The early embryonic transcriptome of a Hawaiian Drosophila picture-wing fly shows evidence of altered gene expression and novel gene evolution.
Hawaiian Drosophila
Hox genes
de novo genes
embryo
maternal-to-zygotic-transition
novel genes
transcriptomics
Journal
Journal of experimental zoology. Part B, Molecular and developmental evolution
ISSN: 1552-5015
Titre abrégé: J Exp Zool B Mol Dev Evol
Pays: United States
ID NLM: 101168228
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
revised:
14
01
2022
received:
15
10
2021
accepted:
13
02
2022
pubmed:
25
3
2022
medline:
22
6
2022
entrez:
24
3
2022
Statut:
ppublish
Résumé
A massive adaptive radiation on the Hawaiian archipelago has produced approximately one-quarter of the fly species in the family Drosophilidae. The Hawaiian Drosophila clade has long been recognized as a model system for the study of both the ecology of island endemics and the evolution of developmental mechanisms, but relatively few genomic and transcriptomic datasets are available for this group. We present here a differential expression analysis of the transcriptional profiles of two highly conserved embryonic stages in the Hawaiian picture-wing fly Drosophila grimshawi. When we compared our results to previously published datasets across the family Drosophilidae, we identified cases of both gains and losses of gene representation in D. grimshawi, including an apparent delay in Hox gene activation. We also found a high expression of unannotated genes. Most transcripts of unannotated genes with open reading frames do not have identified homologs in non-Hawaiian Drosophila species, although the vast majority have sequence matches in genomes of other Hawaiian picture-wing flies. Some of these unannotated genes may have arisen from noncoding sequence in the ancestor of Hawaiian flies or during the evolution of the clade. Our results suggest that both the modified use of ancestral genes and the evolution of new ones may occur in rapid radiations.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
277-291Subventions
Organisme : Louisiana Board of Regents
ID : LEQSF(2017-20)-RD-A-26
Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
Atallah, J., & Lott, S. E. (2018). Evolution of maternal and zygotic mRNA complements in the early Drosophila embryo. PLoS Genetics, 14(12), e1007838. https://doi.org/10.1371/journal.pgen.1007838
Bownes, M. (1975). A photographic study of development in the living embryo of Drosophila melanogaster. Journal of Embryology and Experimental Morphology, 33(3), 789-801.
Carroll, S. B. (2008). Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution. Cell, 134(1), 25-36. https://doi.org/10.1016/j.cell.2008.06.030
Chen, S., Zhang, Y. E., & Long, M. (2010). New genes in Drosophila quickly become essential. Science, 330(6011), 1682-1685. https://doi.org/10.1126/science.1196380
Clark, A. G., Eisen, M. B., Smith, D. R., Bergman, C. M., Oliver, B., Markow, T. A., Kaufman, T. C., Kellis, M., Gelbart, W., Iyer, V. N., Pollard, D. A., Sackton, T. B., Larracuente, A. M., Singh, N. D., Abad, J. P., Abt, D. N., Adryan, B., Aguade, M., … Newfeld, S. (2007). Evolution of genes and genomes on the Drosophila phylogeny. Nature, 450(7167), 203-218. https://doi.org/10.1038/nature06341
Combs, P. A., & Eisen, M. B. (2013). Sequencing mRNA from cryo-sliced Drosophila embryos to determine genome-wide spatial patterns of gene expression. PLoS One, 8(8), e71820. https://doi.org/10.1371/journal.pone.0071820
Corbett-Detig, R. B., Russell, S. L., Nielsen, R., & Losos, J. (2020). Phenotypic convergence is not mirrored at the protein level in a lizard adaptive radiation. Molecular Biology and Evolution, 37(6), 1604-1614. https://doi.org/10.1093/molbev/msaa028
Craddock, E. M., Kambysellis, M. P., Franchi, L., Francisco, P., Grey, M., Hutchinson, A., Nanhoo, S., & Antar, S. (2018). Ultrastructural variation and adaptive evolution of the ovipositor in the endemic Hawaiian Drosophilidae. Journal of Morphology, 279(12), 1725-1752. https://doi.org/10.1002/jmor.20884
Darwin, C. (1845). Journal of researches into the natural history and geology of the countries visited during the voyage of H.M.S. Beagle round the world. John Murray.
Doudna, J. A., & Charpentier, E. (2014). The new frontier of genome engineering with CRISPR-Cas9. Science, 346(6213), 1258096. https://doi.org/10.1126/science.1258096
Edwards, K. A., Doescher, L. T., Kaneshiro, K. Y., & Yamamoto, D. (2007). A database of wing diversity in the Hawaiian Drosophila. PLoS One, 2(5), e487. https://doi.org/10.1371/journal.pone.0000487
Eldon, J., Bellinger, M. R., & Price, D. K. (2019). Hawaiian picture-winged Drosophila exhibit adaptive population divergence along a narrow climatic gradient on Hawaii Island. Ecology and Evolution, 9(5), 2436-2448. https://doi.org/10.1002/ece3.4844
Haas, B. J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P. D., Bowden, J., Couger, M. B., Eccles, D., Li, B., Lieber, M., MacManes, M. D., Ott, M., Orvis, J., Pochet, N., Strozzi, F., Weeks, N., Westerman, R., William, T., Dewey, C. N., … Regev, A. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols, 8(8), 1494-1512. https://doi.org/10.1038/nprot.2013.084
Hahn, M. W., Han, M. V., & Han, S.-G. (2007). gene family evolution across 12 Drosophila genomes. PLoS Genetics, 3(11), 197. https://doi.org/10.1371/journal.pgen.0030197
Heames, B., Schmitz, J., & Bornberg-Bauer, E. (2020). A continuum of evolving de novo genes drives protein-coding novelty in Drosophila. Journal of Molecular Evolution, 88(4), 382-398. https://doi.org/10.1007/s00239-020-09939-z
Horváth, B., & Kalinka, A. T. (2018). The genetics of egg retention and fertilization success in Drosophila: One step closer to understanding the transition from facultative to obligate viviparity. Evolution, 72(2), 318-336. https://doi.org/10.1111/evo.13411
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009a). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4(1), 44-57. https://doi.org/10.1038/nprot.2008.211
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009b). Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research, 37(1), 1-13. https://doi.org/10.1093/nar/gkn923
Hunter, S., Apweiler, R., Attwood, T. K., Bairoch, A., Bateman, A., Binns, D., Bork, P., Das, U., Daugherty, L., Duquenne, L., Finn, R. D., Gough, J., Haft, D., Hulo, N., Kahn, D., Kelly, E., Laugraud, A., Letunic, I., Lonsdale, D., … Yeats, C. (2009). InterPro: The integrative protein signature database. Nucleic Acids Research, 37(suppl_1), D211-D215. https://doi.org/10.1093/nar/gkn785
Jagadeeshan, S., & Singh, R. S. (2005). Rapidly evolving genes of Drosophila: Differing levels of selective pressure in testis, ovary, and head tissues between sibling species. Molecular Biology and Evolution, 22(9), 1793-1801. https://doi.org/10.1093/molbev/msi175
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337(6096), 816-821. https://doi.org/10.1126/science.1225829
Johnson, B. R. (2018). Taxonomically restricted genes are fundamental to biology and evolution. Frontiers in Genetics, 9, 407. https://doi.org/10.3389/fgene.2018.00407
Kambysellis, M. P., & Heed, W. B. (1971). Studies of oogenesis in natural populations of Drosophilidae. I. Relation of ovarian development and ecological habitats of the Hawaiian species. The American Naturalist, 105(941), 31-49.
Kambysellis, M. P., Starmer, T., Smathers, G., & Heed, W. B. (1980). Studies of oogenesis in natural populations of Drosophilidae. II. Significance of microclimatic changes on oogenesis of Drosophila mimica. The American Naturalist, 115(1), 67-91.
Kang, L., Settlage, R., McMahon, W., Michalak, K., Tae, H., Garner, H. R., Stacy, E. A., Price, D. K., & Michalak, P. (2016). Genomic signatures of speciation in sympatric and allopatric Hawaiian picture-winged Drosophila. Genome Biology and Evolution, 8(5), 1482-1488. https://doi.org/10.1093/gbe/evw095
Katoh, T., Izumitani, H. F., Yamashita, S., & Watada, M. (2017). Multiple origins of Hawaiian Drosophilids: Phylogeography of Scaptomyza Hardy (Diptera: Drosophilidae). Entomological Science, 20(1), 33-44. https://doi.org/10.1111/ens.12222
Kim, B. Y., Wang, J. R., Miller, D. E., Barmina, O., Delaney, E., Thompson, A., Comeault, A. A., Peede, D., D'agostino, E. R., Pelaez, J., Aguilar, J. M., Haji, D., Matsunaga, T., Armstrong, E. E., Zych, M., Ogawa, Y., Stamenković-Radak, M., Jelić, M., Veselinović, M. S., … Petrov, D. A. (2021). Highly contiguous assemblies of 101 drosophilid genomes. eLife, 10, e66405. https://doi.org/10.7554/eLife.66405
Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., & Salzberg, S. L. (2013). TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology, 14, R36. https://doi.org/10.1186/gb-2013-14-4-r36
Klasberg, S., Bitard-Feildel, T., Callebaut, I., & Bornberg-Bauer, E. (2018). Origins and structural properties of novel and de novo protein domains during insect evolution. The FEBS journal, 285(14), 2605-2625. https://doi.org/10.1111/febs.14504
Kuntz, S. G., & Eisen, M. B. (2014). Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species. PLoS Genetics, 10(4), e1004293. https://doi.org/10.1371/journal.pgen.1004293
Lange, A., Patel, P. H., Heames, B., Damry, A. M., Saenger, T., Jackson, C. J., Findlay, G. D., & Bornberg-Bauer, E. (2021). Structural and functional characterization of a putative de novo gene in Drosophila. Nature Communications, 12(1), 1667. https://doi.org/10.1038/s41467-021-21667-6
Lapoint, R. T., Magnacca, K. N., & O'Grady, P. M. (2009). Review of the spoon tarsus subgroup of Hawaiian Drosophila (Drosophilidae: Diptera), with a description of one new species. Zootaxa, 2003, 53-68.
Lapoint, R. T., Magnacca, K. N., & O'Grady, P. M. (2014). Phylogenetics of the Antopocerus-Modified Tarsus Clade of Hawaiian Drosophila: Diversification across the Hawaiian Islands. PLoS One, 9(11), e113227. https://doi.org/10.1371/journal.pone.0113227
Lapoint, R. T., O'Grady, P. M., & Whiteman, N. K. (2013). Diversification and dispersal of the Hawaiian Drosophilidae: The evolution of Scaptomyza. Molecular Phylogenetics and Evolution, 69(1), 95-108. https://doi.org/10.1016/j.ympev.2013.04.032
Larkin, A., Marygold, S. J., Antonazzo, G., Attrill, H., dos Santos, G., Garapati, P. V., Goodman, J. L., Gramates, L. S., Millburn, G., Strelets, V. B., Tabone, C. J., & Thurmond, J., FlyBase Consortium. (2021). FlyBase: Updates to the Drosophila melanogaster knowledge base. Nucleic Acids Research, 49(D1), D899-D907. https://doi.org/10.1093/nar/gkaa1026
Losos, J. B., & Ricklefs, R. E. (2009). Adaptation and diversification on islands. Nature, 457(7231), 830-836. https://doi.org/10.1038/nature07893
Lott, S. E., Villalta, J. E., Zhou, Q., Bachtrog, D., & Eisen, M. B. (2014). Sex-Specific Embryonic gene expression in species with newly evolved sex chromosomes. PLoS Genetics, 10(2), e1004159. https://doi.org/10.1371/journal.pgen.1004159
Lu, T.-C., Leu, J.-Y., & Lin, W.-C. (2017). A comprehensive analysis of transcript-supported de novo genes in Saccharomyces sensu stricto yeasts. Molecular Biology and Evolution, 34(11), 2823-2838. https://doi.org/10.1093/molbev/msx210
Magnacca, K. N., & Grady, P. M. (2009). Revision of the Modified Mouthparts Species Group of Hawaiian Drosophila (Diptera: Drosophilidae): The Ceratostoma, Freycinetiae, Semifuscata, and Setiger Subgroups, and Unplaced Species (Vol. 130). University of California Press.
Magnacca, K. N., & Price, D. K. (2015). Rapid adaptive radiation and host plant conservation in the Hawaiian picture wing Drosophila (Diptera: Drosophilidae). Molecular Phylogenetics and Evolution, 92, 226-242. https://doi.org/10.1016/j.ympev.2015.06.014
Mahler, D. L., Lambert, S. M., Geneva, A. J., Ng, J., Hedges, S. B., Losos, J. B., & Glor, R. E. (2016). Discovery of a Giant Chameleon-Like Lizard (Anolis) on Hispaniola and its significance to understanding replicated adaptive radiations. The American Naturalist, 188(3), 357-364. https://doi.org/10.1086/687566
Mahler, D. L., Revell, L. J., Glor, R. E., & Losos, J. B. (2010). Ecological opportunity and the rate of morphological evolution in the diversification of Greater Antillean Anoles. Evolution, 64(9), 2731-2745. https://doi.org/10.1111/j.1558-5646.2010.01026.x
Margaritis, L. H., Dellas, K., Kalantzi, M. C., & Kambysellis, M. P. (1983). Eggshell of Hawaiian Drosophila: Structural and biochemical studies in Drosophila grimshawi and comparison to Drosophila melanogaster. Wilhelm Roux's Archives of Developmental Biology, 192, 303-316. https://scholar.google.com/scholar_lookup?title=eggshell%2Bof%2BHawaiian%2BDrosophila%3A%2Bstructural%2Band%2Bbiochemical%2Bstudies%2Bin%2BDrosophila%2Bgrimshawi%2Band%2Bcomparison%2Bto%2BDrosophila%2Bmelanogaster%26author=Margaritis,%2BL.H.%26publication_year=1983
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.Journal, 17(1), 10-12. https://doi.org/10.14806/ej.17.1.200
McCrea, P. D., Turck, C. W., & Gumbiner, B. (1991). A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science, 254(5036), 1359-1361.
McLysaght, A., & Guerzoni, D. (2015). New genes from non-coding sequence: The role of de novo protein-coding genes in eukaryotic evolutionary innovation. Philosophical Transactions of the Royal Society, B: Biological Sciences, 370(1678), 20140332. https://doi.org/10.1098/rstb.2014.0332
Mestek Boukhibar, L., & Barkoulas, M. (2016). The developmental genetics of biological robustness. Annals of Botany, 117(5), 699-707. https://doi.org/10.1093/aob/mcv128
Mohammed, J., Bortolamiol-Becet, D., Flynt, A. S., Gronau, I., Siepel, A., & Lai, E. C. (2014). Adaptive evolution of testis-specific, recently evolved, clustered miRNAs in Drosophila. RNA, 20(8), 1195-1209. https://doi.org/10.1261/rna.044644.114
Montgomery, S. L. (1975). Comparative breeding site ecology and the adaptive radiation of picture-winged Drosophila (Diptera: Drosophilidae) in Hawaii. Proceedings, Hawaiian Entomological Society, 22(1).
Neme, R., & Tautz, D. (2016). Fast turnover of genome transcription across evolutionary time exposes entire non-coding DNA to de novo gene emergence. eLife, 5, e09977. https://doi.org/10.7554/eLife.09977
O'Grady, P., & DeSalle, R. (2008). Out of Hawaii: The origin and biogeography of the genus Scaptomyza (Diptera: Drosophilidae). Biology Letters, 4(2), 195-199. https://doi.org/10.1098/rsbl.2007.0575
O'Grady, P., & DeSalle, R. (2018). Hawaiian Drosophila as an evolutionary model clade: Days of future past. BioEssays, 40(5), 1700246. https://doi.org/10.1002/bies.201700246
Paris, M., Villalta, J. E., Eisen, M. B., & Lott, S. E. (2015). Sex bias and maternal contribution to gene expression divergence in Drosophila blastoderm embryos. PLoS Genetics, 11(10), e1005592. https://doi.org/10.1371/journal.pgen.1005592
Peifer, M., Berg, S., & Reynolds, A. B. (1994). A repeating amino acid motif shared by proteins with diverse cellular roles. Cell, 76(5), 789-791. https://doi.org/10.1016/0092-8674(94)90353-0
Rothwell, W. F., & Sullivan, W. (2007). Fixation of Drosophila embryos. Cold Spring Harbor Protocols, 2007(9), pdb.prot4827. https://doi.org/10.1101/pdb.prot4827
Sarikaya, D. P., Church, S. H., Lagomarsino, L. P., Magnacca, K. N., Montgomery, S. L., Price, D. K., Kaneshiro, K. Y., & Extavour, C. G. (2019). Reproductive capacity evolves in response to ecology through common changes in cell number in Hawaiian Drosophila. Current Biology, 29(11), 1877-1884 e6. https://doi.org/10.1016/j.cub.2019.04.063
Schmid, K. J., & Aquadro, C. F. (2001). The evolutionary analysis of “Orphans” from the Drosophila genome identifies rapidly diverging and incorrectly annotated genes. Genetics, 159(2), 589-598. https://doi.org/10.1093/genetics/159.2.589
Stark, J. B., & O'Grady, P. M. (2010). Morphological variation in the forelegs of the Hawaiian Drosophilidae. I. The AMC clade. Journal of Morphology, 271(1), 86-103. https://doi.org/10.1002/jmor.10783
Stern, D. L. (2011). Evolution, development, & the predictable genome. Roberts and Co. Publishers. http://agris.fao.org/agris-search/search.do?recordID=US201300151702
Sun, W., Zhao, X.-W., & Zhang, Z. (2015). Identification and evolution of the orphan genes in the domestic silkworm, Bombyx mori. FEBS Letters, 589(19, Part B), 2731-2738. https://doi.org/10.1016/j.febslet.2015.08.008
Tadros, W., & Lipshitz, H. D. (2009). The maternal-to-zygotic transition: A play in two acts. Development, 136(18), 3033-3042. https://doi.org/10.1242/dev.033183
Thompson, J. D., Gibson, Toby J., & Higgins, D. G. (2003). Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics, 00(1), 2.3.1-2.3.22. https://doi.org/10.1002/0471250953.bi0203s00
Trapnell, C., Hendrickson, D. G., Sauvageau, M., Goff, L., Rinn, J. L., & Pachter, L. (2013). Differential analysis of gene regulation at transcript resolution with RNA-seq. Nature Biotechnology, 31(1), 46-53. https://doi.org/10.1038/nbt.2450
Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., & Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols, 7(3), 562-578. https://doi.org/10.1038/nprot.2012.016
Van Oss, S. B., & Carvunis, A.-R. (2019). De novo gene birth. PLoS Genetics, 15(5), e1008160. https://doi.org/10.1371/journal.pgen.1008160
Walter, W., Sánchez-Cabo, F., & Ricote, M. (2015). GOplot: An R package for visually combining expression data with functional analysis. Bioinformatics, 31(17), 2912-2914. https://doi.org/10.1093/bioinformatics/btv300
Wheeler, M. R., & Clayton, F. (1965). A new Drosophila culture technique. Drosophila Information Service, 40, 98.
Whittaker, R. J., Fernández-Palacios, J. M., Matthews, T. J., Borregaard, M. K., & Triantis, K. A. (2017). Island biogeography: Taking the long view of nature's laboratories. Science, 357(6354), https://doi.org/10.1126/science.aam8326
Witt, E., Benjamin, S., Svetec, N., & Zhao, L. (2019). Testis single-cell RNA-seq reveals the dynamics of de novo gene transcription and germline mutational bias in Drosophila. eLife, 8, e47138. https://doi.org/10.7554/eLife.47138
Xia, S., VanKuren, N. W., Chen, C., Zhang, L., Kemkemer, C., Shao, Y., Jia, H., Lee, U., Advani, A. S., Gschwend, A., Vibranovski, M. D., Chen, S., Zhang, Y. E., & Long, M. (2021). Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development. PLoS Genetics, 17(7), e1009654. https://doi.org/10.1371/journal.pgen.1009654
Xie, C., Zhang, Y. E., Chen, J.-Y., Liu, C.-J., Zhou, W.-Z., Li, Y., Zhang, M., Zhang, R., Wei, L., & Li, C.-Y. (2012). Hominoid-specific de novo protein-coding genes originating from long non-coding RNAs. PLoS Genetics, 8(9), e1002942. https://doi.org/10.1371/journal.pgen.1002942
Yang, H., Jaime, M., Polihronakis, M., Kanegawa, K., Markow, T., Kaneshiro, K., & Oliver, B. (2018). Re-annotation of eight Drosophila genomes. Life Science Alliance, 1(6), 201800156. https://doi.org/10.26508/lsa.201800156
Zhao, L., Saelao, P., Jones, C. D., & Begun, D. J. (2014). Origin and spread of de novo genes in Drosophila melanogaster populations. Science, 343(6172), 769-772. https://doi.org/10.1126/science.1248286
Zhong, Y., Jia, Y., Gao, Y., Tian, D., Yang, S., & Zhang, X. (2013). Functional requirements driving the gene duplication in 12 Drosophila species. BMC Genomics, 14(1), 555. https://doi.org/10.1186/1471-2164-14-555