BMC Evolutionary Biology | |
Parasitic plants have increased rates of molecular evolution across all three genomes | |
Robert Lanfear1  Peter F Cowman1  Lindell Bromham1  | |
[1] Centre for Macroevolution and Macroecology, Research School of Biology, Australian National University, Canberra, A.C.T, 0200, Australia | |
关键词: Molecular rates; Population size; Comparative; Substitution; Mutation; | |
Others : 1087067 DOI : 10.1186/1471-2148-13-126 |
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received in 2013-03-21, accepted in 2013-06-05, 发布年份 2013 | |
【 摘 要 】
Background
Theoretical models and experimental evidence suggest that rates of molecular evolution could be raised in parasitic organisms compared to non-parasitic taxa. Parasitic plants provide an ideal test for these predictions, as there are at least a dozen independent origins of the parasitic lifestyle in angiosperms. Studies of a number of parasitic plant lineages have suggested faster rates of molecular evolution, but the results of some studies have been mixed. Comparative analysis of all parasitic plant lineages, including sequences from all three genomes, is needed to examine the generality of the relationship between rates of molecular evolution and parasitism in plants.
Results
We analysed DNA sequence data from the mitochondrial, nuclear and chloroplast genomes for 12 independent evolutionary origins of parasitism in angiosperms. We demonstrated that parasitic lineages have a faster rate of molecular evolution than their non-parasitic relatives in sequences for all three genomes, for both synonymous and nonsynonymous substitutions.
Conclusions
Our results prove that raised rates of molecular evolution are a general feature of parasitic plants, not confined to a few taxa or specific genes. We discuss possible causes for this relationship, including increased positive selection associated with host-parasite arms races, relaxed selection, reduced population size or repeated bottlenecks, increased mutation rates, and indirect causal links with generation time and body size. We find no evidence that faster rates are due to smaller effective populations sizes or changes in selection pressure. Instead, our results suggest that parasitic plants have a higher mutation rate than their close non-parasitic relatives. This may be due to a direct connection, where some aspect of the parasitic lifestyle drives the evolution of raised mutation rates. Alternatively, this pattern may be driven by an indirect connection between rates and parasitism: for example, parasitic plants tend to be smaller than their non-parasitic relatives, which may result in more cell generations per year, thus a higher rate of mutations arising from DNA copy errors per unit time. Demonstration that adoption of a parasitic lifestyle influences the rate of genomic evolution is relevant to attempts to infer molecular phylogenies of parasitic plants and to estimate their evolutionary divergence times using sequence data.
【 授权许可】
2013 Bromham et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
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20150116022500850.pdf | 351KB | download | |
Figure 1. | 26KB | Image | download |
【 图 表 】
Figure 1.
【 参考文献 】
- [1]Haraguchi Y, Sasaki A: Host-parasite arms-race in mutation modifications - indefinate escalation despite a heavy load? J Theor Biol 1996, 183(2):121-137.
- [2]Pal C, Maciá MD, Oliver A, Schachar I, Buckling A: Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 2007, 450(7172):1079-1081.
- [3]Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, Thomson NR, Quail M, Smith F, Walker D, Libberton B: Antagonistic coevolution accelerates molecular evolution. Nature 2010, 464(7286):275-278.
- [4]Young ND, De Pamphilis CW: Rate variation in parasitic plants: correlated and uncorrelated patterns among plastid genes of different function. BMC Evol Biol 2005, 5:16. BioMed Central Full Text
- [5]Dowton M, Austin AD: Increased genetic diversity in mitochondrial genes is correlated with the evolution of parasitism in the Hymenoptera. J Mol Evol 1995, 41:958-965.
- [6]Duff RJ, Nickrent DL: Characterization of mitochondrial small-subunit riibosomal RNAs from holoparasitic plants. J Mol Evol 1997, 45(6):631.
- [7]Lemaire B, Huysmans S, Smets E, Merckx V: Rate accelerations in nuclear 18S rDNA of mycoheterotrophic and parasitic angiosperms. J Plant Res 2011, 124(5):561-576.
- [8]Jiggins FM, Hurst GDD, Yang Z: Host-symbiont conflicts: positive selection on an outer membrane protein of parasitic but not mutualistic Rickettsiaceae. Mol Biol Evol 2002, 19:1341-1349.
- [9]Kuijt J: The biology of flowering plants, vol. Berkeley: University of California Press; 1969.
- [10]Westwood JH, Yoder JI, Timko MP, De Pamphilis CW: The evolution of parasitism in plants. Trends Plant Sci 2010, 15(4):227-235.
- [11]Nickrent DL, Starr EM: High rates of nucleotide substitution in nuclear small-subunit (18S) rDNA from holoparasitic flowering plants. J Mol Evol 1994, 39(1):62.
- [12]Nickrent DL, Garcia MA: On the brink of holoparasitism: plastome evolution in dwarf mistletoes (Arceuthobium, Viscaceae). J Mol Evol 2009, 68(6):603-615.
- [13]Su H-J, Hu J-M: Rate heterogeneity in six protein-coding genes from the holoparasite Balanophora (Balanophoraceae) and other taxa of Santalales. Ann Bot 2012, 110:1137-1147.
- [14]McNeal JR, Kuehl JV, Boore JL, De Pamphilis CW: Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta. BMC Plant Biol 2007, 7(1):57. BioMed Central Full Text
- [15]Wolfe KH, Katz-Downie DS, Morden CW, Palmer JD: Evolution of the plastid ribosomal RNA operon in a nongreen parasitic plant: accelerated sequence evolution, altered promoter structure, and tRNA pseudogenes. Plant Mol Biol 1992, 18(6):1037-1048.
- [16]Lanfear R, Welch JJ, Bromham L: Watching the clock: Studying variation in rates of molecular evolution. Trends Ecol Evol 2010, 25(9):495-503.
- [17]Barkman TJ, McNeal JR, Lim SH, Coat G, Croom HB, Young ND, De Pamphilis CW: Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evol Biol 2007, 7:248. BioMed Central Full Text
- [18]Nickrent DL: Parasitic plants connection. Southern Illinois: Southern Illinois University; 1997.
- [19]Krause K: From chloroplasts to cryptic plastids: evolution of plastid genomes in parasitic plants. Curr Genet 2008, 54(3):111-121.
- [20]Wickett NJ, Zhang Y, Hansen SK, Roper JM, Kuehl JV, Plock SA, Wolf PG, DePamphilis CW, Boore JL, Goffinet B: Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol 2008, 25(2):393-401.
- [21]Randle CP, Wolfe AD: The evolution and expression of rbcL in holoparasitic sister-genera Harveya and Hyobanche (Orobanchaceae). Am J Bot 2005, 92(9):1575-1585.
- [22]Young ND, DePamphilis CW: Purifying selection detected in the plastid gene matK and flanking ribozyme regions within a group II intron of nonphotosynthetic plants. Mol Biol Evol 2000, 17(12):1933-1941.
- [23]Thorogood CJ, Rumsey FJ, Harris SA, Hiscock SJ: Host-driven divergence in the parasitic plant Orobanche minor Sm. (Orobanchaceae). Mol Ecol 2008, 17(19):4289-4303.
- [24]Van der Kooij T, Krause K, Dörr I, Krupinska K: Molecular, functional and ultrastructural characterisation of plastids from six species of the parasitic flowering plant genus Cuscuta. Planta 2000, 210(5):701-707.
- [25]Funk H, Berg S, Krupinska K, Maier U, Krause K: Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol 2007, 7(1):45. BioMed Central Full Text
- [26]Barbrook AC, Howe CJ, Purton S: Why are plastid genomes retained in non-photosynthetic organisms? Trends Plant Sci 2006, 11(2):101-108.
- [27]Yoder JI, Scholes JD: Host plant resistance to parasitic weeds; recent progress and bottlenecks. Curr Opp Plant Biol 2010, 13(4):478-484.
- [28]Honaas L, Wafula E, Yang Z, Der J, Wickett N, Altman N, Taylor C, Yoder J, Timko M, Westwood J, et al.: Functional genomics of a generalist parasitic plant: Laser microdissection of host-parasite interface reveals host-specific patterns of parasite gene expression. BMC Plant Biol 2013, 13(1):9. BioMed Central Full Text
- [29]Gaut B, Yang L, Takuno S, Eguiarte LE: The patterns and causes of variation in plant nucleotide substitution rates. Annu Rev Ecol Evol Syst 2011, 42:245-266.
- [30]Gu WJ, Wang XF, Zhai CY, Xie XY, Zhou T: Selection on synonymous sites for increased accessibility around miRNA binding sites in plants. Mol Biol Evol 2012, 29(10):3037-3044.
- [31]Qiu S, Bergero R, Zeng K, Charlesworth D: Patterns of codon usage bias in Silene latifolia. Mol Biol Evol 2011, 28(1):771-780.
- [32]Lynch M: The origins of genome architecture. Sunderland, Mass: Sinauer Assoc; 2007.
- [33]Woolfit M: Effective population size and the rate and pattern of nucleotide substitutions. Biol Lett 2009, 5(3):417-420.
- [34]Charlesworth B: Effective population size and patterns of molecular evolution and variation. Nature Rev Genet 2009, 10:195-205.
- [35]Ebert D: Experimental evolution of parasites. Science 1998, 282(5393):1432-1436.
- [36]Woolfit M, Bromham L: Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes. Mol Biol Evol 2003, 20(9):1545-1555.
- [37]Musselman LJ: The biology of Striga, Orobanche, and other root-parasitic weeds. Annu Rev Phytopathol 1980, 18(1):463-489.
- [38]Lahti DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, Coss RG, Donohue K, Foster SA: Relaxed selection in the wild. Trends Ecol Evol 2009, 24(9):487-496.
- [39]Hafner M, Sudman P, Villablanca F, Spradling T, Demastes J, Nadler S: Disparate rates if molecular evolution in cospeciating hosts and parasites. Science 1994, 265:1087-1090.
- [40]Kaltz O, Shykoff JA: Local adaptation in host–parasite systems. Heredity 1998, 81(4):361-370.
- [41]Lanfear R, Ho SYW, Love D, Bromham L: Mutation rate influences diversification rate in birds. Proc natl Acad Sci USA 2010, 107(47):20423-20428.
- [42]Lartillot N: Interaction between Selection and Biased Gene Conversion in Mammalian Protein-Coding Sequence Evolution Revealed by a Phylogenetic Covariance Analysis. Mol Biol Evol 2013, 30(2):356-368.
- [43]DeRose-Wilson L, Gaut B: Transcription-related mutations and GC content drive variation in nucleotide substitution rates across the genomes of Arabidopsis thaliana and Arabidopsis lyrata. BMC Evol Biol 2007, 7(1):66. BioMed Central Full Text
- [44]Taddei F, Radman M, Maynard-Smith J, Toupance B, Gouyon P, Godelle B: Role of mutator alleles in adaptive evolution. Nature 1997, 387(6634):700-702.
- [45]Giraud A, Matic I, Tenaillon O, Clara A, Radman M, Fons M, Taddei F: Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 2001, 291(5513):2606-2608.
- [46]Metzgar D, Wills C: Evidence for the adaptive evolution of mutation rates. Cell 2000, 101(6):581.
- [47]Rainey PB: Evolutionary genetics: the economics of mutation. Curr Biol 1999, 9(10):R371-R373.
- [48]Denamur E, Tenaillon O, Deschamps C, Skurnik D, Ronco E, Gaillard JL, Picard B, Branger C, Matic I: Intermediate mutation frequencies favor evolution of multidrug resistance in Escherichia coli. Genetics 2005, 171(2):825-827.
- [49]Weissman DB, Barton NH: Limits to the rate of adaptive substitution in sexual populations. PLoS Genet 2012, 8(6):e1002740.
- [50]Lynch M: The Lower Bound to the Evolution of Mutation Rates. Genome Biol Evol 2011, 3:1107-1118.
- [51]Bromham L: Why do species vary in their rate of molecular evolution? Biol Lett 2009, 5:401-404.
- [52]Smith SA, Donoghue MJ: Rates of molecular evolution are linked to life history in flowering plants. Science 2008, 322:86-89.
- [53]Lanfear R, Ho SYW, Davies TJ, Moles ATA L, Swenson NG, Warman L, Zanne AE, Allen AP: Taller plants have lower rates of molecular evolution: the rate of mitosis hypothesis. Nature Communications 2013, 4:1879.
- [54]Davies TJ, Savolainen V, Chase MW, Moat J, Barraclough TG: Environmental energy and evolutionary rates in flowering plants. Proc R Soc Lond B 2004, 271:2195-2220.
- [55]Wright SD, Keeling J, Gillman L: The road from Santa Rosalia: a faster tempo of evolution in tropical climates. Proc natl Acad Sci USA 2006, 103:7718-7722.
- [56]Barraclough TG, Savolainen V: Evolutionary rates and species diversity in flowering plants. Evolution 2001, 55:677-683.
- [57]Duchene D, Bromham L: Rates of molecular evolution and diversification in plants: chloroplast substitution rates correlate with species richness in the Proteaceae. BMC Evol Biol 2013, 13:65. BioMed Central Full Text
- [58]Hardy NB, Cook LG: Testing for Ecological Limitation of Diversification: A Case Study Using Parasitic Plants. Am Nat 2012, 180(4):438-449.
- [59]Feild TS, Brodribb TJ: A unique mode of parasitism in the conifer coral tree Parasitaxus ustus (Podocarpaceae). Plant Cell Environ 2005, 28(10):1316-1325.
- [60]Braukmann T, Stefanovicá S: Plastid genome evolution in mycoheterotrophic Ericaceae. Plant Mol Biol 2012, 1:16.
- [61]Leake JR, Cameron DD: Physiological ecology of mycoheterotrophy. New Phytol 2010, 185(3):601-605.
- [62]Merckx V, Freudenstein JV: Evolution of mycoheterotrophy in plants: a phylogenetic perspective. New Phytol 2010, 185(3):605-609.
- [63]Filipowicz N, Renner SS: The worldwide holoparasitic Apodanthaceae confidently placed in the Cucurbitales by nuclear and mitochondrial gene trees. BMC Evol Biol 2010, 10(1):219. BioMed Central Full Text
- [64]Nickrent DL, Der JP, Anderson FE: Discovery of the photosynthetic relatives of the “Maltese mushroom” Cynomorium. BMC Evol Biol 2005, 5(1):38. BioMed Central Full Text
- [65]Nickrent D, Blarer A, Qiu Y-L, Vidal-Russell R, Anderson F: Phylogenetic inference in Rafflesiales: the influence of rate heterogeneity and horizontal gene transfer. BMC Evol Biol 2004, 4:1471-2148.
- [66]Barkman TJ, Lim S-H, Salleh KM, Nais J: Mitochondrial DNA sequences reveal the photosynthetic relatives of Rafflesia, the world‘s largest flower. Proc natl Acad Sci USA 2004, 101:787-792.
- [67]Vr M, Nickrent DL: Molecular phylogenetic relationships of Olacaceae and related Santalales. Syst Bot 2008, 33(1):97-106.
- [68]Olmstead RG, Wolfe AD, Young ND, Elisons WJ, Reeves PA: Disintegration of the Scrophulariaceae. Am J Bot 2001, 88(2):348-361.
- [69]Rohwer JG: Toward a phylogenetic classification of the Lauraceae: evidence from matK sequences. Syst Bot 2000, 25(1):60-71.
- [70]Sheahan M, Chase M: A phylogenetic analysis of Zygophyllaceae R. Br. based on morphological, anatomical and rbcL DNA sequence data. Bot J Linn Soc 1996, 122:279-300.
- [71]Soltis D, Soltis P, Chase M, Mort M, Albach D, Zanis M, Savolainen V, Hahn W, Hoot S, Fay M: Angiosperm phylogeny inferred from 18s rDNA, rbcL, and atpB sequences. Bot J Linn Soc 2000, 133:381-461.
- [72]Stefanovic S, Olmstead RG: Testing the phylogenetic position of a parasitic plant (Cuscuta, Convolvulaceae, Asteridae): Bayesian inference and the parametric bootstrap on data drawn from three genomes. Syst Biol 2004, 53(3):384-399.
- [73]Lanfear R, Bromham L: Estimating phylogenies for species assemblages: a complete phylogeny for the past and present native birds of New Zealand. Mol Phylog Evol 2011, 61:958-963.
- [74]Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, et al.: Geneious. 2011. http://www.geneious.com webcite
- [75]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
- [76]Lanfear R, Calcott B, Ho SYW, Guindon S: PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 2012, 29(6):1695-1701.
- [77]Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22(21):2688-2690.
- [78]Paradis E, Claude J: K. S: APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004, 20:289-290.
- [79]Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591. http://abacus.gene.ucl.ac.uk/software/paml.html webcite
- [80]Goldman N, Yang Z: A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 1994, 11:725-736.