View Item 

Show simple item record

Lycophyte plastid genomics: extreme variation in GC, gene and intron content and multiple inversions between a direct and inverted orientation of the rRNA repeat
dc.contributor.authorMower, Jeffrey P.
dc.contributor.authorMa, Peng‐fei
dc.contributor.authorGrewe, Felix
dc.contributor.authorTaylor, Alex
dc.contributor.authorMichael, Todd P.
dc.contributor.authorVanBuren, Robert
dc.contributor.authorQiu, Yin‐long
dc.date.accessioned2019-04-02T18:10:56Z
dc.date.available2020-06-01T14:50:01Zen
dc.date.issued2019-04
dc.identifier.citationMower, Jeffrey P.; Ma, Peng‐fei ; Grewe, Felix; Taylor, Alex; Michael, Todd P.; VanBuren, Robert; Qiu, Yin‐long (2019). "Lycophyte plastid genomics: extreme variation in GC, gene and intron content and multiple inversions between a direct and inverted orientation of the rRNA repeat." New Phytologist 222(2): 1061-1075.
dc.identifier.issn0028-646X
dc.identifier.issn1469-8137
dc.identifier.urihttps://hdl.handle.net/2027.42/148375
dc.publisherAcademic Press
dc.publisherWiley Periodicals, Inc.
dc.subject.otherLycopodiophyta (lycophytes)
dc.subject.otherevolutionary stasis
dc.subject.othergene loss
dc.subject.otherinversion
dc.subject.otherIsoetes (quillworts)
dc.subject.otherLycopodiaceae (clubmosses)
dc.subject.otherplastid genome (plastome)
dc.subject.otherSelaginella (spikemosses)
dc.titleLycophyte plastid genomics: extreme variation in GC, gene and intron content and multiple inversions between a direct and inverted orientation of the rRNA repeat
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelNatural Resources and Environment
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/148375/1/nph15650_am.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/148375/2/nph15650.pdf
dc.identifier.doi10.1111/nph.15650
dc.identifier.sourceNew Phytologist
dc.identifier.citedreferenceSmith DR. 2009. Unparalleled GC content in the plastid DNA of Selaginella. Plant Molecular Biology 71: 627 â 639.
dc.identifier.citedreferenceRaubeson LA, Stein DB. 1995. Insights into fern evolution from mapping chloroplast genomes. American Fern Journal 85: 193 â 204.
dc.identifier.citedreferenceRobison TA, Grusz AL, Wolf PG, Mower JP, Fauskee BD, Sosa K, Schuettpelz E. 2018. Mobile elements shape plastome evolution in ferns. Genome Biology and Evolution 10: 2558 â 2571.
dc.identifier.citedreferenceRuhlman TA, Chang WJ, Chen JJ, Huang YT, Chan MT, Zhang J, Liao DC, Blazier JC, Jin X, Shih MC et al. 2015. NDH expression marks major transitions in plant evolution and reveals coordinate intracellular gene loss. BMC Plant Biology 15: 100.
dc.identifier.citedreferenceSchuettpelz E, Schneider H, Smith AR, Hovenkamp P, Prado J, Rouhan G, Salino A, Sundue M, Almeida TE, Parris B et al. 2016. A communityâ derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54: 563 â 603.
dc.identifier.citedreferenceSigmon BA, Adams RP, Mower JP. 2017. Complete chloroplast genome sequencing of vetiver grass ( Chrysopogon zizanioides ) identifies markers that distinguish the nonâ fertile â Sunshineâ cultivar from other accessions. Industrial Crops and Products 108: 629 â 635.
dc.identifier.citedreferenceSong M, Kuo LY, Huiet L, Pryer KM, Rothfels CJ, Li FW. 2018. A novel chloroplast gene reported for flagellate plants. American Journal of Botany 105: 117 â 121.
dc.identifier.citedreferenceStein DB, Conant DS, Ahearn ME, Jordan ET, Kirch SA, Hasebe M, Iwatsuki K, Tan MK, Thomson JA. 1992. Structural rearrangements of the chloroplast genome provide an important phylogenetic link in ferns. Proceedings of the National Academy of Sciences, USA 89: 1856 â 1860.
dc.identifier.citedreferenceSugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M. 2003. Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Research 31: 5324 â 5331.
dc.identifier.citedreferenceTakenaka M, Zehrmann A, Verbitskiy D, Kugelmann M, Hartel B, Brennicke A. 2012. Multiple organellar RNA editing factor (MORF) family proteins are required for RNA editing in mitochondria and plastids of plants. Proceedings of the National Academy of Sciences, USA 109: 5104 â 5109.
dc.identifier.citedreferenceTesto W, Field A, Barrington D. 2018. Overcoming amongâ lineage rate heterogeneity to infer the divergence times and biogeography of the clubmoss family Lycopodiaceae. Journal of Biogeography 45: 1929 â 1941.
dc.identifier.citedreferenceTillich M, Lehwark P, Pellizzer T, Ulbrichtâ Jones ES, Fischer A, Bock R, Greiner S. 2017. GeSeq â versatile and accurate annotation of organelle genomes. Nucleic Acids Research 45: W6 â W11.
dc.identifier.citedreferenceTsuji S, Ueda K, Nishiyama T, Hasebe M, Yoshikawa S, Konagaya A, Nishiuchi T, Yamaguchi K. 2007. The chloroplast genome from a lycophyte (microphyllophyte), Selaginella uncinata, has a unique inversion, transpositions and many gene losses. Journal of Plant Research 120: 281 â 290.
dc.identifier.citedreferenceVanBuren R, Wai CM, Ou S, Pardo J, Bryant D, Jiang N, Mockler TC, Edger P, Michael TP. 2018. Extreme haplotype variation in the desiccationâ tolerant clubmoss Selaginella lepidophylla. Nature Communications 9: 13.
dc.identifier.citedreferenceVillarreal JC, Forrest LL, Wickett N, Goffinet B. 2013. The plastid genome of the hornwort Nothoceros aenigmaticus (Dendrocerotaceae): phylogenetic signal in inverted repeat expansion, pseudogenization, and intron gain. American Journal of Botany 100: 467 â 477.
dc.identifier.citedreferenceVillarreal JC, Turmel M, Bourgouinâ Couture M, Laroche J, Salazar Allen N, Li FW, Cheng S, Renzaglia K, Lemieux C. 2018. Genomeâ wide organellar analyses from the hornwort Leiosporoceros dussii show low frequency of RNA editing. PLoS ONE 13: e0200491.
dc.identifier.citedreferenceVogel J, Hubschmann T, Borner T, Hess WR. 1997. Splicing and intronâ internal RNA editing of trnK â matK transcripts in barley plastids: support for MatK as an essential splice factor. Journal of Molecular Biology 270: 179 â 187.
dc.identifier.citedreferenceWakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M. 1994. Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proceedings of the National Academy of Sciences, USA 91: 9794 â 9798.
dc.identifier.citedreferenceWeng ML, Blazier JC, Govindu M, Jansen RK. 2014. Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. Molecular Biology and Evolution 31: 645 â 659.
dc.identifier.citedreferenceWicke S, Schneeweiss GM, dePamphilis CW, Muller KF, Quandt D. 2011. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Molecular Biology 76: 273 â 297.
dc.identifier.citedreferenceWickett NJ, Zhang Y, Hansen SK, Roper JM, Kuehl JV, Plock SA, Wolf PG, DePamphilis CW, Boore JL, Goffinet B. 2008. Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Molecular Biology and Evolution 25: 393 â 401.
dc.identifier.citedreferenceWikstrom N, Pryer KM. 2005. Incongruence between primary sequence data and the distribution of a mitochondrial atp1 group II intron among ferns and horsetails. Molecular Phylogenetics and Evolution 36: 484 â 493.
dc.identifier.citedreferenceWolf PG, Karol KG, Mandoli DF, Kuehl J, Arumuganathan K, Ellis MW, Mishler BD, Kelch DG, Olmstead RG, Boore JL. 2005. The first complete chloroplast genome sequence of a lycophyte, Huperzia lucidula (Lycopodiaceae). Gene 350: 117 â 128.
dc.identifier.citedreferenceWolfe KH, Li WH, Sharp PM. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences, USA 84: 9054 â 9058.
dc.identifier.citedreferenceXu Z, Xin T, Bartels D, Li Y, Gu W, Yao H, Liu S, Yu H, Pu X, Zhou J et al. 2018. Genome analysis of the ancient tracheophyte Selaginella tamariscina reveals evolutionary features relevant to the acquisition of desiccation tolerance. Molecular Plant 11: 983 â 994.
dc.identifier.citedreferenceZerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Research 18: 821 â 829.
dc.identifier.citedreferenceZhou XM, Rothfels CJ, Zhang L, He ZR, Le Pechon T, He H, Lu NT, Knapp R, Lorence D, He XJ et al. 2016. A largeâ scale phylogeny of the lycophyte genus Selaginella (Selaginellaceae: Lycopodiopsida) based on plastid and nuclear loci. Cladistics 32: 360 â 389.
dc.identifier.citedreferenceZhu 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 Phytologist 209: 1747 â 1756.
dc.identifier.citedreferenceZoschke R, Nakamura M, Liere K, Sugiura M, Borner T, Schmitzâ Linneweber C. 2010. An organellar maturase associates with multiple group II introns. Proceedings of the National Academy of Sciences, USA 107: 3245 â 3250.
dc.identifier.citedreferenceAbascal F, Zardoya R, Telford MJ. 2010. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Research 38: W7 â W13.
dc.identifier.citedreferenceBankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD et al. 2012. SPAdes: a new genome assembly algorithm and its applications to singleâ cell sequencing. Journal of Computational Biology 19: 455 â 477.
dc.identifier.citedreferenceBell NE, Boore JL, Mishler BD, Hyvönen J. 2014. Organellar genomes of the fourâ toothed moss, Tetraphis pellucida. BMC Genomics 15: 383.
dc.identifier.citedreferenceBendich AJ. 2004. Circular chloroplast chromosomes: the grand illusion. Plant Cell 16: 1661 â 1666.
dc.identifier.citedreferenceBirky CW, Walsh JB. 1992. Biased gene conversion, copy number, and apparent mutationâ rate differences within chloroplast and bacterial genomes. Genetics 130: 677 â 683.
dc.identifier.citedreferenceBlazier CJ, Guisinger MM, Jansen RK. 2011. Recent loss of plastidâ encoded ndh genes within Erodium (Geraniaceae). Plant Molecular Biology 76: 263 â 272.
dc.identifier.citedreferenceBohnert HJ, Loffelhardt W. 1982. Cyanelle DNA from Cyanophora paradoxa exists in 2 forms due to intramolecular recombination. FEBS Letters 150: 403 â 406.
dc.identifier.citedreferenceCai Z, Guisinger M, Kim HG, 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. Journal of Molecular Evolution 67: 696 â 704.
dc.identifier.citedreferenceCastresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540 â 552.
dc.identifier.citedreferenceChaw Sâ M, Wu Câ S, Sudianto E. 2018. Evolution of gymnosperm plastid genomes. In: Chaw Sâ M, Jansen RK, eds. Advances in botanical research. Cambridge, MA, USA: Academic Press, 195 â 222.
dc.identifier.citedreferenceChumley TW, Palmer JD, Mower JP, Fourcade HM, Calie PJ, Boore JL, Jansen RK. 2006. The complete chloroplast genome sequence of Pelargonium à hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Molecular Biology and Evolution 23: 2175 â 2190.
dc.identifier.citedreferenceCosner ME, Jansen RK, Palmer JD, Downie SR. 1997. The highly rearranged chloroplast genome of Trachelium caeruleum (Campanulaceae): multiple inversions, inverted repeat expansion and contraction, transposition, insertions/deletions, and several repeat families. Current Genetics 31: 419 â 429.
dc.identifier.citedreferenceCosner ME, Raubeson LA, Jansen RK. 2004. Chloroplast DNA rearrangements in Campanulaceae: phylogenetic utility of highly rearranged genomes. BMC Evolutionary Biology 4: 27.
dc.identifier.citedreferenceCuenca A, Ross TG, Graham SW, Barrett CF, Davis JI, Seberg O, Petersen G. 2016. Localized retroprocessing as a model of intron loss in the plant mitochondrial genome. Genome Biology and Evolution 8: 2176 â 2189.
dc.identifier.citedreferenceDelannoy E, Stanley WA, Bond CS, Small ID. 2007. Pentatricopeptide repeat (PPR) proteins as sequenceâ specificity factors in postâ transcriptional processes in organelles. Biochemical Society Transactions 35: 1643 â 1647.
dc.identifier.citedreferenceDoyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11 â 15.
dc.identifier.citedreferenceEdgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792 â 1797.
dc.identifier.citedreferenceField AR, Testo W, Bostock PD, Holtum JAM, Waycott M. 2016. Molecular phylogenetics and the morphology of the Lycopodiaceae subfamily Huperzioideae supports three genera: Huperzia, Phlegmariurus and Phylloglossum. Molecular Phylogenetics and Evolution 94: 635 â 657.
dc.identifier.citedreferenceGao L, Zhou Y, Wang ZW, Su YJ, Wang T. 2011. Evolution of the rpoB â psbZ region in fern plastid genomes: notable structural rearrangements and highly variable intergenic spacers. BMC Plant Biology 11: 64.
dc.identifier.citedreferenceGoffinet B, Wickett NJ, Werner O, Ros RM, Shaw AJ, Cox CJ. 2007. Distribution and phylogenetic significance of the 71â kb inversion in the plastid genome in Funariidae (Bryophyta). Annals of Botany 99: 747 â 753.
dc.identifier.citedreferenceGrewe F, Guo W, Gubbels EA, Hansen AK, Mower JP. 2013. Complete plastid genomes from Ophioglossum californicum, Psilotum nudum, and Equisetum hyemale reveal an ancestral land plant genome structure and resolve the position of Equisetales among monilophytes. BMC Evolutionary Biology 13: 8.
dc.identifier.citedreferenceGrewe F, Viehoever P, Weisshaar B, Knoop V. 2009. A trans â splicing group I intron and tRNAâ hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Research 37: 5093 â 5104.
dc.identifier.citedreferenceGrewe F, Zhu A, Mower JP. 2016. Loss of a trans â splicing nad1 intron from Geraniaceae and transfer of the maturase gene matR to the nucleus in Pelargonium. Genome Biology and Evolution 8: 3193 â 3201.
dc.identifier.citedreferenceGrosche C, Funk HT, Maier UG, Zauner S. 2012. The chloroplast genome of Pellia endiviifolia: gene content, RNAâ editing pattern, and the origin of chloroplast editing. Genome Biology and Evolution 4: 1349 â 1357.
dc.identifier.citedreferenceGualberto JM, Newton KJ. 2017. Plant mitochondrial genomes: dynamics and mechanisms of mutation. Annual Review of Plant Biology 68: 225 â 252.
dc.identifier.citedreferenceGuindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximumâ likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307 â 321.
dc.identifier.citedreferenceGuo W, Grewe F, Coboâ Clark A, Fan W, Duan Z, Adams RP, Schwarzbach AE, Mower JP. 2014. Predominant and substoichiometric isomers of the plastid genome coexist within Juniperus plants and have shifted multiple times during cupressophyte evolution. Genome Biology and Evolution 6: 580 â 590.
dc.identifier.citedreferenceGuo W, Grewe F, Fan W, Young GJ, Knoop V, Palmer JD, Mower JP. 2016. Ginkgo and Welwitschia mitogenomes reveal extreme contrasts in gymnosperm mitochondrial evolution. Molecular Biology and Evolution 33: 1448 â 1460.
dc.identifier.citedreferenceGuo W, Mower JP. 2013. Evolution of plant mitochondrial intronâ encoded maturases: frequent lineageâ specific loss and recurrent intracellular transfer to the nucleus. Journal of Molecular Evolution 77: 43 â 54.
dc.identifier.citedreferenceGuo ZY, Zhang HR, Shrestha N, Zhang XC. 2016. Complete chloroplast genome of a valuable medicinal plant, Huperzia serrata (Lycopodiaceae), and comparison with its congener. Applications in Plant Sciences 4: 1600071.
dc.identifier.citedreferenceHaberle RC, Fourcade HM, Boore JL, Jansen RK. 2008. Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. Journal of Molecular Evolution 66: 350 â 361.
dc.identifier.citedreferenceHasebe M, Iwatsuki K. 1992. Gene localization on the chloroplast DNA of the maiden hair fern; Adiantum capillusâ veneris. Botanical Magazine Tokyo 105: 413 â 419.
dc.identifier.citedreferenceHecht J, Grewe F, Knoop V. 2011. Extreme RNA editing in coding islands and abundant microsatellites in repeat sequences of Selaginella moellendorffii mitochondria: the root of frequent plant mtDNA recombination in early tracheophytes. Genome Biology and Evolution 3: 344 â 358.
dc.identifier.citedreferenceJansen RK, Ruhlman TA. 2012. Plastid genomes of seed plants. In: Bock R, Knoop V, eds. Genomics of chloroplasts and mitochondria. Dordrecht, the Netherlands: Springer Netherlands, 103 â 126.
dc.identifier.citedreferenceKarol KG, Arumuganathan K, Boore JL, Duffy AM, Everett KD, Hall JD, Hansen SK, Kuehl JV, Mandoli DF, Mishler BD et al. 2010. Complete plastome sequences of Equisetum arvense and Isoetes flaccida: implications for phylogeny and plastid genome evolution of early land plant lineages. BMC Evolutionary Biology 10: 321.
dc.identifier.citedreferenceKearse M, Moir R, Wilson A, Stonesâ Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647 â 1649.
dc.identifier.citedreferenceKnox EB. 2014. The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms. Proceedings of the National Academy of Sciences, USA 111: 11097 â 11102.
dc.identifier.citedreferenceKorall P, Kenrick P. 2004. The phylogenetic history of Selaginellaceae based on DNA sequences from the plastid and nucleus: extreme substitution rates and rate heterogeneity. Molecular Phylogenetics and Evolution 31: 852 â 864.
dc.identifier.citedreferenceLarsén E, Rydin C. 2016. Disentangling the phylogeny of Isoetes (Isoetales), using nuclear and plastid data. International Journal of Plant Sciences 177: 157 â 174.
dc.identifier.citedreferenceLee J, Cho CH, Park SI, Choi JW, Song HS, West JA, Bhattacharya D, Yoon HS. 2016. Parallel evolution of highly conserved plastid genome architecture in red seaweeds and seed plants. BMC Biology 14: 75.
dc.identifier.citedreferenceLee HL, Jansen RK, Chumley TW, Kim KJ. 2007. Gene relocations within chloroplast genomes of Jasminum and Menodora (Oleaceae) are due to multiple, overlapping inversions. Molecular Biology and Evolution 24: 1161 â 1180.
dc.identifier.citedreferenceLi FW, Kuo LY, Pryer KM, Rothfels CJ. 2016. Genes translocated into the plastid inverted repeat show decelerated substitution rates and elevated GC content. Genome Biology and Evolution 8: 2452 â 2458.
dc.identifier.citedreferenceLiu Y, Wang B, Cui P, Li L, Xue JY, Yu J, Qiu YL. 2012. The mitochondrial genome of the lycophyte Huperzia squarrosa: the most archaic form in vascular plants. PLoS ONE 7: e35168.
dc.identifier.citedreferenceLohse M, Drechsel O, Bock R. 2007. OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of highâ quality custom graphical maps of plastid and mitochondrial genomes. Current Genetics 52: 267 â 274.
dc.identifier.citedreferenceMagallon S, Hilu KW, Quandt D. 2013. Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. American Journal of Botany 100: 556 â 573.
dc.identifier.citedreferenceMalek O, Lättig K, Hiesel R, Brennicke A, Knoop V. 1996. RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO Journal 15: 1403 â 1411.
dc.identifier.citedreferenceMilligan BG, Hampton JN, Palmer JD. 1989. Dispersed repeats and structural reorganization in subclover chloroplast DNA. Molecular Biology and Evolution 6: 355 â 368.
dc.identifier.citedreferenceMorris JL, Puttick MN, Clark JW, Edwards D, Kenrick P, Pressel S, Wellman CH, Yang Z, Schneider H, Donoghue PCJ. 2018. The timescale of early land plant evolution. Proceedings of the National Academy of Sciences, USA 115: E2274 â E2283.
dc.identifier.citedreferenceMower JP, Vickrey TL. 2018. Structural diversity among plastid genomes of land plants. In: Chaw Sâ M, Jansen RK, eds. Advances in botanical research, vol. 85. Cambridge, MA, USA: Academic Press, 263 â 292.
dc.identifier.citedreferenceOldenburg DJ, Bendich AJ. 2016. The linear plastid chromosomes of maize: terminal sequences, structures, and implications for DNA replication. Current Genetics 62: 431 â 442.
dc.identifier.citedreferenceOldenkott B, Yamaguchi K, Tsujiâ Tsukinoki S, Knie N, Knoop V. 2014. Chloroplast RNA editing going extreme: more than 3400 events of Câ toâ U editing in the chloroplast transcriptome of the lycophyte Selaginella uncinata. RNA 20: 1499 â 1506.
dc.identifier.citedreferencePalmer JD. 1983. Chloroplast DNA exists in two orientations. Nature 301: 92 â 93.
dc.identifier.citedreferencePerry AS, Wolfe KH. 2002. Nucleotide substitution rates in legume chloroplast DNA depend on the presence of the inverted repeat. Journal of Molecular Evolution 55: 501 â 508.
dc.identifier.citedreferencePond SLK, Frost SD, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676 â 679.
dc.identifier.citedreferencePosada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817 â 818.
dc.identifier.citedreferenceRaubeson LA, Jansen RK. 1992. Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255: 1697 â 1699.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
nph15650_am.pdf
Size:
254.1KB
Format:
PDF
View/Open
Name:
nph15650.pdf
Size:
767.3KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.