Evolutionary study of duplications of the miRNA machinery in aphids associated with striking rate acceleration and changes in expression profiles

BMC Evolutionary Biology

Rispe Claude¹  Denis Tagu¹  Jean-Pierre Gauthier¹  Sylvie Tanguy¹  Stéphanie Jaubert-Possamai²  Benjamín Ortiz-Rivas¹ 

[1] INRA, UMR 1349 IGEPP, Le Rheu, 35653, France;INRA, UMR1355, Institut Sophia Agrobiotech, Sophia Antipolis, 06903, France

关键词: Neofunctionalization;    Gene duplication;    miRNAs;    Aphids;   

Others  :  1140102
DOI  :  10.1186/1471-2148-12-216

 received in 2012-06-11, accepted in 2012-11-04,  发布年份 2012

【 摘 要 】

Background

The sequencing of the genome of the pea aphid Acyrthosiphon pisum revealed an unusual expansion of the miRNA machinery, with two argonaute-1, two dicer-1 and four pasha gene copies. In this report, we have undertaken a deeper evolutionary analysis of the phylogenetic timing of these gene duplications and of the associated selective pressures by sequencing the two copies of ago-1 and dcr-1 in different aphid species of the subfamily Aphidinae. We have also carried out an analysis of the expression of both copies of ago-1 and dcr-1 by semi-quantitative PCR in different morphs of the pea aphid life cycle.

Results

The analysis has shown that the duplication of ago-1 occurred in an ancestor of the subfamily Aphidinae while the duplication of dcr-1 appears to be more recent. Besides, it has confirmed a pattern of one conserved copy and one accelerated copy for both genes, and has revealed the action of positive selection on several regions of the fast-evolving ago-1b. On the other hand, the semi-quantitative PCR experiments have revealed a differential expression of these genes between the morphs of the parthenogenetic and the sexual phases of Acyrthosiphon pisum.

Conclusions

The discovery of these gene duplications in the miRNA machinery of aphids opens new perspectives of research about the regulation of gene expression in these insects. Accelerated evolution, positive selection and differential expression affecting some of the copies of these genes suggests the possibility of a neofunctionalization of these duplicates, which might play a role in the display of the striking phenotypic plasticity of aphids.

【 授权许可】

   
2012 Ortiz-Rivas et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 5.

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Figure 5.

【 参考文献 】

• [1]Hoekstra HE, Coyne JA: The locus of evolution: evo devo and the genetics of adaptation. Evolution 2007, 61(5):995-1016.
• [2]Lynch M, Conery JS: The evolutionary fate and consequences of duplicate genes. Science 2000, 290(5494):1151-1155.
• [3]Zhen Y, Aardema ML, Medina EM, Schumer M, Andolfatto P: Parallel molecular evolution in an herbivore community. Science 2012, 337(6102):1634-1637.
• [4]Ghildiyal M, Zamore PD: Small silencing RNAs: an expanding universe. Nat Rev Genet 2009, 10(2):94-108.
• [5]Ketting RF: The many faces of RNAi. Dev Cell 2011, 20(2):148-161.
• [6]Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ: Processing of primary microRNAs by the Microprocessor complex. Nature 2004, 432(7014):231-235.
• [7]Hutvagner G, Simard MJ: Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 2008, 9(1):22-32.
• [8]Liu N, Okamura K, Tyler DM, Phillips MD, Chung WJ, Lai EC: The evolution and functional diversification of animal microRNA genes. Cell Res 2008, 18(10):985-996.
• [9]Krol J, Loedige I, Filipowicz W: The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010, 11(9):597-610.
• [10]Meister G, Tuschl T: Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431(7006):343-349.
• [11]Yigit E, Batista PJ, Bei Y, Pang KM, Chen CC, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ, Mello CC: Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 2006, 127(4):747-757.
• [12]Campbell CL, Black WC, Hess AM, Foy BD: Comparative genomics of small RNA regulatory pathway components in vector mosquitoes. BMC Genomics 2008, 9:425. BioMed Central Full Text
• [13]Schurko AM, Logsdon JM Jr, Eads BD: Meiosis genes in Daphnia pulex and the role of parthenogenesis in genome evolution. BMC Evol Biol 2009, 9:78. BioMed Central Full Text
• [14]Kim VN, Han J, Siomi MC: Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009, 10(2):126-139.
• [15]The International Aphid Genomics Consortium: Genome Sequence of the Pea Aphid Acyrthosiphon pisum. PLoS Biol 2010., 8(2)
• [16]Lu HL, Tanguy S, Rispe C, Gauthier JP, Walsh T, Gordon K, Edwards O, Tagu D, Chang CC, Jaubert-Possamai S: Expansion of genes encoding piRNA-associated argonaute proteins in the pea aphid: diversification of expression profiles in different plastic morphs. PLoS One 2011, 6(12):e28051. Epub 22011 Dec 28055
• [17]Jaubert-Possamai S, Rispe C, Tanguy S, Gordon K, Walsh T, Edwards O, Tagu D: Expansion of the miRNA pathway in the hemipteran insect Acyrthosiphon pisum. Mol Biol Evol 2010, 27(5):979-987.
• [18]Shimodaira H, Hasegawa M: Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 1999, 16(8):1114-1116.
• [19]Strimmer K, Rambaut A: Inferring confidence sets of possibly misspecified gene trees. Proc Biol Sci 2002, 269(1487):137-142.
• [20]Le Trionnaire G, Hardie J, Jaubert-Possamai S, Simon JC, Tagu D: Shifting from clonal to sexual reproduction in aphids: physiological and developmental aspects. Biol Cell 2008, 100(8):441-451.
• [21]Ollivier M, Legeai F, Rispe C: Comparative analysis of the Acyrthosiphon pisum genome and expressed sequence tag-based gene sets from other aphid species. Insect Mol Biol 2010, 19(Suppl 2):33-45.
• [22]Clark MA, Moran NA, Baumann P: Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol Biol Evol 1999, 16(11):1586-1598.
• [23]MacRae IJ, Zhou K, Li F, Repic A, Brooks AN, Cande WZ, Adams PD, Doudna JA: Structural basis for double-stranded RNA processing by Dicer. Science 2006, 311(5758):195-198.
• [24]Remaudière G, Remaudière M: Catalogue des Aphididae du Monde. Paris: INRA; 1997.
• [25]Miller SA, Dykes DD, Polesky HF: A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988, 16(3):1215.
• [26]Staden R, Judge DP, Bonfield JK: Analysing sequences using thes Staden package and EMBOSS. In Introduction to Bioinformatics: A Theoretical and practical approach. Edited by Krawetz SA, Womble DD. Totawa: Human Press Inc; 2003:393-410.
• [27]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al.: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2.
• [28]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:4.
• [29]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25(7):1253-1256.
• [30]Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21(9):2104-2105.
• [31]Drummond A, Strimmer K: PAL: an object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 2001, 17(7):662-663.
• [32]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704.
• [33]Swofford DL: PAUP*. phylogenetic analysis using parsimony (*and other methods). version 4. Sunderland, Massachussets: Sinauer Associates; 2002.
• [34]Felsenstein J: Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:9.
• [35]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574.
• [36]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17(8):754-755.
• [37]Rambaut A, Drummond AJ: Tracer v1.4. 2007. Available from http://beast.bio.ed.ac.uk/Tracer webcite
• [38]Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-1591.
• [39]Yang Z: Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 1998, 15(5):568-573.
• [40]Yang Z, Nielsen R: Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 1998, 46(4):409-418.
• [41]Yang Z, Nielsen R, Goldman N, Pedersen AM: Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000, 155(1):431-449.
• [42]Yang Z, Wong WS, Nielsen R: Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 2005, 22(4):1107-1118.
• [43]Zhang J, Nielsen R, Yang Z: Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 2005, 22(12):2472-2479.
• [44]Sawyer SA: GENECONV: A computer package for the statistical detection of gene conversion. St. Louis: Department of Mathematics, Washington University; 1999. Available at http://www.math.wustl.edu/~sawyer webcite
• [45]Nakabachi A, Shigenobu S, Sakazume N, Shiraki T, Hayashizaki Y, Carninci P, Ishikawa H, Kudo T, Fukatsu T: Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc Natl Acad Sci USA 2005, 102(15):5477-5482.