Artículo

De Panis, D.N.; Padró, J.; Furió-Tarí, P.; Tarazona, S.; Milla Carmona, P.S.; Soto, I.M.; Dopazo, H.; Conesa, A.; Hasson, E. "Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila" (2016) Molecular Ecology. 25(18):4534-4550
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Abstract:

High-throughput transcriptome studies are breaking new ground to investigate the responses that organisms deploy in alternative environments. Nevertheless, much remains to be understood about the genetic basis of host plant adaptation. Here, we investigate genome-wide expression in the fly Drosophila buzzatii raised in different conditions. This species uses decaying tissues of cactus of the genus Opuntia as primary rearing substrate and secondarily, the necrotic tissues of the columnar cactus Trichocereus terscheckii. The latter constitutes a harmful host, rich in mescaline and other related phenylethylamine alkaloids. We assessed the transcriptomic responses of larvae reared in Opuntia sulphurea and T. terscheckii, with and without the addition of alkaloids extracted from the latter. Whole-genome expression profiles were massively modulated by the rearing environment, mainly by the presence of T. terscheckii alkaloids. Differentially expressed genes were mainly related to detoxification, oxidation–reduction and stress response; however, we also found genes involved in development and neurobiological processes. In conclusion, our study contributes new data onto the role of transcriptional plasticity in response to alternative rearing environments. © 2016 John Wiley & Sons Ltd

Registro:

Documento: Artículo
Título:Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila
Autor:De Panis, D.N.; Padró, J.; Furió-Tarí, P.; Tarazona, S.; Milla Carmona, P.S.; Soto, I.M.; Dopazo, H.; Conesa, A.; Hasson, E.
Filiación:IEGEBA-CONICET, UNiversidad de Buenos Aires, FAcultad de Ciencias Exactas y Naturales, Intendente Güiraldes 2160, Ciudad Universitaria (C1428 EHA), CABA, Argentina
Genomics of Gene Expression Lab, Centro de Investigación Príncipe Felipe, Eduardo Primo Yúfera 3, Valencia, Spain
Department of Applied Statistics, Operations Research and Quality, Universitat Politècnica de València, Camí de Vera, Valencia, Spain
Laboratorio de Ecosistemas Marinos Fósiles, Instituto de Estudios Andinos Don Pablo Groeber (CONICET-UBA), Intendente Güiraldes 2160, Ciudad Universitaria (C1428 EHA), CABA, Argentina
Microbiology and Cell Science Department, Institute for Food and Agricultural Sciences, University of Florida at Gainesville, Gainesville, FL, United States
Palabras clave:alkaloids; environment adaptation; mescaline; plasticity; RNA-Seq
Año:2016
Volumen:25
Número:18
Página de inicio:4534
Página de fin:4550
DOI: http://dx.doi.org/10.1111/mec.13785
Título revista:Molecular Ecology
Título revista abreviado:Mol. Ecol.
ISSN:09621083
CODEN:MOECE
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09621083_v25_n18_p4534_DePanis

Referencias:

  • Adams, M.D., The genome sequence of Drosophila melanogaster (2000) Science, 287, pp. 2185-2195
  • Ali, J.G., Agrawal, A.A., Specialist versus generalist insect herbivores and plant defense (2012) Trends in Plant Science, 17, pp. 293-302
  • Aminetzach, Y.T., Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila (2005) Science, 309, pp. 764-767
  • Andrews, S., (2010) FastQC: a quality control tool for high throughput sequence data, , http://www.bioinformatics.babraham.ac.uk/projects/fastqc, Available from
  • Aranda, P.S., LaJoie, D.M., Jorcyk, C.L., Bleach gel: a simple agarose gel for analyzing RNA quality (2012) Electrophoresis, 33, pp. 366-369
  • Barker, J.S.F., Starmer, W.T., (1982) Ecological genetics and evolution: the cactus-yeast-Drosophila model system, , https://books.google.com/books/about/Ecological_genetics_and_evolution.html?id=soDwAAAAMAAJ, Academic Pr
  • Bates, D., Maechler, M., Bolker, B., Walker, S., lme4: Linear mixed-effects models using Eigen and S4 (2014) R package version, 1, p. 7
  • Bejsovec, A., Flying at the head of the pack: Wnt biology in Drosophila (2006) Oncogene, 25, pp. 7442-7449
  • Bergink, S., Jentsch, S., Principles of ubiquitin and SUMO modifications in DNA repair (2009) Nature, 458, pp. 461-467
  • Bogart, K., Andrews, J., (2006) Extraction of Total RNA from Drosophila, , Center for Genomics and Bioinformatics CGB Technical Report, 10
  • Bono, J.M., Matzkin, L.M., Castrezana, S., Markow, T.A., Molecular evolution and population genetics of two Drosophila mettleri cytochrome P450 genes involved in host plant utilization (2008) Molecular Ecology, 17, pp. 3211-3221
  • Carreira, V.P., Padró, J., Koch, N.M., Fontanarrosa, P., Alonso, I., Soto, I.M., Nutritional composition of Opuntia sulphurea G. Don Cladodes (2014) Haseltonia, 19, pp. 38-45
  • Celorio-Mancera, M., Wheat, C.W., Vogel, H., Söderlind, L., Janz, N., Nylin, S., Mechanisms of macroevolution: polyphagous plasticity in butterfly larvae revealed by RNA-Seq (2013) Molecular Ecology, 22, pp. 4884-4895
  • Clark, A.G., Eisen, M.B., Smith, D.R., Evolution of genes and genomes on the Drosophila phylogeny (2007) Nature, 450, pp. 203-218
  • Conesa, A., Götz, S., García-Gómez, J.M., Terol, J., Talón, M., Robles, M., Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research (2005) Bioinformatics, 21, pp. 3674-3676
  • Corio, C., Soto, I.M., Carreira, V., Padró, J., Betti, M.I., Hasson, E., An alkaloid fraction extracted from the cactus Trichocereus terscheckii affects fitness in the cactophilic fly Drosophila buzzatii (Diptera: Drosophilidae) (2013) Biological Journal of the Linnean Society, 109, pp. 342-353
  • Danielsson, O., Jörnvall, H., Enzymogenesis”: classical liver alcohol dehydrogenase origin from the glutathione-dependent formaldehyde dehydrogenase line (1992) Proceedings of the National Academy of Sciences, 89, pp. 9247-9251
  • De Kort, C.A.D., Granger, N.A., Regulation of JH titers: the relevance of degradative enzymes and binding proteins (1996) Archives of Insect Biochemistry and Physiology, 33, pp. 1-26
  • De Leeuw, J., Mair, P., (2008) Multidimensional scaling using majorization: SMACOF in R, , https://escholarship.org/uc/item/6q9542qc
  • De, S., Teichmann, S.A., Babu, M.M., The impact of genomic neighborhood on the evolution of human and chimpanzee transcriptome (2009) Genome Research, 19, pp. 785-794
  • Després, L., David, J.-P., Gallet, C., The evolutionary ecology of insect resistance to plant chemicals (2007) Trends in Ecology & Evolution, 22, pp. 298-307
  • Dow, J.A.T., Davies, S.A., The Malpighian tubule: rapid insights from post-genomic biology (2006) Journal of Insect Physiology, 52, pp. 365-378
  • Etges, W.J., Trotter, M.V., Oliveira, C.C., Rajpurohit, S., Gibbs, A.G., Tuljapurkar, S., Deciphering life history transcriptomes in different environments (2015) Molecular Ecology, 24, pp. 151-179
  • Fanara, J.J., Hasson, E., Oviposition acceptance and fecundity schedule in the cactophilic sibling species Drosophila buzzatii and D. koepferae on their natural hosts (2001) Evolution, 55, pp. 2615-2619
  • Fanara, J.J., Fontdevila, A., Hasson, E., Oviposition preference and life history traits in cactophilic Drosophila koepferae and D. buzzatii in association with their natural hosts (1999) Evolutionary Ecology, 13, pp. 173-190
  • Fanara, J.J., Folguera, G., Iriarte, P.F., Mensch, J., Hasson, E., Genotype by environment interactions in viability and developmental time in populations of cactophilic Drosophila (2006) Journal of Evolutionary Biology, 19, pp. 900-908
  • Feder, M.E., Walser, J.-C., The biological limitations of transcriptomics in elucidating stress and stress responses (2005) Journal of Evolutionary Biology, 18, pp. 901-910
  • Feyereisen, R., Insect P450 enzymes (1999) Annual Review of Entomology, 44, pp. 507-533
  • Fogleman, J.C., Danielson, P.B., Chemical interactions in the cactus-microorganism-Drosophila model system of the Sonoran Desert (2001) American Zoologist, 41, pp. 877-889
  • Fredholm, B.B., Bättig, K., Holmén, J., Nehlig, A., Zvartau, E.E., Actions of caffeine in the brain with special reference to factors that contribute to its widespread use (1999) Pharmacological Reviews, 51, pp. 83-133
  • Goldman-Huertas, B., Mitchell, R.F., Lapoint, R.T., Faucher, C.P., Hildebrand, J.G., Whiteman, N.K., Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet (2015) Proceedings of the National Academy of Sciences, 112, pp. 3026-3031
  • Grimaldi, D., Engel, M.S., (2005) Evolution of the Insects, , Cambridge University Press, New York
  • Guillén, Y., Rius, N., Delprat, A., Genomics of ecological adaptation in cactophilic Drosophila (2015) Genome Biology and Evolution, 7, pp. 349-366
  • Hasson, E., Naveira, H., Fontdevila, A., The breeding sites of Argentinian cactophilic species of the Drosophila mulleri complex (subgenus Drosophila-repleta group) (1992) Revista Chilena de Historia Natural (Valparaíso, Chile : 1983), 65, pp. 319-326
  • Hasson, E., Rodriguez, C., Fanara, J.J., Naveira, H., Reig, O.A., Fontdevila, A., The evolutionary history of Drosophila buzzatti. XXVI. Macrogeographic patterns of inversion polymorphism in New World populations (1995) Journal of Evolutionary Biology, 8, pp. 369-384
  • Hoang, K., Matzkin, L.M., Bono, J.M., Transcriptional variation associated with cactus host plant adaptation in Drosophila mettleri populations (2015) Molecular Ecology, 24, pp. 5186-5199
  • Hoffmann, A.A., Hercus, M.J., Environmental stress as an evolutionary force (2000) BioScience, 50, pp. 217-226
  • Jiang, J.Q., Ye, W.C., Liu, Y.H., Chen, Z., Min, Z.D., Lou, F.C., [A new alkaloid from Opuntia vulgaris] (2003) Yao xue xue bao = Acta pharmaceutica Sinica, 38, pp. 677-679
  • Li, B., Dewey, C.N., RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome (2011) BMC Bioinformatics, 12, p. 1
  • Li, H.-M., Buczkowski, G., Mittapalli, O., Transcriptomic profiles of Drosophila melanogaster third instar larval midgut and responses to oxidative stress (2008) Insect Molecular Biology, 17, pp. 325-339
  • Low, W.Y., Ng, H.L., Morton, C.J., Parker, M.W., Batterham, P., Robin, C., Molecular evolution of glutathione S-transferases in the genus Drosophila (2007) Genetics, 177, pp. 1363-1375
  • Manfrin, M.H., Sene, F.M., Cactophilic Drosophila in South America: a model for evolutionary studies (2006) Genetica, 126, pp. 57-75
  • Markow, T.A., O'Grady, P.M., Drosophila biology in the genomic age (2007) Genetics, 177, pp. 1269-1276
  • Markow, T.A., O'Grady, P., Reproductive ecology of Drosophila (2008) Functional Ecology, 22, pp. 747-759
  • Matzkin, L.M., The molecular basis of host adaptation in cactophilic Drosophila: molecular evolution of a glutathione S-transferase gene (GstD1) in Drosophila mojavensis (2008) Genetics, 178, pp. 1073-1083
  • Matzkin, L.M., Population transcriptomics of cactus host shifts in Drosophila mojavensis (2012) Molecular Ecology, 21, pp. 2428-2439
  • Matzkin, L.M., Watts, T.D., Bitler, B.G., Machado, C.A., Markow, T.A., Functional genomics of cactus host shifts in Drosophila mojavensis (2006) Molecular Ecology, 15, pp. 4635-4643
  • Merilä, J., Hendry, A.P., Climate change, adaptation, and phenotypic plasticity: the problem and the evidence (2014) Evolutionary Applications, 7, pp. 1-14
  • Muratani, M., Tansey, W.P., How the ubiquitin–proteasome system controls transcription (2003) Nature Reviews Molecular Cell Biology, 4, pp. 192-201
  • Nobel, P.S., (2002) Cacti: Biology and Uses, , University of California Press, Berkeley
  • Ogunbodede, O., McCombs, D., Trout, K., Daley, P., Terry, M., New mescaline concentrations from 14 taxa/cultivars of Echinopsis spp. (Cactaceae) (“San Pedro”) and their relevance to shamanic practice (2010) Journal of Ethnopharmacology, 131, pp. 356-362
  • Oliveira, D.C., Almeida, F.C., O'Grady, P.M., Armella, M.A., DeSalle, R., Etges, W.J., Monophyly, divergence times, and evolution of host plant use inferred from a revised phylogeny of the Drosophila repleta species group (2012) Molecular Phylogenetics and Evolution, 64, pp. 533-544
  • Padró, J., Soto, I.M., Exploration of the nutritional profile of Trichocereus terscheckii (Parmentier) Britton & Rose stems (2013) Journal of the Professional Association for Cactus Development, 15, pp. 1-12
  • Padró, J., Carreira, V., Corio, C., Hasson, E., Soto, I.M., Host alkaloids differentially affect developmental stability and wing vein canalization in cactophilic Drosophila buzzatii (2014) Journal of Evolutionary Biology, 27, pp. 2781-2797
  • Parsons, P.A., Stanley, S.M., Spence, G.E., Environmental ethanol at low concentrations: longevity and development in the sibling species Drosophila melanogaster and D. simulans (1979) Australian Journal of Zoology, 27, pp. 747-754
  • Qiu, Y., Tittiger, C., Wicker-Thomas, C., An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis (2012) Proceedings of the National Academy of Sciences, 109, pp. 14858-14863
  • Radyuk, S.N., Klichko, V.I., Spinola, B., Sohal, R.S., Orr, W.C., The peroxiredoxin gene family in Drosophila melanogaster (2001) Free Radical Biology and Medicine, 31, pp. 1090-1100
  • Ragland, G.J., Almskaar, K., Vertacnik, K.L., Differences in performance and transcriptome-wide gene expression associated with Rhagoletis (Diptera: Tephritidae) larvae feeding in alternate host fruit environments (2015) Molecular Ecology, 24, pp. 2759-2776
  • Reti, L., Castrillón, J.A., Cactus alkaloids. I. Trichocereus terscheckii (Parmentier) Britton and Rose (1951) Journal of the American Chemical Society, 73, pp. 1767-1769
  • Rewitz, K.F., Rybczynski, R., Warren, J.T., Gilbert, L.I., The Halloween genes code for cytochrome P450 enzymes mediating synthesis of the insect moulting hormone (2006) Biochemical Society Transactions, 34, pp. 1256-1260
  • Roelofs, D., Morgan, J., Stürzenbaum, S., The significance of genome-wide transcriptional regulation in the evolution of stress tolerance (2010) Evolutionary Ecology, 24, pp. 527-539
  • Roy, S., Ernst, J., Kharchenko, P.V., Identification of functional elements and regulatory circuits by Drosophila modENCODE (2010) Science, 330, pp. 1787-1797
  • Ruiz, A., Heed, W.B., Host-plant specificity in the cactophilic Drosophila mulleri species complex (1988) The Journal of Animal Ecology, 57, p. 237
  • Schoonhoven, L.M., Van Loon, J.J., Dicke, M., (2005) Insect–Plant Biology, , Oxford University Press, Oxford
  • Shang, F., Taylor, A., Ubiquitin–proteasome pathway and cellular responses to oxidative stress (2011) Free Radical Biology and Medicine, 51, pp. 5-16
  • Smith, G., Fang, Y., Liu, X., Transcriptome-wide expression variation associated with environmental plasticity and mating success in cactophilic Drosophila mojavensis (2013) Evolution, 67, pp. 1950-1963
  • Soto, I.M., Carreira, V.P., Soto, E.M., Hasson, E., Wing morphology and fluctuating asymmetry depend on the host plant in cactophilic Drosophila (2008) Journal of Evolutionary Biology, 21, pp. 598-609
  • Soto, E.M., Goenaga, J., Hurtado, J.P., Hasson, E., Oviposition and performance in natural hosts in cactophilic Drosophila (2012) Evolutionary Ecology, 26, pp. 975-990
  • Soto, I.M., Carreira, V.P., Corio, C., Padró, J., Soto, E.M., Hasson, E., Differences in tolerance to host cactus alkaloids in Drosophila koepferae and D. buzzatii (2014) PLoS One, 9
  • Supek, F., Bošnjak, M., Škunca, N., Šmuc, T., REVIGO summarizes and visualizes long lists of gene ontology terms (2011) PLoS One, 6
  • Tarazona, S., Garcia-Alcalde, F., Dopazo, J., Ferrer, A., Conesa, A., Differential expression in RNA-seq: a matter of depth (2011) Genome Research, 21, pp. 2213-2223
  • Tarazona, S., Furió-Tarí, P., Turrà, D., Di Pietro, A., Nueda, M.J., Ferrer, A., Conesa, A., Data quality aware analysis of differential expression in RNA-seq with NOISeq R/Bioc package (2015) Nucleic acids research, 43, p. 21
  • Team, R.C., (2015) R: A Language and Environment for Statistical Computing, , http://www.R-project.org, R Foundation for Statistical Computing, Vienna, 2012. Available from
  • Throckmorton, L.H., The phylogeny, ecology and geography of Drosophila (1975) Handbook of Genetics, 3, pp. 421-469
  • Tilmon, K.J., (2008) Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects, , University of California Press, Berkeley
  • Tu, C.D., Akgül, B., Drosophila glutathione S transferases (2005) Methods in Enzymology, 401, pp. 204-226
  • Ujváry, I., Nicotine and other insecticidal alkaloids (1999) Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor, pp. 29-69. , In, (eds, Yamamoto I, Casida JE, Springer Japan, Tokyo
  • Ulukan, H., Swaan, P.W., Camptothecins (2002) Drugs, 62, pp. 2039-2057
  • Reorganizing the protein space at the universal protein resource (UniProt) (2011) Nucleic Acids Research, 40, pp. D71-D75
  • Vogel, H., Musser, R.O., Celorio-Mancera, M., Transcriptome responses in herbivorous insects towards host plant and toxin feeding (2014) Annual Plant Reviews, 47, pp. 197-233
  • Wasserman, M., Evolution of the repleta group (1982) The Genetics and Biology of Drosophila, 3b, pp. 61-140. , In, (eds, Ashburner M, Carson HL, Academic Press, London
  • Willoughby, L., Chung, H., Lumb, C., Robin, C., Batterham, P., Daborn, P.J., A comparison of Drosophila melanogaster detoxification gene induction responses for six insecticides, caffeine and phenobarbital (2006) Insect Biochemistry and Molecular Biology, 36, pp. 934-942
  • Wojtasek, H., Prestwich, G.D., An insect juvenile hormone-specific epoxide hydrolase is related to vertebrate microsomal epoxide hydrolases (1996) Biochemical and Biophysical Research Communications, 220, pp. 323-329
  • Yamanaka, N., Rewitz, K.F., O'Connor, M.B., Ecdysone control of developmental transitions: lessons from Drosophila research (2013) Annual Review of Entomology, 58, pp. 497-516
  • Yang, P., Tanaka, H., Kuwano, E., Suzuki, K., A novel cytochrome P450 gene (CYP4G25) of the silkmoth Antheraea yamamai: cloning and expression pattern in pharate first instar larvae in relation to diapause (2008) Journal of Insect Physiology, 54, pp. 636-643
  • Young, M.D., Wakefield, M.J., Smyth, G.K., Oshlack, A., Method gene ontology analysis for RNA-seq: accounting for selection bias (2010) Genome Biology, 11, p. R14
  • Zou, D., Coudron, T.A., Liu, C., Zhang, L., Wang, M., Chen, H., Nutrigenomics in Arma chinensis: transcriptome analysis of Arma chinensis fed on artificial diet and Chinese oak silk moth Antheraea pernyi pupae (2013) PLoS One, 8

Citas:

---------- APA ----------
De Panis, D.N., Padró, J., Furió-Tarí, P., Tarazona, S., Milla Carmona, P.S., Soto, I.M., Dopazo, H.,..., Hasson, E. (2016) . Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila. Molecular Ecology, 25(18), 4534-4550.
http://dx.doi.org/10.1111/mec.13785
---------- CHICAGO ----------
De Panis, D.N., Padró, J., Furió-Tarí, P., Tarazona, S., Milla Carmona, P.S., Soto, I.M., et al. "Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila" . Molecular Ecology 25, no. 18 (2016) : 4534-4550.
http://dx.doi.org/10.1111/mec.13785
---------- MLA ----------
De Panis, D.N., Padró, J., Furió-Tarí, P., Tarazona, S., Milla Carmona, P.S., Soto, I.M., et al. "Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila" . Molecular Ecology, vol. 25, no. 18, 2016, pp. 4534-4550.
http://dx.doi.org/10.1111/mec.13785
---------- VANCOUVER ----------
De Panis, D.N., Padró, J., Furió-Tarí, P., Tarazona, S., Milla Carmona, P.S., Soto, I.M., et al. Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila. Mol. Ecol. 2016;25(18):4534-4550.
http://dx.doi.org/10.1111/mec.13785