Transcriptional responses underlying the hormetic and detrimental effects of the plant secondary metabolite gossypol on the generalist herbivore Helicoverpa armigera

BMC Genomics

Volumn 12, Issue , 2011, Pages

  de la Paz Celorio Mancera, Maria ^a,b   Ahn, Seung Joon ^a,c   Vogel, Heiko ^a   Heckel, David G ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c Rural Development Administration   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BETA FRUCTOFURANOSIDASE; GOSSYPOL; OXIDOREDUCTASE; OXYGEN RADICAL;

ARTHROPOD LARVA; ARTICLE; CELL ADHESION; CONTROLLED STUDY; DETOXIFICATION; DOWN REGULATION; FEEDING BEHAVIOR; GENE EXPRESSION; GENE EXPRESSION PROFILING; HELICOVERPA ARMIGERA; HERBIVORE; HORMESIS; LARVAL DEVELOPMENT; NONHUMAN; PH; PUPA (LIFE CYCLE STAGE); TRANSCRIPTION REGULATION; UPREGULATION; WEIGHT GAIN; ANIMAL; DNA MICROARRAY; DOSE RESPONSE; DRUG EFFECT; EXPRESSED SEQUENCE TAG; GENE; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; MOTH;

GOSSYPIUM HIRSUTUM; HELICOVERPA ARMIGERA; HEXAPODA; MALVACEAE;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENES, INSECT; GOSSYPOL; HORMESIS; LARVA; MOTHS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTION, GENETIC;

EID: 83155192028     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-575     Document Type: Article

References (51)

1. Lukefahr MJ, Fryxell PA. Content of gossypol in plants belonging to Genera related to cotton. Econ Bot 1967, 21(2):128-131.
2. Depeyster A, Wang YY. Genetic toxicity studies of gossypol. Mutation Res 1993, 297(3):293-312.
3. Abou-Donia MB. Physiological effects and metabolism of gossypol. Residue Reviews 1976, 61:124-161.
4. Laughton MJ, Halliwell B, Evans PJ, Hoult JRS. Antioxidant and pro-oxidant actions of the plant phenolics quercetin, gossypol and myricetin - Effects on lipid-peroxidation, hydroxyl radical generation and bleomycin-dependent damage to DNA. Biochem Pharmacol 1989, 38(17):2859-2865. 10.1016/0006-2952(89)90442-5, 2476132.
5. Dodou K. Investigations on gossypol: past and present developments. Expert Opinion Investigational Drugs 2005, 14(11):1419-1434.
6. Oliver CL, Miranda MB, Shangary S, Land S, Wang SM, Johnson DE. (-)-Gossypol acts directly on the mitochondria to overcome Bcl-2-mediated and Bcl-X-L-mediated apoptosis resistance. Mol Cancer Therapeutics 2005, 4(1):23-31.
7. Gershenzon J, Dudareva N. The function of terpene natural products in the natural world. Nature Chem Biol 2007, 3(7):408-414.
8. Cai YF, Zhang H, Zeng Y, Mo JC, Bao JK, Miao C, Bai J, Yan F, Chen F. An optimized gossypol high-performance liquid chromatography assay and its application in evaluation of different gland genotypes of cotton. J Biosci 2004, 29(1):67-71. 10.1007/BF02702563, 15286405.
9. Cass QB, Oliveira RV, De Pietro AC. Determination of gossypol enantiomer ratio in cotton plants by chiral higher-performance liquid chromatography. J Agric Food Chem 2004, 52(19):5822-5827. 10.1021/jf049626p, 15366827.
10. Yang HC, Davis DD. Variations in gossypol concentration of flower buds of cotton. Crop Science 1976, 16(4):485-488.
11. Cho S, Mitchell A, Mitter C, Regier J, Matthews M, Robertson R. Molecular phylogenetics of heliothine moths (Lepidoptera: Noctuidae: Heliothinae), with comments on the evolution of host range and pest status. Syst Entomol 2008, 33(4):581-594.
12. Lusas EW, Jividen GM. A review of the first 25 years of processing and utilization research. J Amer Oil Chemists' Soc 1987, 64(6):839-854.
13. Stipanovic RD, Williams HJ, Smith LA. Cotton terpenoid inhibition of Heliothis virescens development. Amer Chem Soc Symp Ser 1986, 79-94.
14. Kaiser J. Hormesis - Sipping from a poisoned chalice. Science 2003, 302(5644):376-379. 10.1126/science.302.5644.376, 14563981.
15. Douglas H. Science, hormesis and regulation. Human Exp Toxicol 2008, 27(8):603-607.
16. Le Bourg E. Hormesis, aging and longevity. Biochim Biophys Acta 2009, 1790(10):1030-1039. 10.1016/j.bbagen.2009.01.004, 19463497.
17. Steinberg CEW, Stürzenbaum SR, Menzel R. Genes and environment -- Striking the fine balance between sophisticated biomonitoring and true functional environmental genomics. Sci Total Environ 2008, 400(1-3):142-161. 10.1016/j.scitotenv.2008.07.023, 18817948.
18. Toyoshiba H, Sone H, Yamanaka T, Parham FM, Irwin RD, Boorman GA, Portier CJ. Gene interaction network analysis suggests differences between high and low doses of acetaminophen. Toxicol Appl Pharmacol 2006, 215(3):306-316. 10.1016/j.taap.2006.03.009, 16701773.
19. Gong P, Guan X, Inouye LS, Pirooznia M, Indest KJ, Athow RS, Deng YP, Perkins EJ. Toxicogenomic analysis provides new insights into molecular mechanisms of the sublethal toxicity of 2,4,6-trinitrotoluene in Eisenia fetida. Environ Toxicol Chem 1995, 26:954-959.
20. Hutchinson RW, Ing NH, Burghardt RC. Induction of c-fos, and cytochrome c oxidase subunits I and II by gossypol acetic acid in rat liver cells. Cell Biol Toxicol 1998, 14(6):391-399. 10.1023/A:1007543510337, 9879931.
21. Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, Wang LJ, Huang YP, Chen XY. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature Biotechnol 2007, 25(11):1307-1313.
22. Zhou XJ, Ma CX, Li M, Sheng CF, Liu HX, Qiu XH. CYP9A12 and CYP9A17 in the cotton bollworm, Helicoverpa armigera: sequence similarity, expression profile and xenobiotic response. Pest Manag Sci 2010, 66(1):65-73. 10.1002/ps.1832, 19728321.
23. Fitt GP. The ecology of Heliothis species in relation to agroecosystems. Ann Rev Entomol 1989, 34:17-52.
24. Liu ZD, Li DM, Gong PY, Wu KJ. Life table studies of the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae), on different host plants. Environ Entomol 2004, 33(6):1570-1576.
25. Stipanovic RD, Lopez JD, Dowd MK, Puckhaber LS, Duke SE. Effect of racemic and (+)- and (-)-gossypol on the survival and development of Helicoverpa zea larvae. J Chem Ecol 2006, 32(5):959-968. 10.1007/s10886-006-9052-9, 16739016.
26. Fischer HM, Wheat CW, Heckel DG, Vogel H. Evolutionary origins of a novel host plant detoxification gene in butterflies. Mol Biol Evol 2008, 25(5):809-820. 10.1093/molbev/msn014, 18296701.
27. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene Ontology: tool for the unification of biology. Nature Genetics 2000, 25(1):25-29. 10.1038/75556, 3037419, 10802651.
28. Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 2008, 36:3420-3435. 10.1093/nar/gkn176, 2425479, 18445632.
29. Doniger SW, Salomonis N, Dahlquist KD, Vranizan K, Lawlor SC, Conklin BR. MAPPFinder: using Gene Ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biology 2003, 4(1):R7. 10.1186/gb-2003-4-1-r7, 151291, 12540299.
30. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 1997, 25(17):3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
31. Breitling R, Armengaud P, Amtmann A, Herzyk P. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. Febs Letters 2004, 573(1-3):83-92. 10.1016/j.febslet.2004.07.055, 15327980.
32. Stipanovic RD, Lopez JD, Dowd MK, Puckhaber LS, Duke SE. Effect of Racemic, (+)- and (-)-Gossypol on Survival and Development of Heliothis virescens Larvae. Environ Entomol 2008, 37(5):1081-1085. 10.1603/0046-225X(2008)37[1081:EORAGO]2.0.CO;2, 19036185.
33. Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B. Drosophila Intestinal Response to Bacterial Infection: Activation of Host Defense and Stem Cell Proliferation. Cell Host Microbe 2009, 5(2):200-211. 10.1016/j.chom.2009.01.003, 19218090.
34. Herve JC, Pluciennik F, Bastide B, Cronier L, Verrecchia F, Malassine A, Joffre M, Deleze J. Contraceptive gossypol blocks cell-to-cell communication in human and rat cells. Eur J Pharmacol 1996, 313(3):243-255. 10.1016/0014-2999(96)00476-1, 8911921.
35. Depeyster A, Hyslop PA, Kuhn CE, Sauerheber RD. Membrane structural functional perturbations induced by gossypol - effects on membrane order, liposome permeability, and insulin-sensitive hexose-transport. Biochem Pharmacol 1986, 35(19):3293-3300. 10.1016/0006-2952(86)90426-0, 3533079.
36. Moon DO, Choi YH, Moon SK, Kim WJ, Kim GY. Gossypol decreases tumor necrosis factor-alpha-induced intercellular adhesion molecule-1 expression via suppression of NF-kappa B activity. Food Chem Toxicol 2011, 49(4):999-1005. 10.1016/j.fct.2011.01.006, 21223991.
37. Gahan LJ, Gould F, Heckel DG. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 2001, 293(5531):857-860. 10.1126/science.1060949, 11486086.
38. Carriere Y, Showalter AM, Fabrick JA, Sollome J, Ellers-Kirk C, Tabashnik BE. Cadherin gene expression and effects of Bt resistance on sperm transfer in pink bollworm. J Insect Physiol 2009, 55(11):1058-1064. 10.1016/j.jinsphys.2009.07.013, 19666026.
39. Carriere Y, Ellers-Kirk C, Biggs R, Higginson DM, Dennehy TJ, Tabashnik BE. Effects of gossypol on fitness costs associated with resistance to Bt cotton in pink bollworm. J Econ Entomol 2004, 97(5):1710-1718. 10.1603/0022-0493-97.5.1710, 15568363.
40. Przybylski P, Pyta K, Stefanska J, Ratajczak-Sitarz M, Katrusiak A, Huczynski A, Brzezinski B. Synthesis, crystal structures and antibacterial activity studies of aza-derivatives of phytoalexin from cotton plant - gossypol. Eur J Med Chem 2009, 44(11):4393-4403. 10.1016/j.ejmech.2009.05.032, 19577825.
41. Reyes J, Borriero L, Tanphaichitr N, Bellve AR, Benos DJ. Energy-metabolism of cultured tm4 cells and the action of gossypol. Biol Reprod 1986, 34(5):809-819. 10.1095/biolreprod34.5.809, 3730478.
42. Tvermyr SM, Froysa A, Jutte N, Hansson V. Glucose-metabolism in rat germ-cells - mechanism of action of gossypol. Annals New York Acad Sci 1984, 438(DEC):543-545.
43. Daimon T, Taguchi T, Meng Y, Katsuma S, Mita K, Shimada T. Beta-fructofuranosidase genes of the silkworm, Bombyx mori - Insights into enzymatic adaptation of B. mori to toxic alkaloids in mulberry latex. J Biol Chem 2008, 283(22):15271-15279. 10.1074/jbc.M709350200, 18397891.
44. Krishnan N, Kodrik D, Turanli F, Sehnal F. Stage-specific distribution of oxidative radicals and antioxidant enzymes in the midgut of Leptinotarsa decemlineata. J Insect Physiol 2007, 53(1):67-74. 10.1016/j.jinsphys.2006.10.001, 17126855.
45. Owen J, Hedley BA, Svendsen C, Wren J, Jonker MJ, Hankard PK, Lister LJ, Sturzenbaum SR, Morgan AJ, Spurgeon DJ, et al. Transcriptome profiling of developmental and xenobiotic responses in a keystone soil animal, the oligochaete annelid Lumbricus rubellus. BMC Genomics 2008, 9(art. 266).
46. Rojas MG, Stipanovic RD, Williams HJ, Vinson SB. Metabolism of gossypol by Heliothis virescens (F.) (Lepidoptera, Noctuidae). Environmental Entomology 1992, 21(3):518-526.
47. Abou-Donia MB, Lyman CM, Dieckert JW. Metabolic fate of gossypol - metabolism of 14C-gossypol in rats. Lipids 1970, 5(11):938-946. 10.1007/BF02531126, 5484207.
48. Abou-Donia MB, Dieckert JW. Metabolic-fate of gossypol - metabolism of [14C]gossypol in swine. Toxicol Appl Pharmacol 1975, 31(1):32-46. 10.1016/0041-008X(75)90049-6, 1129787.
49. Depeyster A, Quintanilha A, Packer L, Smith MT. Oxygen radical formation induced by gossypol in rat liver microsomes and human sperm. Biochem Biophys Res Comm 1984, 118(2):573-579. 10.1016/0006-291X(84)91341-X, 6322752.
50. Oakeshott J, Claudianos C, Campbell P. Biochemical genetics and genomics of insect esterases. Comprehensive molecular insect science 5:309-81. Oxford: Elsevier, Gilbert L, Iatrou K, Gill S.
51. Thorsteinson AJ. The chemotactic responses that determine host specificity in an oligophagous insect (Plutella maculipennis (Curt.) Lepidoptera). Canadian J Zool 1953, 31:52-72.