Skip to main content
SpringerLink
Log in

Plastome-Wide Nucleotide Substitution Rates Reveal Accelerated Rates in Papilionoideae and Correlations with Genome Features Across Legume Subfamilies

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

This study represents the most comprehensive plastome-wide comparison of nucleotide substitution rates across the three subfamilies of Fabaceae: Caesalpinioideae, Mimosoideae, and Papilionoideae. Caesalpinioid and mimosoid legumes have large, unrearranged plastomes compared with papilionoids, which exhibit varying levels of rearrangement including the loss of the inverted repeat (IR) in the IR-lacking clade (IRLC). Using 71 genes common to 39 legume taxa representing all the three subfamilies, we show that papilionoids consistently have higher nucleotide substitution rates than caesalpinioids and mimosoids, and rates in the IRLC papilionoids are generally higher than those in the IR-containing papilionoids. Unsurprisingly, this pattern was significantly correlated with growth habit as most papilionoids are herbaceous, whereas caesalpinioids and mimosoids are largely woody. Both nonsynonymous (dN) and synonymous (dS) substitution rates were also correlated with several biological features including plastome size and plastomic rearrangements such as the number of inversions and indels. In agreement with previous reports, we found that genes in the IR exhibit between three and fourfold reductions in the substitution rates relative to genes within the large single-copy or small single-copy regions. Furthermore, former IR genes in IR-lacking taxa exhibit accelerated rates compared with genes contained in the IR.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Barnard-Kubow K, Sloan DB, Galloway LF (2014) Correlation between sequence divergence and polymorphism reveals similar evolutionary mechanisms acting across multiple timescales in a rapidly evolving plastid genome. BMC Evol Biol 14:268. doi:10.1186/s12862-014-0268-y

    Article  PubMed  Google Scholar 

  • Barraclough TG, Harvey PH, Nee S (1996) Rate of rbcL gene sequence evolution and species diversification in flowering plants (angiosperms). Proc R Soc Lond B 263:589–591

    Article  Google Scholar 

  • Bernt M, Merkle D, Ramsch K, Fritzsch G, Perseke M, Bernhard D, Schlegel M, Stadler PF, Middendorf M (2007) CREx: inferring genomic rearrangements based on common intervals. Bioinformatics 23:2957–2958

    Article  CAS  PubMed  Google Scholar 

  • Birky CW, Walsh JB (1992) Biased gene conversion, copy number, and apparent mutation rate differences within chloroplast and bacterial genomes. Genetics 130:677–683

    PubMed  Google Scholar 

  • Blazier CJ, Guisinger MM, Jansen RK (2011) Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae). Plant Mol Biol 76:263–272. doi:10.1007/s11103-011-9753-5

    Article  CAS  Google Scholar 

  • Blazier JC, Jansen RK, Mower JP, Govindu M, Zhang J, Weng M-L, Ruhlman TA (2016a) Variable presence of the inverted repeat and plastome stability in Erodium. Ann Bot 117:1209–1220. doi:10.1093/aob/mcw065

    Article  PubMed  Google Scholar 

  • Blazier JC, Ruhlman TA, Weng M-L, Rehman SK, Sabir JSM, Jansen RK (2016b) Divergence of RNA polymerase α subunits in angiosperm plastid genomes is mediated by genomic rearrangement. Sci Rep 6:24595. doi:10.1038/srep24595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bobiwash K, Schultz S, Schoen D (2013) Somatic deleterious mutation rate in a woody plant: estimation from phenotypic data. Heredity 111:338–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bousquet J, Strauss S, Doerksen A, Price R (1992) Extensive variation in evolutionary rate of rbcL gene sequences among seed plants. Proc Natl Acad Sci USA 89:7844–7848. doi:10.1073/pnas.89.16.7844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Britten RJ (1986) Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393–1398

    Article  CAS  PubMed  Google Scholar 

  • Bromham L, Hua X, Lanfear R, Cowman PF (2015) Exploring the relationships between mutation rates, life history, genome size, environment, and species richness in flowering plants. Am Nat 185:507–524

    Article  PubMed  Google Scholar 

  • Buschiazzo E, Ritland C, Bohlmann J, Ritland K (2012) Slow but not low: genomic comparisons reveal slower evolutionary rate and higher dN/dS in conifers compared to angiosperms. BMC Evol Biol 12:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai Z, Guisinger M, Kim H-G, Ruck E, Blazier JC, McMurtry V, Kuehl JV, Boore J, Jansen RK (2008) Extensive reorganization of the plastid genome of Trifolium subterraneum (Fabaceae) is associated with numerous repeated sequences and novel DNA insertions. J Mol Evol 67:696–704

    Article  CAS  PubMed  Google Scholar 

  • Cardoso D, de Queiroz LP, Pennington RT, de Lima HC, Fonty E, Wojciechowski MF, Lavin M (2012) Revisiting the phylogeny of papilionoid legumes: new insights from comprehensively sampled early-branching lineages. Am J Bot 99:1991–2013

    Article  PubMed  Google Scholar 

  • Cardoso D, Pennington RT, de Queiroz LP, Boatwright JS, Van Wyk B-E, Wojciechowski MF, Lavin M (2013) Reconstructing the deep-branching relationships of the papilionoid legumes. S Afr J Bot 89:58–75

    Article  CAS  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Chumley TW, Palmer JD, Mower JP, Fourcade HM, Calie PJ, Boore JL, Jansen RK (2006) The complete chloroplast genome sequence of Pelargonium × hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol Biol Evol 23:2175–2190

    Article  CAS  PubMed  Google Scholar 

  • Cosner ME, Raubeson LA, Jansen RK (2004) Chloroplast DNA rearrangements in Campanulaceae: phylogenetic utility of highly rearranged genomes. BMC Evol Biol 4:27. doi:10.1186/1471-2148-4-27

    Article  PubMed  PubMed Central  Google Scholar 

  • Doebley J, Durbin M, Golenberg EM, Clegg MT, Ma DP (1990) Evolutionary analysis of the large subunit of carboxylase (rbcL) nucleotide sequence among the grasses (Gramineae). Evolution 44:1097–1108

    Article  CAS  Google Scholar 

  • Downie SR, Palmer JD (1992) Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, New York, pp 14–35

    Chapter  Google Scholar 

  • Dugas DV, Hernandex D, Koenen E, Schwarz E, Straub S, Hughes CE, Jansen RK, Nageswara-Rao M, Staats M, Trujillo J, Hajrah NH, Alharbi NS, Al-Malki AL, Sabir JSM, Bailey CD (2015) Mimosoid legume plastome evolution: IR expansion, tandem repeat expansions, and accelerated rate of evolution in clpP. Sci Rep 5:16958. doi:10.1038/srep16958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eyre-Walker A, Gaut B (1997) Correlated rates of synonymous site evolution across plant genomes. Mol Biol Evol 14:455–460. doi:10.1093/oxfordjournals.molbev.a025781

    Article  CAS  PubMed  Google Scholar 

  • Fajardo D, Senalik D, Ames M, Zhu H, Steffan SA, Harbut R, Polashock J, Vorsa N, Gillespie E, Kron K, Zalapa JE (2013) Complete plastid genome sequence of Vaccinium macrocarpon: structure, gene content, and rearrangements revealed by next generation sequencing. Tree Genet Genomes 9:489–498

    Article  Google Scholar 

  • Gaut B, Muse S, Clark W, Clegg M (1992) Relative rates of nucleotide substitution at the rbcL locus of monocotyledonous plants. J Mol Evol 35:292–303. doi:10.1007/BF00161167

    Article  CAS  PubMed  Google Scholar 

  • Gaut B, Morton B, McCaig B, Clegg M (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93:10274–10279. doi:10.1073/pnas.93.19.10274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grewe F, Gubbels EA, Mower JP (2015) The mitochondrial genome evolution of the geranium family: elevated substitution rates decrease genomic complexity. Plant and animal genome XXIII San Diego, CA, USA. https://pag.confex.com/pag/xxiii/webprogram/Paper14712.html. Accessed 25 March 2016

  • Guisinger MM, Kuehl JV, Boore JL, Jansen RK (2008) Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc Natl Acad Sci USA 105:18424–18429. doi:10.1073/pnas.0806759105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guisinger MM, Chumley TW, Kuehl JV, Boore JL, Jansen RK (2010) Implications of the plastid genome sequence of Typha (Typhaceae, Poales) for understanding genome evolution in Poaceae. J Mol Evol 70:149–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guisinger MM, Kuehl JV, Boore JL, Jansen RK (2011) Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage. Mol Biol Evol 28:583–600. doi:10.1093/molbev/msq22

    Article  CAS  PubMed  Google Scholar 

  • Haberle RC, Fourcade HM, Boore JL, Jansen RK (2008) Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. J Mol Evol 66:350–361

    Article  CAS  PubMed  Google Scholar 

  • Hirao T, Watanabe A, Kurita M, Kondo T, Takata K (2008) Complete nucleotide sequence of the Cryptomeria japonica D. Don. chloroplast genome and comparative chloroplast genomics: diversified genomic structure of coniferous species. BMC Plant Biol 8:70. doi:10.1186/1471-2229-8-70

    Article  PubMed  PubMed Central  Google Scholar 

  • Jansen RK, Ruhlman TA (2012) Plastid genomes of seed plants. In: Bock R, Knoop V (eds) Genomics of chloroplasts and mitochondria. Advances in photosynthesis and respiration, vol 35. Springer, Dordrecht, pp 103–126

    Chapter  Google Scholar 

  • Jansen RK, Cai Z, Raubeson LA, Daniell H, dePamphilis CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee S-B, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 104:19369–19374. doi:10.1073/pnas.0709121104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kay K, Whittall J, Hodges S (2006) A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol Biol 6:36. doi:10.1186/1471-2148-6-36

    Article  PubMed  PubMed Central  Google Scholar 

  • Kimura M (1984) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Knox EB (2014) The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms. Proc Natl Acad Sci USA 111:11097–11102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kode V, Mudd EA, Iamtham S, Day A (2005) The tobacco plastid accD gene is essential and is required for leaf development. Plant J 44:237–244. doi:10.1111/j.1365-313X.2005.02533

    Article  CAS  PubMed  Google Scholar 

  • Koller B, Delius H (1980) Vicia faba chloroplast DNA has only one set of ribosomal RNA genes as shown by partial denaturation mapping and R-loop analysis. Mol Gen Genet 178:261–269. doi:10.1007/BF00270471

    Article  CAS  Google Scholar 

  • Kosakovsky Pond SL, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. In: Nielsen R (ed) Statistical methods in molecular evolution. Springer, New York, pp 125–181

    Chapter  Google Scholar 

  • Laroche J, Li P, Maggia L, Bousquet J (1997) Molecular evolution of angiosperm mitochondrial introns and exons. Proc Natl Acad Sci USA 94:5722–5727. doi:10.1073/pnas.94.11.5722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavin M, Doyle JJ, Palmer JD (1990) Evolutionary significance of the loss of the chloroplast-DNA inverted repeat in the Leguminosae subfamily Papilionoideae. Evolution 44:390–402

    Article  CAS  Google Scholar 

  • Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst Biol 54(4):575–594

    Article  PubMed  Google Scholar 

  • Lee H-L, Jansen RK, Chumley TW, Kim K-J (2007) Gene relocations within chloroplast genomes of Jasminum and Menodora (Oleaceae) are due to multiple overlapping inversions. Mol Biol Evol 24:1161–1180

    Article  CAS  PubMed  Google Scholar 

  • Lewis G, Schrire B, Mackinder B, Lock M (eds.) (2005) Legumes of the world. Royal Botanic Gardens, Kew

  • Li F-W, Kuo L-Y, Pryer KM, Rothfels CJ (2016) Genes translocated into the plastid inverted repeat show decelerated substitution rates and elevated GC content. Genome Biol Evol (epub):1–17. doi:10.1093/gbe/evw167

  • Liston A (1995) Use of the polymerase chain reaction to survey for the loss of the inverted repeat in the legume chloroplast genome. In: Crisp MD, Doyle JJ (eds) Advances in legume systematics: phylogeny, vol 7. Royal Botanic Gardens, Kew, pp 31–40

    Google Scholar 

  • LPWG (2013) Legume phylogeny and classification in the 21st century: progress, prospects and lessons for other species-rich clades. Taxon 62:217–248

    Article  Google Scholar 

  • Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 311:1727–1730

    Article  CAS  PubMed  Google Scholar 

  • MacKay J, Liu W, Whetten R, Sederoff RR, O’Malley DM (1995) Genetic analysis of cinnamyl alcohol dehydrogenase in loblolly pine: single gene inheritance, molecular characterization and evolution. Mol Gen Genet 247:537–545. doi:10.1007/BF00290344

    Article  CAS  PubMed  Google Scholar 

  • Maier RM, Neckermann K, Igloi GL, Kössel H (1995) Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J Mol Biol 251:614–628. doi:10.1006/jmbi.1995.0460

    Article  CAS  PubMed  Google Scholar 

  • Martin A, Palumbi S (1993) Body size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci USA 90:4087–4091. doi:10.1073/pnas.90.9.4087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez-Alberola F, del Campo EM, Lázaro-Gimeno D, Mezquita-Claramonte S, Molins A, Mateu-Andrés I, Pedrola-Monfort J, Casano LM, Barreno E, Vendramin GG (2013) Balanced gene losses, duplications and intensive rearrangements led to an unusual regularly sized genome in Arbutus unedo chloroplasts. PLoS ONE 8:e79685

    Article  PubMed  PubMed Central  Google Scholar 

  • McCoy SR, Kuehl JV, Boore JL, Raubeson LA (2008) The complete plastid genome sequence of Welwitschia mirabilis: an unusually compact plastome with accelerated divergence rates. BMC Evol Biol 8:130. doi:10.1186/1471-2148-8-130

    Article  PubMed  PubMed Central  Google Scholar 

  • Mooers AØ, Harvey PH (1994) Metabolic rate, generation time and the rate of molecular evolution in birds. Mol Phylogenet Evol 3:344–350

    Article  CAS  PubMed  Google Scholar 

  • Müller K, Albach DC (2010) Evolutionary rates in Veronica L. (Plantaginaceae): disentangling the influence of life history and breading system. J Mol Evol 70(1):44–56

    Article  PubMed  Google Scholar 

  • Ohta T (1993) An examination of the generation time effect on molecular evolution. Proc Natl Acad Sci USA 90:10676–10680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer JD, Thompson WF (1981) Rearrangements in the chloroplast genomes of mung bean and pea. Proc Natl Acad Sci USA 78:5533–5537. doi:10.1073/pnas.78.9.5533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer J, Osorio B, Aldrich J, Thompson W (1987) Chloroplast DNA evolution among legumes: loss of a large inverted repeat occurred prior to other sequence rearrangements. Curr Genet 11:275–286. doi:10.1007/BF00355401

    Article  CAS  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Peltier J-B, Ripoll DR, Friso G, Rudella A, Cai Y, Ytterberg J, Giacomelli L, Pillardy J, van Wijk KJ (2004) Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted three-dimensional structures, and functional implications. J Biol Chem 279:4768–4781. doi:10.1074/jbc.M309212200

    Article  CAS  PubMed  Google Scholar 

  • Perry AS, Wolfe KH (2002) Nucleotide substitution rates in legume chloroplast DNA depend on the presence of the inverted repeat. J Mol Evol 55:501–508. doi:10.1007/PL00020998

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Ann Rev Ecol Evol Syst 37:187–214. doi:10.2307/annurev.ecolsys.37.091305.30000009

    Article  Google Scholar 

  • Raubeson LA, Peery R, Chumley TW, Dziubek C, Fourcade HM, Boore JL, Jansen RK (2007) Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genom 8:174

    Article  Google Scholar 

  • Ruhlman TA, Jansen RK (2014) The plastid genomes of flowering plants. In: Maliga P (ed) Chloroplast biotechnology: methods and protocols, methods in molecular biology, vol 1132. Springer, New York, pp 3–38

    Chapter  Google Scholar 

  • Sabir J, Schwarz EN, Ellison N, Zhang J, Baeshen NA, Mutwakil M, Jansen RK, Ruhlman TA (2014) Evolutionary and biotechnology implications of plastid genome variation in the inverted-repeat-lacking clade of legumes. Plant Biotechnol J 12:743–754

    Article  CAS  PubMed  Google Scholar 

  • Sanderson MJ, Copetti D, Búrquez A, Bustamante E, Charboneau JL, Eguiarge LE, Kumar S, Lee HO, Lee J, McMahon M, Steele K, Wing R, Yang TJ, Zwickl Wojciechowski MF (2015) Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): loss of the ndh gene suite and inverted repeat. Am J Bot 102:1115–1127

    Article  CAS  PubMed  Google Scholar 

  • Schwarz EN, Ruhlman T, Sabir JSM, Hajrah NH, Alharbi NS, Al-Malki AL, Bailey CD, Jansen RK (2015) Plastid genomes reveal parallel inversions and multiple losses of rps16 in papilionoids. J Syst Evol 53:458–468

    Article  Google Scholar 

  • Sloan DB, Alverson AJ, Wu M, Palmer JD, Taylor DR (2012a) Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol Evol 4:294–306. doi:10.1093/gbe/evs006

    Article  PubMed  PubMed Central  Google Scholar 

  • Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR (2012b) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10:e1001241. doi:10.1371/journal.pbio.1001241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SA, Donoghue MJ (2008) Rates of molecular evolution are linked to life history in flowering plants. Science 322:86–89. doi:10.1126/science.1163197

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 75:758–771

    Article  Google Scholar 

  • Sveinsson S, Cronk Q (2014) Evolutionary origin of highly repetitive plastid genomes within the clover genus (Trifolium). BMC Evol Biol 14:228

    Article  PubMed  PubMed Central  Google Scholar 

  • Weber CC, Nabholz B, Romiguier J, Ellegren H (2014) Kr/Kc but not dN/dS correlates positively with body mass in birds, raising implications for inferring lineage-specific selection. Genome Biol 15:542

    Article  PubMed  PubMed Central  Google Scholar 

  • Weng M-L, Blazier CJ, Govindu M, Jansen RK (2014) Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats and nucleotide substitution rates. Mol Biol Evol 31:645–659. doi:10.1093/molbev/mst257

    Article  CAS  PubMed  Google Scholar 

  • Weng M-L, Ruhlman TA, Jansen RK (2016) Plastid–nuclear interaction and accelerated coevolution in plastid ribosomal genes in Geraniaceae. Genome Biol Evol 8:1824–1838

    Article  PubMed  PubMed Central  Google Scholar 

  • Weng M-L, Ruhlman TA, Jansen RK (2017) Expansion of inverted repeat does not decrease substitution rates in Pelargonium plastid genomes. New Phytol 214:842–851

    Article  CAS  PubMed  Google Scholar 

  • Whittle C-A, Johnston M (2003) Broad-scale analysis contradicts the theory that generation time affects molecular evolutionary rates in plants. J Mol Evol 56:223–233. doi:10.1007/s00239-002-2395-0

    Article  CAS  PubMed  Google Scholar 

  • Williams A, Boykin L, Howell K, Nevill PG, Small I (2015) The complete sequence of the Acacia ligulata chloroplast genome reveals a highly divergent clpP1 gene. PLoS ONE 10:e0125768. doi:10.1371/journal.pone.0125768

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson M, Gaut B, Clegg M (1990) Chloroplast DNA evolves slowly in the palm family (Arecaceae). Mol Biol Evol 7:303–314

    CAS  PubMed  Google Scholar 

  • Wojciechowski MF, Lavin M, Sanderson MJ (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot 91:1846–1862

    Article  CAS  PubMed  Google Scholar 

  • Wolfe KH (1988) The site of deletion of the inverted repeat in pea chloroplast DNA contains duplicated gene fragments. Curr Genet 13:97–99

    Article  CAS  PubMed  Google Scholar 

  • Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058. doi:10.1073/pnas.84.24.9054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu C-S, Chaw S-M (2014) Highly rearranged and size-variable chloroplast genomes in conifers II clade (cupressophytes): evolution towards shorter intergenic spacers. Plant Biotechnol J 12:344–353

    Article  CAS  PubMed  Google Scholar 

  • Wu CS, Chaw SM (2015) Evolutionary stasis in cycad plastomes and the first case of plastome GC-biased gene conversion. Gen Biol Evol 7:2000–2009. doi:10.1093/gbe/evv125

    Article  CAS  Google Scholar 

  • Wu C, Li W (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745. doi:10.1073/pnas.82.6.1741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Ruhlman T, Sabir J, Blazier JC, Weng M-L, Park S, Jansen RK (2016) Coevolution between nuclear encoded DNA replication, recombination and repair genes and plastid genome complexity. Genome Biol Evol 8:622–634. doi:10.1093/gbe/evw033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong BJ, Yonezawa T, Zhong Y, Hasegawa M (2009) Episodic evolution and adaptation of chloroplast genomes in ancestral grasses. PLoS ONE 4:e5297

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu A, Guo W, Gupta S, Fan W, Mower JP (2016) Evolutionary dynamics of the plastid inverted repeat: the effects of expansion, contraction, and loss on substitution rates. New Phytol 209:1747–1756. doi:10.1111/nph.13743

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge the financial support from the President of King Abdulaziz University (KAU) Jeddah, Saudi Arabia, Prof. Dr. Abdulrahman O. Alyoubi. The authors also thank the Genome Sequencing and Analysis Facility at the University of Texas at Austin for performing the Illumina sequencing; the Texas Advanced Computing Center at the University of Texas at Austin for access to supercomputers; TEX-LL for serving as a repository for voucher specimens; and four anonymous reviewers for their valuable suggestions on an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, St. Edward’s University, Austin, TX, 78704, USA

    Erika N. Schwarz

  2. Department of Integrative Biology, University of Texas at Austin, Austin, TX, 78712, USA

    Erika N. Schwarz, Tracey A. Ruhlman, Mao-Lun Weng & Robert K. Jansen

  3. Department of Biology and Microbiology, South Dakota State University, Brookings, SD, 57006, USA

    Mao-Lun Weng

  4. King Abdulaziz City for Science and Technology (KACST), Riyadh, 11442, Saudi Arabia

    Mohammad A. Khiyami

  5. Genomics and Biotechnology Section, Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah, 21589, Saudi Arabia

    Jamal S. M. Sabir, Nahid H. Hajarah, Njud S. Alharbi & Robert K. Jansen

  6. Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah, 21589, Saudi Arabia

    Samar O. Rabah

Authors
  1. Erika N. Schwarz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tracey A. Ruhlman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mao-Lun Weng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohammad A. Khiyami
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jamal S. M. Sabir
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nahid H. Hajarah
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Njud S. Alharbi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Samar O. Rabah
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Robert K. Jansen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Erika N. Schwarz.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schwarz, E.N., Ruhlman, T.A., Weng, ML. et al. Plastome-Wide Nucleotide Substitution Rates Reveal Accelerated Rates in Papilionoideae and Correlations with Genome Features Across Legume Subfamilies. J Mol Evol 84, 187–203 (2017). https://doi.org/10.1007/s00239-017-9792-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-017-9792-x

Keywords

Search

Navigation