Sex Pheromone Evolution Is Associated with Differential Regulation of the Same Desaturase Gene in Two Genera of Leafroller Moths
Chemical signals are prevalent in sexual communication systems. Mate recognition has been extensively studied within the Lepidoptera, where the production and recognition of species-specific sex pheromone signals are typically the defining character. While the specific blend of compounds that makes up the sex pheromones of many species has been characterized, the molecular mechanisms underpinning the evolution of pheromone-based mate recognition systems remain largely unknown. We have focused on two sets of sibling species within the leafroller moth genera Ctenopseustis and Planotortrix that have rapidly evolved the use of distinct sex pheromone blends. The compounds within these blends differ almost exclusively in the relative position of double bonds that are introduced by desaturase enzymes. Of the six desaturase orthologs isolated from all four species, functional analyses in yeast and gene expression in pheromone glands implicate three in pheromone biosynthesis, two Δ9-desaturases, and a Δ10-desaturase, while the remaining three desaturases include a Δ6-desaturase, a terminal desaturase, and a non-functional desaturase. Comparative quantitative real-time PCR reveals that the Δ10-desaturase is differentially expressed in the pheromone glands of the two sets of sibling species, consistent with differences in the pheromone blend in both species pairs. In the pheromone glands of species that utilize (Z)-8-tetradecenyl acetate as sex pheromone component (Ctenopseustis obliquana and Planotortrix octo), the expression levels of the Δ10-desaturase are significantly higher than in the pheromone glands of their respective sibling species (C. herana and P. excessana). Our results demonstrate that interspecific sex pheromone differences are associated with differential regulation of the same desaturase gene in two genera of moths. We suggest that differential gene regulation among members of a multigene family may be an important mechanism of molecular innovation in sex pheromone evolution and speciation.
Vyšlo v časopise:
Sex Pheromone Evolution Is Associated with Differential Regulation of the Same Desaturase Gene in Two Genera of Leafroller Moths. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002489
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002489
Souhrn
Chemical signals are prevalent in sexual communication systems. Mate recognition has been extensively studied within the Lepidoptera, where the production and recognition of species-specific sex pheromone signals are typically the defining character. While the specific blend of compounds that makes up the sex pheromones of many species has been characterized, the molecular mechanisms underpinning the evolution of pheromone-based mate recognition systems remain largely unknown. We have focused on two sets of sibling species within the leafroller moth genera Ctenopseustis and Planotortrix that have rapidly evolved the use of distinct sex pheromone blends. The compounds within these blends differ almost exclusively in the relative position of double bonds that are introduced by desaturase enzymes. Of the six desaturase orthologs isolated from all four species, functional analyses in yeast and gene expression in pheromone glands implicate three in pheromone biosynthesis, two Δ9-desaturases, and a Δ10-desaturase, while the remaining three desaturases include a Δ6-desaturase, a terminal desaturase, and a non-functional desaturase. Comparative quantitative real-time PCR reveals that the Δ10-desaturase is differentially expressed in the pheromone glands of the two sets of sibling species, consistent with differences in the pheromone blend in both species pairs. In the pheromone glands of species that utilize (Z)-8-tetradecenyl acetate as sex pheromone component (Ctenopseustis obliquana and Planotortrix octo), the expression levels of the Δ10-desaturase are significantly higher than in the pheromone glands of their respective sibling species (C. herana and P. excessana). Our results demonstrate that interspecific sex pheromone differences are associated with differential regulation of the same desaturase gene in two genera of moths. We suggest that differential gene regulation among members of a multigene family may be an important mechanism of molecular innovation in sex pheromone evolution and speciation.
Zdroje
1. HoekstraHECoyneJA 2007 The locus of evolution: evo devo and the genetics of adaptation. Evolution 61 995 1016
2. CarrollSB 2005 Evolution at two levels: on genes and form. PLoS Biol 3 e245 doi:10.1371/journal.pbio.0030245
3. WrayGA 2007 The evolutionary significance of cis-regulatory mutations. Nature Reviews Genetics 8 206 216
4. KingM-CWilsonAC 1975 Evolution at two levels in humans and chimpanzees. Science 188 107 116
5. KirschnerMGerhartJ 1998 Evolvability. Proceedings of the National Academy of Sciences USA 95 8420 8427
6. SternDL 2000 Perspective: evolutionary developmental biology and the problem of variation. Evolution 54 1079 1091
7. CarrollSB 2008 Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134 25 36
8. NosilPSchluterD 2011 The genes underlying the process of speciation. Trends in Ecology and Evolution 26 160 167
9. HartleyCJNewcombRDRussellRJYongCGStevens 2006 Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapid evolution of insecticide resistance. Proceedings of the National Academy of Sciences USA 103 8757 8762
10. KarasovTMesserPWPetrovDA 2010 Evidence that adaptation in Drosophila is not limited by mutation at single sites. PLoS Genet 6 e1000924 doi:10.1371/journal.pgen.1000924
11. SmadjaCButlinRK 2009 On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102 77 97
12. LinnCEJrRoelofsWL 1995 Pheromone communication in moths and its role in the speciation process. LambertDMSpencerHG Speciation and the recognition concept: theory and application Baltimore and London 263 300
13. El-SayedAM 2008 The Pherobase: database of insect pheromones and semiochemicals. http://www.pherobase.com
14. TillmanJASeyboldSJJurenkaRABlomquistGG 1999 Insect pheromones - an overview of biosynthesis and endocrine regulation. insect Biochemistry and Molecular Biology 29 481 514
15. MatsumotoS 2010 Molecular mechanisms underlying sex pheromone production in moths. Bioscience Biotechnology & Biochemistry 74 223 231
16. KnippleDCRosenfieldC-LNielsenRYouKMJeongSE 2002 Evolution of the integral membrane desaturase gene family in moths and flies. Genetics 162 1737 1752
17. LiénardMAStrandhMHedenströmEJohanssonTLöfstedtC 2008 Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evolutionary Biology 8 270
18. WangH-LLiénardMAZhaoC-HWangC-ZLöfstedtC 2010 Neofunctionalization in an ancestral insect desaturase lineage led to rare Δ6 pheromone signals in the Chinese tussah silkworm. Insect Biochemistry and Molecular Biology 40 742 751
19. RoelofsWLLiuWHaoGJiaoHRooneyAP 2002 Evolution of moth sex pheromones via ancestral genes. Proceedings of the National Academy of Sciences USA 99 13621 13626
20. SakaiRFukuzawaMNakanoRTatsukiSIshikawaY 2009 Alternative suppression of transcription from two desaturase genes is the key for species-specific sex pheromone biosynthesis in two Ostrinia moths. Insect Biochemistry and Molecular Biology 39 62 67
21. ShirangiTRDufourHDWilliamsTMCarrollSB 2009 Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLoS Biol 7 e1000168 doi:10.1371/journal.pbio.1000168
22. DugdaleJS 1990 Reassessment of Ctenopseustis Meyrick and Planotortrix Dugdale with descriptions of two new genera (Lepidoptera: Tortricidae). New Zealand Journal of Zoology 17 437 465
23. LanghoffPAuthierABuckleyTRDugdaleJSRodrigoA 2009 DNA barcoding of the endemic New Zealand leafroller moth genera, Ctenopseustis and Planotortrix. Molecular Ecology Resources 9 691 698
24. FosterSPDugdaleJSWhiteCS 1991 Sex pheromones and the status of greenheaded and brown headed leafroller moths in New Zealand. New Zealand Journal of Zoology 18 63 74
25. GalbreathRABennMHYoungHHoltVA 1985 Sex pheromone components in the New Zealand greenheaded leafroller Planotortrix excessana (Lepidoptera: Tortricidae). Zeitschrift fur Naturforschung 40 266 271
26. FosterSPClearwaterJRMugglestonSJShawPW 1990 Sex pheromone of a Planotortrix excessana sibling species and reinvestigation of related species. Journal of Chemical Ecology 16 2461 2474
27. YoungHGalbreathRABennMHHoltVAStrubleDL 1996 Sex pheromone components in New Zealand brownheaded leafroller Ctenopseustis obliquana (Lepidoptera: Tortricidae). Zeitschrift fur Naturforschung 40 262 265
28. FosterSPRoelofsWL 1987 Sex pheromone differences in populations of the brownheaded leafroller, Ctenopseustis obliquana. Journal of Chemical Ecology 13 623 629
29. ClearwaterJRFosterSPMugglestonSJDugdaleJSPriesnerE 1991 Intraspecific variation and interspecific differences in sex pheromones of sibling species in Ctenopseustis obliquana complex. Journal of Chemical Ecology 17 413 429
30. FosterSPMugglestonSJLöfstedtCHanssonB 1997 A genetic study on pheromonal communication in two Ctenopseustis moths. CardéRTMinksA Insect Pheromones: New Directions 514 524
31. WhiteCSLambertDM 1994 Genetic differences among pheromonally distinct New Zealand leafroller moths. Biochemical Systematics and Ecology 22 329 339
32. WhiteCSLambertDM 1995 Genetic continuity within, and discontinuities among, populations of leafroller moths with distinct sex-pheromones. Heredity 75 243 255
33. LöfstedtCRoelofsWL 1985 Sex pheromone precursors in two primitive New Zealand tortricid moth species. Insect Biochemistry 15 729 734
34. FosterSPRoelofsWL 1996 Sex pheromone biosynthesis in the tortricid moth, Ctenopseustis herana (Felder & Rogenhofer). Archives of Insect Biochemistry and Physiology 32 135 147
35. FosterSPRoelofsWL 1988 Sex pheromone biosynthesis in the leafroller moth Planotortix excessana by Δ10 desaturation. Archives of Insect Biochemistry and Physiology 8 1 9
36. FosterSP 1998 Sex pheromone biosynthesis in the tortricid moth Planotortrix excessana (Walker) involves chain-shortening of palmitoleate and oleate. Archives of Insect Biochemistry and Physiology 37 158 167
37. HaoGLiuWO'ConnorMRoelofsWL 2002 Acyl-CoA Z9- and Z10-desaturase genes from a New Zealand leafroller moth species, Planotortrix octo. Insect Biochemistry and Molecular Biology 32 961 966
38. HaoGO'ConnorMLiuWRoelofsWL 2002 Characterization of Z/E11- and Z9-desaturases from the obliquebanded leafroller moth, Choristoneura rosaceana. Journal of Insect Science 2 11 Available online: insectscience.org/12.11
39. LiuWJiaoHMurrayNCO'ConnorMRoelofsWL 2002 Gene characterized for membrane desaturase that produces (E)-11 isomers of mono- and diunsaturated fatty acids. Proceedings of the National Academy of Sciences USA 99 620 624
40. DingB-JLiénardMAWangH-LZhaoC-HLöfstedtC 2011 Terminal fatty-acyl-CoA desaturase involved in sex pheromone biosynthesis in the winter moth (Operophtera brumata). Insect Biochemistry and Molecular Biology 41 715 722
41. YangZ 1997 PAML: a program for package for phylogenetic analysis by maximum likelihood. CABIOS 15 555 556
42. RosenfieldC-LYouKMMarsella-HerrickPRoelofsWLKnippleDC 2001 Structural and functional conservation and divergence among acyl-CoA desaturases of two noctuid species, the corn earworm, Helicoverpa zea, and the cabbage looper, Trichoplusia ni. Insect Biochemistry and Molecular Biology 31 949 964
43. LiuWRooneyAPXueBRoelofsWL 2004 Desaturases from the spotted fireworm moth (Choristoneura parallela) shed light on the evolutionary origins of novel moth sex pheromone desaturases. Gene 342 303 311
44. JeongSERosenfieldC-LMarsella-HerrickPYouKMKnippleDC 2003 Multiple acyl-CoA desaturase-encoding transcripts in pheromone glands of Helicoverpa assulta, the oriental tobacco budworm. Insect Biochemistry and Molecular Biology 33 609 622
45. LassanceJ-MGrootATLiénardMAAntonyBBorgwardtC 2010 Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466 486 489
46. NewcombRDGleesonDM 1998 Pheromone evolution within the genera Ctenopseustis and Planotortrix (Lepidoptera: Tortricidae) inferred from a phylogeny based on cytochrome oxidase I gene variation. Biochemical Systematics and Ecology 26 473 484
47. FosterSPClearwaterJRMugglestonSJDugdaleJS 1986 Probable sibling species complexes within two described New Zealand leafroller moths. Naturwissenschaften 73 156 158
48. DalleracRLabeurCJallonJ-MKnippleDCRoelofsWL 2000 A Δ9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proceedings of the National Academy of Sciences USA 97 9449 9454
49. ThompsonJDGibsonTJPlewniakFJeanmouginFHigginsDG 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25 4876 4882
50. PosadaDCrandallKA 1998 Modeltest: testing the model of DNA substitution. Bioinformatics 14 817 818
51. RonquistFHuelsenbeckJP 2003 MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 1572 1574
52. LivakKJSchmittgenTD 2001 Analysis of relative gene expression data using Real-Time Quantitative PCR and the 2−ΔΔCT method. METHODS 25 402 408
53. PfafflMW 2006 Relative quantification. DorakT Real-time PCR La Jolla, CA, USA International University Line 63 82
54. RamakersCRuijterJMLekanne DeprezRHMoormanAFM 2003 Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339 62 66
55. VandesompeleJDe PreterKPattynFPoppeBVan RoyN 2002 Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3 RESEARCH0034
56. SchneiterRTatzerVGoggGLeitnerEKohlweinS-D 2000 Elo1-dependent carboxy-terminal elongation of C14:1 Δ9 to C16:1Δ11 fatty acids in Saccharomyces cerevisiae. Journal of Bacteriology 182 3655 3660
57. StuckeyJEMcDonoughVMMartinCE 1990 The OLE1 gene of Saccharomyces cerevisiae encodes the Δ9 fatty acid desaturase and can be functionally replaced by the rat stearoyl-CoA desaturase gene. The Journal of Biological Chemistry 265 20144 20149
58. KnippleDCRosenfieldC-LMillerSJLiuWTangJ 1998 Cloning and functional expression of a cDNA encoding a pheromone gland-specific acyl-CoA Δ11-desaturase of the cabbage looper moth, Trichoplusia ni. Proceedings of the National Academy of Sciences USA 95 15287 15292
59. BuserHRArnHGuerinPRauscherS 1983 Determination of double bond position in mono-unsaturated acetates by mass spectrometry of dimethyl disulfide adducts. Analytical Chemistry 55 818 822
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 1
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Microenvironmental Regulation by Fibrillin-1
- Poly(ADP-Ribose) Polymerase 1 (PARP-1) Regulates Ribosomal Biogenesis in Nucleoli
- Parallel Mapping and Simultaneous Sequencing Reveals Deletions in and Associated with Discrete Inherited Disorders in a Domestic Dog Breed
- Two-Component Elements Mediate Interactions between Cytokinin and Salicylic Acid in Plant Immunity