[en] [en] BACKGROUND: Moths have evolved highly successful mating systems, relying on species-specific mixtures of sex pheromone components for long-distance mate communication. Acyl-CoA desaturases are key enzymes in the biosynthesis of these compounds and to a large extent they account for the great diversity of pheromone structures in Lepidoptera. A novel desaturase gene subfamily that displays Delta11 catalytic activities has been highlighted to account for most of the unique pheromone signatures of the taxonomically advanced ditrysian species. To assess the mechanisms driving pheromone evolution, information is needed about the signalling machinery of primitive moths. The currant shoot borer, Lampronia capitella, is the sole reported primitive non-ditrysian moth known to use unsaturated fatty-acid derivatives as sex-pheromone. By combining biochemical and molecular approaches we elucidated the biosynthesis paths of its main pheromone component, the (Z,Z)-9,11-tetradecadien-1-ol and bring new insights into the time point of the recruitment of the key Delta11-desaturase gene subfamily in moth pheromone biosynthesis.
RESULTS: The reconstructed evolutionary tree of desaturases evidenced two ditrysian-specific lineages (the Delta11 and Delta9 (18C>16C)) to have orthologs in the primitive moth L. capitella despite being absent in Diptera and other insect genomes. Four acyl-CoA desaturase cDNAs were isolated from the pheromone gland, three of which are related to Delta9-desaturases whereas the fourth cDNA clusters with Delta11-desaturases. We demonstrated that this transcript (Lca-KPVQ) exclusively accounts for both steps of desaturation involved in pheromone biosynthesis. This enzyme possesses a Z11-desaturase activity that allows transforming the palmitate precursor (C16:0) into (Z)-11-hexadecenoic acid and the (Z)-9-tetradecenoic acid into the conjugated intermediate (Z,Z)-9,11-tetradecadienoic acid.
CONCLUSION: The involvement of a single Z11-desaturase in pheromone biosynthesis of a non-ditrysian moth species, supports that the duplication event leading to the origin of the Lepidoptera-specific Delta11-desaturase gene subfamily took place before radiation of ditrysian moths and their divergence from other heteroneuran lineages. Our findings uncover that this novel class of enzymes affords complex combinations of unique unsaturated fatty acyl-moieties of variable chain-lengths, regio- and stereo-specificities since early in moth history and contributes a notable innovation in the early evolution of moth-pheromones.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Lienard, Marjorie ; Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases ; Chemical Ecology and Ecotoxicology, Department of Ecology, Lund University, Ecology Building, SE-22362, Lund, Sweden. marjorie.lienard@ekol.lu.se
Strandh, Maria; Chemical Ecology and Ecotoxicology, Department of Ecology, Lund University, SE-22362, Lund, Sweden
Hedenström, Erik; Department of Natural Sciences, Institute of Natural Sciences, SE-85170, Sundsvall, Sweden
Johansson, Tomas; Microbial Ecology, Department of Ecology, Lund University, SE-22362, Lund, Sweden
Löfstedt, Christer; Chemical Ecology and Ecotoxicology, Department of Ecology, Lund University, SE-22362, Lund, Sweden
Language :
English
Title :
Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera.
Publication date :
02 October 2008
Journal title :
BMC Evolutionary Biology
eISSN :
1471-2148
Publisher :
Springer Science and Business Media LLC, England
Volume :
8
Issue :
1
Pages :
270
Peer reviewed :
Peer Reviewed verified by ORBi
Funding text :
We gratefully acknowledge Sven Hellqvist and Martin Barrlund for collecting Lampronia capitella larvae and Erling Jirle for technical assistance; Charles Martin for providing the ole1 yeast strain; Roger Schneiter for providing the ole1 elo1 yeast strain; Joanne Caine for providing the pYEX-CHT vector; Wendell Roelofs for stimulating discussions and Douglas Knipple for providing the YEpOLEX plasmid; Jure Piškur for supervision and valuable advice in heterologous expression; Aleš Svatoš for advice regarding the MTAD reaction; Jean-Marc Lassance for valuable advice in GC-MS analyses and comments on the manuscript and Fredrik Andersson and Anna Nilsson for contributing to methyl esters synthesis. Three anonymous referees are acknowledged for valuable comments on a previous version of this manuscript. This work was supported by the Swedish Research Council (VR) (for CL) and EU (Objective 1 the region of South Forest Countries) and Länss-tyrelsen i Västernorrlands län (for EH).
M Scoble, The Lepidoptera: Form, function and diversity Oxford University Press, Oxford 1992
D Grimaldi MS Engel, Evolution of the insects Cambridge University Press 2005
Chemistry of sex attraction. WL Roelofs, Proc Natl Acad Sci USA 1995 92 44 49 7816846 10.1073/pnas.92.1.44
The pherobase: Database of Insect pheromones and semiochemicals. AM El-Sayed, 2007 http://www.pherobase.com/
Biology and ultrastructure of sex pheromone producing glands. JE Percy-Cunningham JA MacDonald, Pheromone biochemistry 1987 27 76
Sex pheromone biosynthesis in Trichoplusia ni: key steps involve delta-11 desaturation and chain-shortening. LB Bjostad WL Roelofs, Science 1983 220 1387 1389 10.1126/science.220.4604.1387 17730655
Pheromone biosynthesis in lepidopterans: desaturation and chain shortening. LB Bjostad W Wolf WL Roelofs, Pheromone Biochemistry Academic Press, New-York, Blomquist GJ, Prestwich GD, 1987 77 120
Biosynthesis and endocrine regulation of fatty acid derived pheromones in moths. RA Jurenka WL Roelofs, Insect lipids: chemistry, biochemistry and biology University of Nebraska Press, Lincoln, Nebraska, Stanley-Samuelson DW, Nelson DR, 1993 353 388
Insect pheromones-an overview of biosynthesis and endocrine regulation. JA Tillman SJ Seybold RA Jurenka GJ Blomquist, Insect Biochem Molec Biol 1999 29 481 514 10.1016/S0965-1748(99)00016-8
Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. WL Roelofs AP Rooney, Proc Natl Acad Sci USA 2003 100 9179 9184 10.1073/pnas.1233767100 12876197
Plant acyl lipids: structure, distribution and analysis. JL Harwood, The biochemistry of plants Academic Press, New-York, Stumpf PK, Conn EE, 1980 1 55
The OLE1 gene of Saccharomyces cerevisiae encodes the Δ9 fatty acid desaturase and can be functionally replaced by the rat stearoyl-CoA desaturase gene. JE Stuckey VM McDonough CE Martin, J Biol Chem 1990 265 20144 20149 1978720
Eight histidine residues are catalytically essential in a membrane-associated iron enzyme, stearoyl-CoA desaturase, and are conserved in alkane hydroxylase and xylene monooxygenase. J Shanklin E Whittle BG Fox, Biochemistry 1994 33 12787 12794 10.1021/bi00209a009 7947684
Desaturation and related modifications of fatty acids. J Shanklin EB Cahoon, Annu Rev Plant Physiol Mol Biol 1998 49 611 641 10.1146/annurev.arplant. 49.1.611
Evolution of the integral membrane desaturase gene family in moths and flies. DC Knipple C-L Rosenfield R Nielsen KM You SE Jeong, Genetics 2002 162 1737 1752 12524345
Biosynthesis of Lepidopteran pheromones. WL Roelofs L Bjostad, Bioorg Chem 1984 12 279 298 10.1016/0045-2068(84)90011-7
Cloning and functional expression of a cDNA encoding a pheromone gland-specific acyl-CoA Delta11-desaturase of the cabbage looper moth, Trichoplusia ni. DC Knipple C-L Rosenfield SJ Miller W Liu J Tang PWK Ma WL Roelofs, Proc Natl Acad Sci USA 1998 95 15287 15292 9860961 10.1073/pnas.95.26. 15287
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. C-L Rosenfield KM You DC Knipple, Insect Biochem Molec Biol 2001 31 949 964 10.1016/S0965-1748(01)00043-1
Acyl-CoA Z9- and Z10-desaturase genes from a New Zealand leafroller moth species, Planotortrix octo. G Hao W Liu M O'Connor WL Roelofs, Insect Biochem Molec Biol 2001 32 961 966 10.1016/S0965-1748(01)00176-X
Characterization of Z/E11- and Z9-desaturases from the obliquebanded leafroller moth, Choristoneura rosaceana. G Hao M O'Connor W Liu WL Roelofs, J Ins Sci 2002 2 26 32
Evolution of moth sex pheromones via ancestral genes. WL Roelofs W Liu G Hao H Jiao AP Rooney CEJr Linn, Proc Natl Acad Sci USA 2002 99 13621 26 10.1073/pnas.152445399 12237399
Cloning and functional expression of a cDNA encoding a metabolic acyl-CoA Δ9-desaturase of the cabbage looper moth, Trichoplusia ni. W Liu PWK Ma P Marsella-Herrick C-L Rosenfield DC Knipple WL Roelofs, Insect Biochem Molec Biol 1999 29 435 443 10.1016/S0965-1748(99)00020-X
Moth desaturase characterized that produces both Z and E isomers of Δ11-tetradecenoic acids. W Liu H Jiao M O'Connor WL Roelofs, Insect Biochem Molec Biol 2002 32 1489 1495 10.1016/S0965-1748(02)00069-3
Gene characterized for membrane desaturase that produces (E)-11 isomers of mono- and diunsaturated fatty acids. W Liu H Jiao NC Murray M O'Connor WL Roelofs, Proc Natl Acad Sci USA 2002 99 620 624 11805319 10.1073/pnas.221601498
Desaturases from the spotted fireworm moth (Choristoneura parallela) shed light on the evolutionary origins of novel moth sex pheromone desaturases. W Liu AP Rooney B Xue WL Roelofs, Gene 2004 342 303 311 15527989 10.1016/j.gene.2004.08.017
Multiple acyl-CoA desaturase-encoding transcripts in pheromone glands of Helicoverpa assulta, the oriental tobacco budworm. SE Jeong C-L Rosenfield P Marsella-Herrick KM You DC Knipple, Insect Biochem Molec Biol 2003 33 609 622 10.1016/S0965-1748(03)00043-2
Involvement of a bifunctional fatty-acyl desaturase in the biosynthesis of the silkmoth, Bombyx mori, sex pheromone. K Moto MG Suzuki JJ Hull R Kurata S Takahashi M Yamamoto K Okano K Imai T Ando S Matsumoto, Proc Natl Acad Sci USA 2004 101 8631 8636 10.1073/pnas.0402056101 15173596
Expression and evolution of Δ9 and Δ11 desaturase genes in the moth Spodoptera littoralis. S Rodríguez G Hao W Liu B Pĩa AP Rooney F Camps WL Roelofs G Fabriàs, Insect Biochem Molec Biol 2004 34 1315 1328 10.1016/j.ibmb.2004.09.003
Biosynthesis of 10,12-dienoic fatty acids by a bifunctional Δ11 desaturase in Spodoptera littoralis. M Serra B Pĩa J Bujons F Camps G Fabriàs, Insect Biochem Molec Biol 2006 36 634 641 10.1016/j.ibmb.2006.05.005
A multifunctional desaturase involved in the biosynthesis of the processionary moth sex pheromone. M Serra B Pĩa JL Abad F Camps G Fabriàs, Proc Natl Acad Sci USA 2007 104 16444 16449 10.1073/pnas. 0705385104 17921252
Functional characterization of a desaturase from the tobacco hornworm moth (Manduca sexta) with bifunctional Z11 and 10,12-desaturase activity. P Matoušková I Pichová A Svatoš Insect Biochem Molec Biol 2007 37 601 610 10.1016/j.ibmb.2007.03.004
An abundant Acyl-CoA (Δ9) desaturase transcript in pheromone glands of the cabbage moth Mamestra brassicae, encodes a catalytically inactive protein. HY Park MS Kim A Paek SE Jeong DC Knipple, Insect Biochem Molec Biol 2008 38 581 595 10.1016/j.ibmb.2008.01.005
Novel type of sex pheromone structure identified from Stigmella malella (Stainton) (Lepidoptera: Nepticulidae). M Tóth G Szöcs EJ van Nieukerken P Philipp F Schmidt W Francke, J Chem Ecol 1994 21 13 23 10.1007/BF02033659
Identification of a novel moth sex-pheromone in Eriocrania cicatricella (Zett.) (Lepidoptera: Eriocraniidae) and its phylogenetic implications. J Zhu MV Kozlov P Philipp W Francke C Löfstedt, J Chem Ecol 1995 21 29 43 10.1007/BF02033660
Pheromone specificity in Eriocrania semipurpurella (Stephens) and E. sangii (Wood) (Lepidoptera: Eriocraniidae) based on chirality of semiochemicals. MV Koslov J Zhu P Philipp W Francke EL Zvereva BS Hansson C Löfstedt, J Chem Ecol 1996 22 431 454 10.1007/BF02033647
Evolution of mate-signalling in moths: phylogenetic considerations and predictions from the asymmetric tracking hypothesis. PL Phelan, The evolution of mating systems in Insects and Arachnids 1997 240 256
Identification of the sex pheromone of the currant shoot borer Lampronia capitella. C Löfstedt J Zhu MV Kozlov V Buda EV Jirle S Hellqvist J Löfqvist E Plass S Franke W Francke, J Chem Ecol 2004 30 643 657 10.1023/B:JOEC.0000018635.40128.2e 15139314
A phylogenetic analysis of pheromone communication in primitive moths. C Löfstedt M Kozlov, Insect pheromone research 1997 473 489
Saccharomyces cerevisiae expression vectors with thrombin-cleavable N- and C-terminal 6x(His) tags. O Patel R Fernley I Macreadie, Biotechnol Lett 2003 25 331 334 10.1023/A:1022384828795 12882547
Elo1-dependent carboxy-terminal elongation of C14:1Delta(9) to C16:1Delta(11) fatty acids in Saccharomyces cerevisiae. R Schneiter V Tatzer G Gogg E Leitner SD Kohlwein, J Bacteriol 2000 182 3655 3660 10.1128/JB.182.13. 3655-3660.2000 10850979
Gas chromatographic analysis of Diels-Alder adducts of geometrical and positional isomers of conjugated linoleic acid. JTM Reaney YD Liu WG Taylor, JAOCS 2001 78 1083 1086 10.1007/s11746-001-0393-x
Mechanisms of thermal adaptation in bacteria: blueprints for survival. JN Russel, Trends Biochem Sci 1984 9 108 112 10.1016/0968-0004(84)90106-3
Fatty feedback and fluidity. B Maresca AR Cossins, Nature 1993 365 606 607 8413623 10.1038/365606a0
The temperature-dependent expression of the desaturase gene desA in Synechocystis PCC6803. D Los I Horvath L Vigh N Murata, FEBS lett 1993 318 57 60 10.1016/0014-5793(93)81327-V 8436227
Gene duplication: The genomic trade in spare parts. M Hurles, PLoS Biol 2004 2 900 904 10.1371/journal.pbio.0020206
S Ohno, Evolution by Gene Duplication Springer-Verlag, Berlin-Heidelberg-New York 1970
The evolution of functionally novel proteins after gene duplication. AL Hughes, Proc R Soc Lond B Biol Sci 1994 256 119 124 10.1098/rspb.1994.0058
The probability of preservation of a newly arisen gene duplicate. M Lynch M O'Hely B Walsh A Force, Genetics 2001 159 1789 1804 11779815
An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. MW Gaunt MA Miles, Mol Biol Evol 2002 19 748 761 11961108
A delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. R Dallerac C Labeur JM Jallon DC Knipple WL Roelofs C Wicker-Thomas, Proc Natl Acad Sci USA 2000 97 9449 9454 10.1073/pnas.150243997 10920187
Concerted birth-and-death evolution of multigene families. M Nei AP Rooney, Annu Rev Genet 2005 39 121 152 10.1146/annurev.genet.39.073003.112240 16285855
Structure of the pheromone communication channels in moths. RT Cardé KF Haynes, Advances in insect chemical ecology Cambridge University Press, Cardé RT, Millar JG, 2004 283 332
Moth pheromone genetics and evolution. C Löfstedt, Phil Trans R Soc Lond B 1993 340 167 177 10.1098/rstb.1993.0055
Determination of double bond position in mono-unsaturated acetates by mass spectrometry of dimethyl disulfide adducts. H-R Buser H Arn P Guerin S Rauscher, Anal Chem 1983 55 818 822 10.1021/ac00257a003
Efficient method to locate double bond positions in conjugated trienes. FA Marques JG Millar S McElfresh, J Chromatogr A 2004 1048 59 65 15453419
2-Methylalkanoic acids resolved by esterification catalysed by lipase from Candida rugosa: Alcohol chain length and enantioselectivity. P Berglund M Holmquist E Hedenström K Hult H-E Högberg, Tetrahedron: Assymetry 1993 4 1869 1878 10.1016/S0957-4166(00)80427-9
BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. TA Hall, Nucl Acids Symp Ser 1999 41 95 98
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller DJ Lipman, Nucleic Acids Res 1997 25 3389 3402 10.1093/nar/25.17.3389 9254694
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. DJ Higgins JD Thompson TJ Gibson, Nucleic Acids Res 1994 22 4673 4680 7984417 10.1093/nar/22.22.4673
Printing and Shading of Multiple-Alignment files, BOXSHADE 3.21. http://www.ch.embnet.org/index.html
Prediction of protein sorting signals and localization sites in amino acid sequences (PSORT). http://psort.ims.u-tokyo.ac.jp/form2.html
National Centre for Biotechnology Information (NCBI). http://www.ncbi.nlm.nih.gov
MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. S Kumar K Tamura M Nei, Briefings in Bioinformatics 2004 5 150 163 10.1093/bib/5.2.150 15260895
