期刊论文详细信息
BMC Evolutionary Biology
Contrasted patterns of selective pressure in three recent paralogous gene pairs in the Medicago genus (L.)
Nathalie Chantret3  Audrey Weber3  Isabelle Hochu3  Thomas Bataillon1  Stéphane De Mita2  Joëlle Ronfort3  Joan Ho-Huu3 
[1] Bioinformatics Research Center (BiRC), Aarhus University, Aarhus, Denmark;INRA - Institut National de la Recherche Agronomique, UMR IAM, Nancy, France;INRA - Institut National de la Recherche Agronomique, UMR AGAP, Montpellier, 34060, France
关键词: Paralogs evolution;    Subfunctionalization;    Neofunctionalization;    Medicago;    Duplication;   
Others  :  1140232
DOI  :  10.1186/1471-2148-12-195
 received in 2012-02-17, accepted in 2012-09-20,  发布年份 2012
PDF
【 摘 要 】

Background

Gene duplications are a molecular mechanism potentially mediating generation of functional novelty. However, the probabilities of maintenance and functional divergence of duplicated genes are shaped by selective pressures acting on gene copies immediately after the duplication event. The ratio of non-synonymous to synonymous substitution rates in protein-coding sequences provides a means to investigate selective pressures based on genic sequences. Three molecular signatures can reveal early stages of functional divergence between gene copies: change in the level of purifying selection between paralogous genes, occurrence of positive selection, and transient relaxed purifying selection following gene duplication. We studied three pairs of genes that are known to be involved in an interaction with symbiotic bacteria and were recently duplicated in the history of the Medicago genus (Fabaceae). We sequenced two pairs of polygalacturonase genes (Pg11-Pg3 and Pg11a-Pg11c) and one pair of auxine transporter-like genes (Lax2-Lax4) in 17 species belonging to the Medicago genus, and sought for molecular signatures of differentiation between copies.

Results

Selective histories revealed by these three signatures of molecular differentiation were found to be markedly different between each pair of paralogs. We found sites under positive selection in the Pg11 paralogs while Pg3 has mainly evolved under purifying selection. The most recent paralogs examined Pg11a and Pg11c, are both undergoing positive selection and might be acquiring new functions. Lax2 and Lax4 paralogs are both under strong purifying selection, but still underwent a temporary relaxation of purifying selection immediately after duplication.

Conclusions

This study illustrates the variety of selective pressures undergone by duplicated genes and the effect of age of the duplication. We found that relaxation of selective constraints immediately after duplication might promote adaptive divergence.

【 授权许可】

   
2012 Ho-Huu et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150324153823805.pdf 377KB PDF download
Figure 2. 42KB Image download
Figure 1. 39KB Image download
【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】
  • [1]Ohno S: Evolution by gene duplication. London: George Allen and Unwin; 1970.
  • [2]Lynch M: Genomic expansion by gene duplication. Sunderland, Massachusetts: Sinauer Associates; 2007. [The origins of genome architecture]
  • [3]Lynch M, Conery JS: The evolutionary fate and consequences of duplicate genes. Science 2000, 290:1151-1155.
  • [4]Blanc G, Barakat A, Guyot R, Cooke R, Delseny M: Extensive duplication and reshuffing in the Arabidopsis genome. Plant Cell 2000, 12:1093-1101.
  • [5]Blanc G, Wolfe KH: Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 2004, 16:1679-1691.
  • [6]Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, et al.: Widespread genome duplications throughout the history of flowering plants. Genome Res 2006, 16:738-749.
  • [7]Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, et al.: The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449:463-467.
  • [8]Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, et al.: Genome sequence of the palaeopolyploid soybean. Nature 2010, 463:178-183.
  • [9]Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, et al.: The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313:1596-1604.
  • [10]Wendel JF: Genome evolution in polyploids. Plant Mol Biol 2000, 42:225-249.
  • [11]Innan H, Kondrashov F: The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 2010, 11:97-108.
  • [12]Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J: Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545.
  • [13]Moore RC, Purugganan MD: The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 2005, 8:122-128.
  • [14]Gu Z, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li WH: Role of duplicate genes in genetic robustness against null mutations. Nature 2003, 421:63-66.
  • [15]He X, Zhang J: Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 2005, 169:1157-1164.
  • [16]Nadeau JH, Sankoff D: Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. Genetics 1997, 147:1259-1266.
  • [17]Li WH, Yang J, Gu X: Expression divergence between duplicate genes. Trends Genet 2005, 21:602-607.
  • [18]Adams KL: Evolution of Duplicate Gene Expression in Polyploid and Hybrid Plants. J Hered 2007, 98:136-141.
  • [19]Chain FJ, Ilieva D, Evans BJ: Duplicate gene evolution and expression in the wake of vertebrate allopolyploidization. BMC Evol Biol 2008, 8:43.
  • [20]Chaudhary B, Flagel L, Stupar RM, Udall JA, Verma N, Springer NM, Wendel JF: Reciprocal silencing, transcriptional bias and functional divergence of homeologs in polyploid cotton (gossypium). Genetics 2009, 182:503-517.
  • [21]Des Marais DL, Rausher MD: Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature 2008, 454:762-765.
  • [22]Hittinger CT, Carroll SB: Gene duplication and the adaptive evolution of a classic genetic switch. Nature 2007, 449:677-681.
  • [23]Gayral P, Caminade P, Boursot P, Galtier N: The evolutionary fate of recently duplicated retrogenes in mice. J Evol Biol 2007, 20:617-626.
  • [24]Casneuf T, De Bodt S, Raes J, Maere S, Van de Peer Y: Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana. Genome Biol 2006, 7:R13.
  • [25]Duarte JM, Cui L, Wall PK, Zhang Q, Zhang X, Leebens-Mack J, Ma H, Altman N, de Pamphilis CW: Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 2006, 23:469-478.
  • [26]Rodriguez-Llorente ID, Perez-Hormaeche J, El Mounadi K, Dary M, Caviedes MA, Cosson V, Kondorosi A, Ratet P, Palomares AJ: From pollen tubes to infection threads: recruitment of Medicago floral pectic genes for symbiosis. Plant J 2004, 39:587-598.
  • [27]Sprent JI: Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 2007, 174:11-25.
  • [28]Young ND, Debelle F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H, et al.: The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 2011, 480:520-524.
  • [29]Lavin M, Herendeen PS, Wojciechowski MF: Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol 2005, 54:575-594.
  • [30]Bena G, Jubier MF, Olivieri II, Lejeune B: Ribosomal External and Internal Transcribed Spacers: Combined Use in the Phylogenetic Analysis of Medicago (Leguminosae). J Mol Evol 1998, 46:299-306.
  • [31]Steele KP, Ickert-Bond SM, Zarre S, Wojciechowski MF: Phylogeny and character evolution in Medicago (Leguminosae): Evidence from analyses of plastid trnK/matK and nuclear GA3ox1 sequences. Am J Bot 2010, 97:1142-1155.
  • [32]Maureira-Butler IJ, Pfeil BE, Muangprom A, Osborn TC, Doyle JJ: The reticulate history of Medicago (Fabaceae). Syst Biol 2008, 57:466-482.
  • [33]Bielawski JP, Yang Z: A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. J Mol Evol 2004, 59:121-132.
  • [34]Teshima KM, Innan H: The effect of gene conversion on the divergence between duplicated genes. Genetics 2004, 166:1553-1560.
  • [35]Kim J, Shiu SH, Thoma S, Li WH, Patterson SE: Patterns of expansion and expression divergence in the plant polygalacturonase gene family. Genome Biol 2006, 7:R87.
  • [36]Sun X, Cao Y, Wang S: Point mutations with positive selection were a major force during the evolution of a receptor-kinase resistance gene family of rice. Plant Physiol 2006, 140:998-1008.
  • [37]Jia L, Clegg MT, Jiang T: Excess non-synonymous substitutions suggest that positive selection episodes occurred during the evolution of DNA-binding domains in the Arabidopsis R2R3-MYB gene family. Plant Mol Biol 2003, 52:627-642.
  • [38]Yang Z, Gu S, Wang X, Li W, Tang Z, Xu C: Molecular evolution of the CPP-like gene family in plants: insights from comparative genomics of Arabidopsis and rice. J Mol Evol 2008, 67:266-277.
  • [39]Schnabel EL, Frugoli J: The PIN and LAX families of auxin transport genes in Medicago truncatula. Mol Genet Genomics 2004, 272:420-432.
  • [40]Desbrosses GJ, Stougaard J: Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 2011, 10:348-358.
  • [41]De Mita S, Santoni S, Hochu I, Ronfort J, Bataillon T: Molecular evolution and positive selection of the symbiotic gene NORK in Medicago truncatula. J Mol Evol 2006, 62:234-244.
  • [42]Staden R: The Staden sequence analysis package. Mol Biotechnol 1996, 5:233-241.
  • [43]Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B: Artemis: sequence visualization and annotation. Bioinformatics 2000, 16:944-945.
  • [44]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
  • [45]Goldman N, Yang Z: A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 1994, 11:725-736.
  • [46]Yang Z: Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 1998, 15:568-573.
  • [47]Yang Z, Nielsen R, Goldman N, Pedersen AM: Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000, 155:431-449.
  • [48]Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997, 13:555-556.
  文献评价指标  
  下载次数:2次 浏览次数:4次