P450 cDNA from Helicoverpa zea. Insect Biochem Mol Biol. 2000; 30(1):75-84. DOI: 10.1016/s0965-1748(99)00102-2. View

Foster S, Denholm I, Poppy G, Thompson R, Powell W . Fitness trade-off in peach-potato aphids (Myzus persicae) between insecticide resistance and vulnerability to parasitoid attack at several spatial scales. Bull Entomol Res. 2011; 101(6):659-66. DOI: 10.1017/S0007485310000623. View

10.

Azzouz H, Cherqui A, Campan E, Rahbe Y, Duport G, Jouanin L . Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae). J Insect Physiol. 2005; 51(1):75-86. DOI: 10.1016/j.jinsphys.2004.11.010. View

11.

Feder M, Hofmann G . Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol. 1999; 61:243-82. DOI: 10.1146/annurev.physiol.61.1.243. View

12.

Field L, Devonshire A . Evidence that the E4 and FE4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer) are part of a gene family. Biochem J. 1998; 330 ( Pt 1):169-73. PMC: 1219123. DOI: 10.1042/bj3300169. View

13.

Ramsey J, Rider D, Walsh T, De Vos M, Gordon K, Ponnala L . Comparative analysis of detoxification enzymes in Acyrthosiphon pisum and Myzus persicae. Insect Mol Biol. 2010; 19 Suppl 2:155-64. DOI: 10.1111/j.1365-2583.2009.00973.x. View

14.

Berticat C, Bonnet J, Duchon S, Agnew P, Weill M, Corbel V . Costs and benefits of multiple resistance to insecticides for Culex quinquefasciatus mosquitoes. BMC Evol Biol. 2008; 8:104. PMC: 2359736. DOI: 10.1186/1471-2148-8-104. View

15.

Francis F, Vanhaelen N, Haubruge E . Glutathione S-transferases in the adaptation to plant secondary metabolites in the Myzus persicae aphid. Arch Insect Biochem Physiol. 2005; 58(3):166-74. DOI: 10.1002/arch.20049. View

16.

Zhu-Salzman K, Koiwa H, Salzman R, Shade R, Ahn J . Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Mol Biol. 2003; 12(2):135-45. DOI: 10.1046/j.1365-2583.2003.00395.x. View

17.

Fenton B, Kasprowicz L, Malloch G, Pickup J . Reproductive performance of asexual clones of the peach-potato aphid, ( Myzus persicae, Homoptera: Aphididae), colonising Scotland in relation to host plant and field ecology. Bull Entomol Res. 2009; 100(4):451-60. DOI: 10.1017/S0007485309990447. View

18.

Field L, Devonshire A . Structure and organization of amplicons containing the E4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer). Biochem J. 1997; 322 ( Pt 3):867-71. PMC: 1218268. DOI: 10.1042/bj3220867. View

19.

Ryan M, Byrne O . Plant-insect coevolution and inhibition of acetylcholinesterase. J Chem Ecol. 2013; 14(10):1965-75. DOI: 10.1007/BF01013489. View

20.

Tsuji A, Kikuchi Y, Ogawa K, Saika H, Yuasa K, Nagahama M . Purification and characterization of cathepsin B-like cysteine protease from cotyledons of daikon radish, Raphanus sativus. FEBS J. 2008; 275(21):5429-43. DOI: 10.1111/j.1742-4658.2008.06674.x. View