Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III.

Although the chloroplast genome contains many noncoding regions, relatively few have been exploited for interspecific phylogenetic and intraspecific phylogeographic studies. In our recent evaluation of the phylogenetic utility of 21 noncoding chloroplast regions, we found the most widely used noncoding regions are among the least variable, but the more variable regions have rarely been employed. That study led us to conclude that there may be unexplored regions of the chloroplast genome that have even higher relative levels of variability. To explore the potential variability of previously unexplored regions, we compared three pairs of single-copy chloroplast genome sequences in three disparate angiosperm lineages: Atropa vs. Nicotiana (asterids); Lotus vs. Medicago (rosids); and Saccharum vs. Oryza (monocots). These three separate sequence alignments highlighted 13 mutational hotspots that may be more variable than the best regions of our former study. These 13 regions were then selected for a more detailed analysis. Here we show that nine of these newly explored regions (rpl32-trnL((UAG)), trnQ((UUG))-5'rps16, 3'trnV((UAC))-ndhC, ndhF-rpl32, psbD-trnT((GGU)), psbJ-petA, 3'rps16-5'trnK((UUU)), atpI-atpH, and petL-psbE) offer levels of variation better than the best regions identified in our earlier study and are therefore likely to be the best choices for molecular studies at low taxonomic levels.

[1]  K. Rudi,et al.  Differentiation of important and closely related cereal plant species (Poaceae) in food by hybridization to an oligonucleotide array. , 2005, Journal of agricultural and food chemistry.

[2]  Bengt Oxelman,et al.  Origin and Evolution of a Circumpolar Polyploid Species Complex in Silene (Caryophyllaceae) Inferred from Low Copy Nuclear RNA Polymerase Introns, rDNA, and Chloroplast DNA , 2005 .

[3]  K. H. Wolfe,et al.  Nucleotide Substitution Rates in Legume Chloroplast DNA Depend on the Presence of the Inverted Repeat , 2002, Journal of Molecular Evolution.

[4]  J. Wendel,et al.  The tortoise and the hare: choosing between noncoding plastome and nuclear Adh sequences for phylogeny reconstruction in a recently diverged plant group. , 1998, American journal of botany.

[5]  T. Ban,et al.  Phylogenetic and evolutionary relationships between Elymus humidus and other Elymus species based on sequencing of non-coding regions of cpDNA and AFLP of nuclear DNA , 2004, Theoretical and Applied Genetics.

[6]  P. Schönswetter,et al.  Central Asian origin of and strong genetic differentiation among populations of the rare and disjunct Carex atrofusca (Cyperaceae) in the Alps , 2006 .

[7]  P. Taberlet,et al.  The use of chloroplast DNA to resolve plant phylogenies: noncoding versus rbcL sequences. , 1994, Molecular biology and evolution.

[8]  Reed A. Cartwright,et al.  DNA assembly with gaps (Dawg): simulating sequence evolution , 2005, Bioinform..

[9]  K. Yamane,et al.  Intra- and interspecific phylogenetic relationships among diploid Triticum-Aegilops species (Poaceae) based on base-pair substitutions, indels, and microsatellites in chloroplast noncoding sequences. , 2005, American journal of botany.

[10]  S. Mathews,et al.  Universal primers for the amplification of chloroplast microsatellites in grasses (Poaceae) , 2004 .

[11]  W. Hahn.  A phylogenetic analysis of the Arecoid Line of palms based on plastid DNA sequence data. , 2002, Molecular phylogenetics and evolution.

[12]  D. Janzen,et al.  Use of DNA barcodes to identify flowering plants. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  B. Gaut.  Molecular Clocks and Nucleotide Substitution Rates in Higher Plants , 1998 .

[14]  G. Gutman,et al.  Slipped-strand mispairing: a major mechanism for DNA sequence evolution. , 1987, Molecular biology and evolution.

[15]  K. H. Wolfe,et al.  Nucleotide substitution rates in legume chloroplast DNA depend on the presence of the inverted repeat. , 2002 .

[16]  G. Bucci,et al.  Detection of haplotypic variation and natural hybridization in halepensis‐complex pine species using chloroplast simple sequence repeat (SSR) markers , 1998 .

[17]  Jeffrey D. Palmer,et al.  Use of Chloroplast DNA Rearrangements in Reconstructing Plant Phylogeny , 1992 .

[18]  T. Hayashi,et al.  Genetic characterization of pear varieties revealed by chloroplast DNA sequences , 2003 .

[19]  H. Kudoh,et al.  Origin and diversification of Hibiscus glaber, species endemic to the oceanic Bonin Islands, revealed by chloroplast DNA polymorphism , 2005, Molecular ecology.

[20]  R. Cronn,et al.  Length polymorphism scanning is an efficient approach for revealing chloroplast DNA variation. , 2006, Genome.

[21]  T. Barkman,et al.  Hybrid Origin and Parentage of Dendrochilum acuiferum (Orchidaceae) Inferred in a Phylogenetic Context Using Nuclear and Plastid DNA Sequence Data , 2009 .

[22]  P. Schönswetter,et al.  Rare arctic‐alpine plants of the European Alps have different immigration histories: the snow bed species Minuartia biflora and Ranunculus pygmaeus , 2006, Molecular ecology.

[23]  E. Pahlich,et al.  A rapid DNA isolation procedure for small quantities of fresh leaf tissue , 1980 .

[24]  J. Shaw,et al.  Chloroplast DNA phylogeny and phylogeography of the North American plums (Prunus subgenus Prunus section Prunocerasus, Rosaceae). , 2005, American journal of botany.

[25]  K. O’Donnell.  Ribosomal DNA internal transcribed spacers are highly divergent in the phytopathogenic ascomycete Fusarium sambucinum (Gibberella pulicaris) , 1992, Current Genetics.

[26]  J. Lundberg,et al.  An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants : APG II THE ANGIOSPERM PHYLOGENY GROUP * , 2003 .

[27]  Y. Terajima,et al.  Very close relationship of the chloroplast genomes among Saccharum species , 2005, Theoretical and Applied Genetics.

[28]  M. Clegg,et al.  Molecular evolution of chloroplast DNA sequences. , 1984, Molecular biology and evolution.

[29]  S. Cameron,et al.  Are plant DNA barcodes a search for the Holy Grail? , 2006, Trends in ecology & evolution.

[30]  K. H. Wolfe.  CHAPTER 15 – Protein-Coding Genes in Chloroplast DNA: Compilation of Nucleotide Sequences, Data Base Entries, and Rates of Molecular Evolution , 1991 .

[31]  J. Shaw,et al.  The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. , 2005, American journal of botany.

[32]  Genetic discontinuities among populations of Cleistes (Orchidaceae, Vanilloideae) in North America. , 2004 .

[33]  P. Taberlet,et al.  Universal primers for amplification of three non-coding regions of chloroplast DNA , 1991, Plant Molecular Biology.

[34]  M. Sugiura,et al.  Updated Gene Map of Tobacco Chloroplast DNA , 1998, Plant Molecular Biology Reporter.

[35]  J. Doyle,et al.  A rapid DNA isolation procedure for small amounts of fresh leaf tissue , 1987 .

[36]  Apgii.  An update of the angiosperm phylogeny group classification for the orders and families of flowering plants : APGII , 2003 .

[37]  S. Carnevale,et al.  A new set of mono‐ and dinucleotide chloroplast microsatellites in Fagaceae , 2004 .

[38]  M. Clegg,et al.  A chloroplast DNA mutational hotspot and gene conversion in a noncoding region near rbcL in the grass family (Poaceae) , 1993, Current Genetics.

[39]  B. Menale,et al.  PCR amplification of Michele Tenore's historical specimens and facility to utilize an alternative approach to resolve taxonomic problems , 2004 .

[40]  Wen-Hsiung Li,et al.  Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[41]  J. Palmer,et al.  Chloroplast DNA systematics: a review of methods and data analysis , 1994 .

[42]  J. Tomkins,et al.  Complete chloroplast genome sequences of Solanum bulbocastanum, Solanum lycopersicum and comparative analyses with other Solanaceae genomes , 2006, Theoretical and Applied Genetics.

[43]  Tsan-piao Lin,et al.  Phylogeography of Trochodendron aralioides (Trochodendraceae) in Taiwan and its adjacent areas , 2004 .

[44]  M T Clegg,et al.  Rates and patterns of chloroplast DNA evolution. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[45]  K. Will,et al.  Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification , 2004, Cladistics : the international journal of the Willi Hennig Society.

[46]  Jeremy R. deWaard,et al.  Biological identifications through DNA barcodes , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[47]  R. Eastwood,et al.  From famine to feast? Selecting nuclear DNA sequence loci for plant species-level phylogeny reconstruction , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[48]  M T Clegg,et al.  Evolution of a noncoding region of the chloroplast genome. , 1993, Molecular phylogenetics and evolution.

[49]  S. Ratnasingham,et al.  Biological identifications through DNA barcodes: the case of the Crustacea , 2007 .

[50]  J. Wen,et al.  Phylogeny and biogeography of Altingiaceae: evidence from combined analysis of five non-coding chloroplast regions. , 2006, Molecular phylogenetics and evolution.

[51]  J. Burke,et al.  Chloroplast DNA variation confirms a single origin of domesticated sunflower (Helianthus annuus L.). , 2006, The Journal of heredity.

[52]  R. Jansen,et al.  A comparative analysis of the Lactuca and Helianthus (Asteraceae) plastid genomes: identification of divergent regions and categorization of shared repeats. , 2007, American journal of botany.