Correlation between sequence divergence and polymorphism reveals similar evolutionary mechanisms acting across multiple timescales in a rapidly evolving plastid genome

BMC Evolutionary Biology

Laura F Galloway¹  Daniel B Sloan²  Karen B Barnard-Kubow¹ 

[1] Department of Biology, University of Virginia, Charlottesville 22904-4328, VA, USA;Department of Biology, Colorado State University, Fort Collins 80523, CO, USA

关键词: Sequence evolution;    Chloroplast;    Intraspecific;    Reproductive isolation;    pN/pS;    dN/dS;    Selection;    Plastid;   

Others  :  1158321
DOI  :  10.1186/s12862-014-0268-y

 received in 2014-07-05, accepted in 2014-12-11,  发布年份 2014

【 摘 要 】

Background

Although the plastid genome is highly conserved across most angiosperms, multiple lineages have increased rates of structural rearrangement and nucleotide substitution. These lineages exhibit an excess of nonsynonymous substitutions (i.e., elevated dN/dS ratios) in similar subsets of plastid genes, suggesting that similar mechanisms may be leading to relaxed and/or positive selection on these genes. However, little is known regarding whether these mechanisms continue to shape sequence diversity at the intraspecific level.

Results

We examined patterns of interspecific divergence and intraspecific polymorphism in the plastid genome of Campanulastrum americanum, and across plastid genes found a significant correlation between dN/dS and pN/pS (i.e., the within-species equivalent of dN/dS). A number of genes including ycf1, ycf2, clpP, and ribosomal protein genes exhibited high dN/dS ratios. McDonald-Kreitman tests detected little evidence for positive selection acting on these genes, likely due to the presence of substantial intraspecific divergence.

Conclusions

These results suggest that mechanisms leading to increased nucleotide substitution rates in the plastid genome are continuing to act at the intraspecific level. Accelerated plastid genome evolution may increase the likelihood of intraspecific cytonuclear genetic incompatibilities, and thereby contribute to the early stages of the speciation process.

【 授权许可】

   
2014 Barnard-Kubow et al.; licensee BioMed Central.

【 图 表 】

Figure 3.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Jansen R, Ruhlman T: Plastid genomes of seed plants. In Genomics of Chloroplasts and Mitochondria. Edited by Bock R, Knoop V. pringer, Netherlands; 2012:103-126.
• [2]Drouin G, Daoud H, Xia J: Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol 2008, 49(3):827-831.
• [3]Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Muller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee SB, Peery R, McNeal JR, Kuehl JV, Boore JL: Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci U S A 2007, 104(49):19369-19374.
• [4]Guisinger MM, Kuehl JV, Boore JL, Jansen RK: Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc Natl Acad Sci U S A 2008, 105(47):18424-18429.
• [5]Khakhlova O, Bock R: Elimination of deleterious mutations in plastid genomes by gene conversion. Plant J 2006, 46(1):85-94.
• [6]Erixon P, Oxelman B: Whole-gene positive selection, elevated synonymous substitution rates, duplication, and indel evolution of the chloroplast clpP1 gene. PLoS ONE 2008, 3(1):e1386.
• [7]Greiner S, Wang X, Herrmann RG, Rauwolf U, Mayer K, Haberer G, Meurer J: The complete nucleotide sequences of the 5 genetically distinct plastid genomes of Oenothera, subsection Oenothera: II. A microevolutionary view using bioinformatics and formal genetic data. Mol Biol Evol 2008, 25(9):2019-2030.
• [8]Sloan DB, Alverson AJ, Wu M, Palmer JD, Taylor DR: Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol Evol 2012, 4(3):294-306.
• [9]Sloan DB, Triant DA, Forrester NJ, Bergner LM, Wu M, Taylor DR: A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae). Mol Phylogenet Evol 2014, 72:82-89.
• [10]Weng ML, Ruhlman TA, Gibby M, Jansen RK: Phylogeny, rate variation, and genome size evolution of Pelargonium (Geraniaceae). Mol Phylogenet Evol 2012, 64(3):654-670.
• [11]Hudson RR, Kreitman M, Aguade M: A test of neutral molecular evolution based on nucleotide data. Genetics 1987, 116(1):153-159.
• [12]McDonald JH, Kreitman M: Adaptive protein evolution at the Adh locus in Drosophila. Nature 1991, 351(6328):652-654.
• [13]Cosner ME, Raubeson LA, Jansen RK: Chloroplast DNA rearrangements in Campanulaceae: phylogenetic utility of highly rearranged genomes.BMC Evol Biol 2004, 4:27
• [14]Knox EB: The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms. Proc Natl Acad Sci U S A 2014, 111(30):11097-11102.
• [15]Galloway LF, Etterson JR: Population differentiation and hybrid success in Campanula americana: geography and genome size. J Evol Biol 2005, 18(1):81-89.
• [16]Galloway LF, Etterson JR, Hamrick JL: Outcrossing rate and inbreeding depression in the herbaceous autotetraploid, Campanula americana. Heredity 2003, 90(4):308-315.
• [17]Corriveau JL, Coleman AW: Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Am J Bot 1988, 75(10):1443-1458.
• [18]Zhang Q, Liu Y, Sodmergen : Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiol 2003, 44(9):941-951.
• [19]Palmer JD: Isolation and structural-analysis of chloroplast DNA. Methods Enzymol 1986, 118:167-186.
• [20]Jansen RK, Raubeson LA, Boore JL, DePamphilis CW, Chumley TW, Haberle RC, Wyman SK, Alverson AJ, Peery R, Herman SJ, Fourcade HM, Kuehl JV, McNeal JR, Leebens-Mack J, Cui L: Methods for obtaining and analyzing whole chloroplast genome sequences. Method Enzymol 2005, 395:348-384.
• [21]Gordon D, Abajian C, Green P: Consed: A graphical tool for sequence finishing. Genome Res 1998, 8(3):195-202.
• [22]Wyman SK, Jansen RK, Boore JL: Automatic annotation of organellar genomes with DOGMA. Bioinformatics 2004, 20(17):3252-3255.
• [23]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
• [24]Barnard-Kubow KB, Sloan DB, Galloway LF (2014) Data from: Correlation between sequence divergence and polymorphism reveals similar evolutionary mechanisms acting across multiple timescales in a rapidly evolving plastid genome. Dryad Digit Repository. 10.5061/dryad.d143r
• [25]Yang ZH: PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-1591.
• [26]Yang ZH: Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 1998, 15(5):568-573.
• [27]Darriba D, Taboada GL, Doallo R, Posada D: jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012, 9(8):772.
• [28]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704.
• [29]Haberle RC, Fourcade HM, Boore JL, Jansen RK: Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. J Mol Evol 2008, 66(4):350-361.
• [30]Rousseau-Gueutin M, Huang X, Higginson E, Ayliffe M, Day A, Timmis JN: Potential functional replacement of the plastidic acetyl-CoA carboxylase subunit (accD) gene by recent transfers to the nucleus in some angiosperm lineages. Plant Physiol 2013, 161(4):1918-1929.
• [31]Millen RS, Olmstead RG, Adams KL, Palmer JD, Lao NT, Heggie L, Kavanagh TA, Hibberd JM, Giray JC, Morden CW, Calie PJ, Jermiin LS, Wolfe KH: Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 2001, 13(3):645-658.
• [32]Zurawski G, Clegg MT: Evolution of higher-plant chloroplast DNA-encoded genes: implications for structure-function and phylogenetic studies. Annu Rev Plant Physiol Plant Mol Biol 1987, 38:391-418.
• [33]Delannoy E, Fujii S, des Francs-Small CC, Brundrett M, Small I: Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol Biol Evol 2011, 28(7):2077-2086.
• [34]Kikuchi S, Bedard J, Hirano M, Hirabayashi Y, Oishi M, Imai M, Takase M, Ide T, Nakai M: Uncovering the protein translocon at the chloroplast inner envelope membrane. Science 2013, 339(6119):571-574.
• [35]Drescher A, Ruf S, Calsa T, Carrer H, Bock R: The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. Plant J 2000, 22(2):97-104.
• [36]Rand DM, Haney RA, Fry AJ: Cytonuclear coevolution: the genomics of cooperation. Trends Ecol Evol 2004, 19(12):645-653.
• [37]Fishman L, Willis JH: A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 2006, 60(7):1372-1381.
• [38]Levin DA: The cytoplasmic factor in plant speciation. Syst Bot 2003, 28(1):5-11.
• [39]Chou JY, Leu JY: Speciation through cytonuclear incompatibility: Insights from yeast and implications for higher eukaryotes. Bioessays 2010, 32(5):401-411.
• [40]Ellison CK, Burton RS: Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 2008, 62(3):631-638.
• [41]Leppala J, Savolainen O: Nuclear-cytoplasmic interactions reduce male fertility in hybrids of Arabidopsis lyrata subspecies. Evolution 2011, 65(10):2959-2972.
• [42]Sambatti JBM, Ortiz-Barrientos D, Baack EJ, Rieseberg LH: Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecol Lett 2008, 11(10):1082-1091.
• [43]Etterson JR, Keller SR, Galloway LF: Epistatic and cytonuclear interactions govern outbreeding depression in the autotetraploid Campanulastrum americanum. Evolution 2007, 61(11):2671-2683.
• [44]Barreto FS, Burton RS: Evidence for compensatory evolution of ribosomal proteins in response to rapid divergence of mitochondrial rRNA. Mol Biol Evol 2013, 30(2):310-314.
• [45]Sloan DB, Triant DA, Wu M, Taylor DR: Cytonuclear interactions and relaxed selection accelerate sequence evolution in organelle ribosomes. Mol Biol Evol 2014, 31(3):673-682.
• [46]Greiner S, Rauwolf U, Meurer J, Herrmann RG: The role of plastids in plant speciation. Mol Ecol 2011, 20(4):671-691.
• [47]Metzlaf M, Pohlheim F, Börner T, Hagemann R: Hybrid variegation in the genus Pelargonium. Curr Genet 1982, 5(3):245-249.
• [48]Weihe A, Apitz J, Pohlheim F, Salinas-Hartwig A, Borner T: Biparental inheritance of plastidial and mitochondrial DNA and hybrid variegation in Pelargonium. Mol Genet Genomics 2009, 282(6):587-593.