Construction and characterisation of near-isogenic Plutella xylostella (Lepidoptera: Plutellidae) strains resistant to Cry1Ac toxin.

BACKGROUND Resistance to insecticidal Bacillus thuringiensis (Bt) toxins has arisen in multiple populations of the worldwide Brassica pest Plutella xylostella (L.). To help elucidate the mechanism of resistance to Bt Cry1Ac toxin in a population from Florida, two pairs of near-isogenic lines (NILs) were developed. RESULTS NILs were generated using either backcross or recombinant inbred line methodologies and evaluated for near-isogenicity with inter-simple-sequence-repeat (ISSR) markers. Backcross line BC6F4 maintained a similar level of Cry1Ac resistance to parental strain DBM1Ac-R (>5000-fold) yet showed 98.24% genetic similarity to the susceptible parental strain DBM1Ac-S. Single-pair backcrosses between DBM1Ac-S and BC6F4 revealed that Cry1Ac resistance was controlled by one recessive autosomal locus. BC6F4 exhibited high levels of cross-resistance to Cry1Ab and Cry1Ah but not to Cry1Ca or Cry1Ie. CONCLUSION Near-isogenic strains were constructed to provide a reliable biological system to investigate the mechanism of Cry1Ac resistance in P. xylostella. These data suggest that resistance to Cry1Ac, Cry1Ab and Cry1Ah is probably caused by the alteration of a common receptor not recognised by Cry1Ca or Cry1Ie. Understanding Bt toxin cross-resistance provides valuable information to consider when developing pest control strategies to delay resistance evolution. © 2014 Society of Chemical Industry.

[1]  Liping Zhang,et al.  Susceptibility of Cry1Ab maize-resistant and -susceptible strains of sugarcane borer (Lepidoptera: Crambidae) to four individual Cry proteins. , 2013, Journal of invertebrate pathology.

[2]  Michael J Furlong,et al.  Diamondback moth ecology and management: problems, progress, and prospects. , 2013, Annual review of entomology.

[3]  J. Schwartz,et al.  Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. , 2012, Journal of invertebrate pathology.

[4]  J. Jurat-Fuentes,et al.  Association of Cry1Ac Toxin Resistance in Helicoverpa zea (Boddie) with Increased Alkaline Phosphatase Levels in the Midgut Lumen , 2012, Applied and Environmental Microbiology.

[5]  Ping Wang,et al.  Parallel Evolution of Bacillus thuringiensis Toxin Resistance in Lepidoptera , 2011, Genetics.

[6]  Ping Wang,et al.  Differential alteration of two aminopeptidases N associated with resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper , 2011, Proceedings of the National Academy of Sciences.

[7]  A. Crespo,et al.  Cross-resistance and mechanism of resistance to Cry1Ab toxin from Bacillus thuringiensis in a field-derived strain of European corn borer, Ostrinia nubilalis. , 2011, Journal of invertebrate pathology.

[8]  M. Adang,et al.  Reduced Levels of Membrane-Bound Alkaline Phosphatase Are Common to Lepidopteran Strains Resistant to Cry Toxins from Bacillus thuringiensis , 2011, PloS one.

[9]  S. Downes,et al.  Characteristics of Resistance to Bacillus thuringiensis Toxin Cry2Ab in a Strain of Helicoverpa punctigera (Lepidoptera: Noctuidae) Isolated from a Field Population , 2010, Journal of economic entomology.

[10]  S. Kasai,et al.  Use of isogenic strains indicates CYP9M10 is linked to permethrin resistance in Culex pipiens quinquefasciatus , 2010, Insect molecular biology.

[11]  D. Heckel,et al.  An ABC Transporter Mutation Is Correlated with Insect Resistance to Bacillus thuringiensis Cry1Ac Toxin , 2010, PLoS genetics.

[12]  E. Pereira,et al.  Measurements of Cry1F binding and activity of luminal gut proteases in susceptible and Cry1F resistant Ostrinia nubilalis larvae (Lepidoptera: Crambidae). , 2010, Journal of invertebrate pathology.

[13]  W. Gao,et al.  Introgression of a disrupted cadherin gene enables susceptible Helicoverpa armigera to obtain resistance to Bacillus thuringiensis toxin Cry1Ac. , 2009, Bulletin of entomological research.

[14]  N. Crickmore,et al.  Cross-resistance between a Bacillus thuringiensis Cry toxin and non-Bt insecticides in the diamondback moth. , 2008, Pest management science.

[15]  W. Moar,et al.  Production and Characterization of Bacillus thuringiensis Cry1Ac-Resistant Cotton Bollworm Helicoverpa zea (Boddie) , 2007, Applied and Environmental Microbiology.

[16]  D. Ellar,et al.  Role of Receptors in Bacillus thuringiensis Crystal Toxin Activity , 2007, Microbiology and Molecular Biology Reviews.

[17]  M. Gevrey,et al.  ISSR-PCR: tool for discrimination and genetic structure analysis of Plutella xylostella populations native to different geographical areas. , 2007, Molecular phylogenetics and evolution.

[18]  A. Shelton,et al.  The diversity of Bt resistance genes in species of Lepidoptera. , 2007, Journal of invertebrate pathology.

[19]  M. Soberón,et al.  Role of receptor interaction in the mode of action of insecticidal Cry and Cyt toxins produced by Bacillus thuringiensis , 2007, Peptides.

[20]  A. Shelton,et al.  Mechanism of Resistance to Bacillus thuringiensis Toxin Cry1Ac in a Greenhouse Population of the Cabbage Looper, Trichoplusia ni , 2006, Applied and Environmental Microbiology.

[21]  G. Churchill,et al.  Complex Genetic Architecture Revealed by Analysis of High-Density Lipoprotein Cholesterol in Chromosome Substitution Strains and F2 Crosses , 2006, Genetics.

[22]  Shuwen Wu,et al.  Investigation of resistance mechanisms to fipronil in diamondback moth (Lepidoptera: Plutellidae). , 2006, Journal of economic entomology.

[23]  A. Blanco,et al.  Detection of QTLs for grain protein content in durum wheat , 2006, Theoretical and Applied Genetics.

[24]  N. Crickmore,et al.  Common, but Complex, Mode of Resistance of Plutella xylostella to Bacillus thuringiensis Toxins Cry1Ab and Cry1Ac , 2005, Applied and Environmental Microbiology.

[25]  B. Raymond,et al.  Genes and environment interact to determine the fitness costs of resistance to Bacillus thuringiensis , 2005, Proceedings of the Royal Society B: Biological Sciences.

[26]  Andrew J. Millar,et al.  Natural Allelic Variation in the Temperature-Compensation Mechanisms of the Arabidopsis thaliana Circadian Clock Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. AY685131 and AY685132. , 2005, Genetics.

[27]  A. Trubuil,et al.  Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family , 2005, Theoretical and Applied Genetics.

[28]  J. Léon,et al.  Development of candidate introgression lines using an exotic barley accession (Hordeum vulgare ssp. spontaneum) as donor , 2004, Theoretical and Applied Genetics.

[29]  A. Shelton,et al.  Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution , 2003, Nature Biotechnology.

[30]  M. Pitcairn,et al.  DNA phenotyping to find a natural enemy in Uzbekistan for California biotypes of Salsola tragus L. , 2003 .

[31]  Richard T. Roush,et al.  Insect Resistance to Transgenic Bt Crops: Lessons from the Laboratory and Field , 2003, Journal of economic entomology.

[32]  A. Shelton,et al.  Examination of the F2 Screen for Rare Resistance Alleles to Bacillus thuringiensis Toxins in the Diamondback Moth (Lepidoptera: Plutellidae) , 2002, Journal of economic entomology.

[33]  J. Ferré,et al.  Biochemistry and Genetics of Insect Resistance to Bacillus thuringiensis , 2002 .

[34]  A. Shelton,et al.  Different Cross-Resistance Patterns in the Diamondback Moth (Lepidoptera: Plutellidae) Resistant to Bacillus thuringiensis Toxin Cry1C , 2001, Journal of Economic Entomology.

[35]  D. Wright,et al.  Fitness costs and stability of resistance to Bacillus thuringiensis in a field population of the diamondback moth Plutella xylostella L. , 2001 .

[36]  Juliet D. Tang,et al.  Development and Characterization of Diamondback Moth Resistance to Transgenic Broccoli Expressing High Levels of Cry1C , 2000, Applied and Environmental Microbiology.

[37]  S. Herrero,et al.  Genetic and Biochemical Approach for Characterization of Resistance to Bacillus thuringiensis Toxin Cry1Ac in a Field Population of the Diamondback Moth, Plutella xylostella , 2000, Applied and Environmental Microbiology.

[38]  T. Malvar,et al.  Integrative Model for Binding of Bacillus thuringiensis Toxins in Susceptible and Resistant Larvae of the Diamondback Moth (Plutella xylostella) , 1999, Applied and Environmental Microbiology.

[39]  M. Adang,et al.  Toxicity, Binding, and Permeability Analyses of FourBacillus thuringiensis Cry1 δ-Endotoxins Using Brush Border Membrane Vesicles of Spodoptera exigua and Spodoptera frugiperda , 1999, Applied and Environmental Microbiology.

[40]  N. Crickmore,et al.  Revision of the Nomenclature for the Bacillus thuringiensis Pesticidal Crystal Proteins , 1998, Microbiology and Molecular Biology Reviews.

[41]  Y. Shirai,et al.  Low Intrinsic Rate of Natural Increase in BT-resistant Population of Diamondback Moth, Plutella xylostella (L.) (Lepidoptera: Yponomeutidae). , 1998 .

[42]  T. Malvar,et al.  Global variation in the genetic and biochemical basis of diamondback moth resistance to Bacillus thuringiensis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Juliet D. Tang,et al.  Inheritance, Stability, and Lack-of-Fitness Costs of Field-Selected Resistance to Bacillus thuringiensis in Diamondback Moth (Lepidoptera: Plutellidae) from Florida , 1997 .

[44]  D. Wright,et al.  A Change in a Single Midgut Receptor in the Diamondback Moth (Plutella xylostella) Is Only in Part Responsible for Field Resistance to Bacillus thuringiensis subsp. kurstaki and B. thuringiensis subsp. aizawai , 1997, Applied and environmental microbiology.

[45]  L. Masson,et al.  One gene in diamondback moth confers resistance to four Bacillus thuringiensis toxins. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[46]  B. Tabashnik,et al.  Field-evolved resistance to Bacillus thuringiensis toxin CryIC in diamondback moth (Lepidoptera: Plutellidae) , 1996 .

[47]  A. Shelton,et al.  Toxicity of Bacillus thuringiensis Spore and Crystal Protein to Resistant Diamondback Moth (Plutella xylostella) , 1996, Applied and environmental microbiology.

[48]  D. Heckel,et al.  Cross-Resistance to Bacillus thuringiensis Toxin CryIF in the Diamondback Moth (Plutella xylostella) , 1994, Applied and environmental microbiology.

[49]  K. Dong,et al.  Linkage of kdr-type resistance and the para-homologous sodium channel gene in German cockroaches (Blattella germanica). , 1994, Insect biochemistry and molecular biology.

[50]  B. Tabashnik,et al.  Evolution of Resistance to Bacillus Thuringiensis , 1994 .

[51]  B. Tabashnik,et al.  Resistance to Toxins from Bacillus thuringiensis subsp. kurstaki Causes Minimal Cross-Resistance to B. thuringiensis subsp. aizawai in the Diamondback Moth (Lepidoptera: Plutellidae) , 1993, Applied and environmental microbiology.

[52]  M. Whalon,et al.  Managing Insect Resistance to Bacillus thuringiensis Toxins , 1992, Science.

[53]  N. White,et al.  Inheritance of Malathion Resistance in a Strain of Tribolium castaneum (Coleoptera: Tenebrionidae) and Effects of Resistance Genotypes on Fecundity and Larval Survival in Malathion-Treated Wheat , 1988 .

[54]  R. Roush,et al.  Inheritance of Methomyl Resistance in the Tobacco Budworm (Lepidoptera: Noctuidae) , 1985 .

[55]  J. A. Mckenzie,et al.  The effect of genetic background on the fitness of diazinon resistance genotypes of the Australian sheep blowfly, Lucilia cuprina , 1982, Heredity.

[56]  G. Shanahan Genetics of diazinon resistance in larvae of Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae) , 1979 .