Strategies for complete plastid genome sequencing

Plastid sequencing is an essential tool in the study of plant evolution. This high‐copy organelle is one of the most technically accessible regions of the genome, and its sequence conservation makes it a valuable region for comparative genome evolution, phylogenetic analysis and population studies. Here, we discuss recent innovations and approaches for de novo plastid assembly that harness genomic tools. We focus on technical developments including low‐cost sequence library preparation approaches for genome skimming, enrichment via hybrid baits and methylation‐sensitive capture, sequence platforms with higher read outputs and longer read lengths, and automated tools for assembly. These developments allow for a much more streamlined assembly than via conventional short‐range PCR. Although newer methods make complete plastid sequencing possible for any land plant or green alga, there are still challenges for producing finished plastomes particularly from herbarium material or from structurally divergent plastids such as those of parasitic plants.

[1]  Damon P. Little,et al.  Choosing and Using a Plant DNA Barcode , 2011, PloS one.

[2]  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.

[3]  Jason D. Buenrostro,et al.  Finding a (pine) needle in a haystack: chloroplast genome sequence divergence in rare and widespread pines , 2010, Molecular ecology.

[4]  R. Ennos Estimating the relative rates of pollen and seed migration among plant populations , 1994, Heredity.

[5]  Jerrold I. Davis,et al.  Resolving ancient radiations: can complete plastid gene sets elucidate deep relationships among the tropical gingers (Zingiberales)? , 2014, Annals of botany.

[6]  L. Clark,et al.  Evolution of the bamboos (Bambusoideae; Poaceae): a full plastome phylogenomic analysis , 2015, BMC Evolutionary Biology.

[7]  L. Prince Plastid primers for angiosperm phylogenetics and phylogeography , 2015, Applications in plant sciences.

[8]  F. Bakker,et al.  Genomic Treasure Troves: Complete Genome Sequencing of Herbarium and Insect Museum Specimens , 2013, PloS one.

[9]  James Leebens-Mack,et al.  Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns , 2007, Proceedings of the National Academy of Sciences.

[10]  James F. Smith Phylogenetics of seed plants : An analysis of nucleotide sequences from the plastid gene rbcL , 1993 .

[11]  D. Du,et al.  Variation, Evolution, and Correlation Analysis of C+G Content and Genome or Chromosome Size in Different Kingdoms and Phyla , 2014, PloS one.

[12]  B. Miflin,et al.  Isolation of intact plastids from a range of plant tissues. , 1974, Plant physiology.

[13]  Quentin C. B. Cronk,et al.  Plann: A command-line application for annotating plastome sequences1 , 2015, Applications in plant sciences.

[14]  A. Twyford Will Benchtop Sequencers Resolve the Sequencing Trade-off in Plant Genetics? , 2016, Front. Plant Sci..

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

[16]  B. Gravendeel,et al.  The Complete Chloroplast Genome of 17 Individuals of Pest Species Jacobaea vulgaris: SNPs, Microsatellites and Barcoding Markers for Population and Phylogenetic Studies , 2011, DNA research : an international journal for rapid publication of reports on genes and genomes.

[17]  F. Takaiwa,et al.  The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression , 1986, The EMBO journal.

[18]  Mark Fishbein,et al.  Navigating the tip of the genomic iceberg: Next-generation sequencing for plant systematics. , 2012, American journal of botany.

[19]  Pierre Taberlet,et al.  From barcodes to genomes: extending the concept of DNA barcoding , 2016, Molecular ecology.

[20]  R. Henry,et al.  Chloroplast genome sequences from total DNA for plant identification. , 2011, Plant biotechnology journal.

[21]  Ju Gao,et al.  An Improved Chloroplast DNA Extraction Procedure for Whole Plastid Genome Sequencing , 2012, PloS one.

[22]  Robert K Jansen,et al.  Sources of inversion variation in the small single copy (SSC) region of chloroplast genomes. , 2015, American journal of botany.

[23]  M. Metzlaff,et al.  Variations of chloroplast DNAs in the genus Pelargonium and their biparental inheritance , 2004, Theoretical and Applied Genetics.

[24]  J. Palmer,et al.  Chloroplast DNA evolution among legumes: Loss of a large inverted repeat occurred prior to other sequence rearrangements , 2004, Current Genetics.

[25]  M. Lascoux,et al.  Extensive sharing of chloroplast haplotypes among European birches indicates hybridization among Betula pendula, B. pubescens and B. nana , 2004, Molecular ecology.

[26]  W. Powell,et al.  Chloroplast microsatellites: new tools for studies in plant ecology and evolution. , 2001, Trends in ecology & evolution.

[27]  C. dePamphilis,et al.  Disproportional plastome-wide increase of substitution rates and relaxed purifying selection in genes of carnivorous Lentibulariaceae. , 2014, Molecular biology and evolution.

[28]  M. Blaxter,et al.  Blobology: exploring raw genome data for contaminants, symbionts and parasites using taxon-annotated GC-coverage plots , 2013, Front. Genet..

[29]  Sarah T. Wagner,et al.  Detecting and Characterizing the Highly Divergent Plastid Genome of the Nonphotosynthetic Parasitic Plant Hydnora visseri (Hydnoraceae) , 2016, Genome biology and evolution.

[30]  M. Vallejo‐Marín,et al.  Strongly asymmetric hybridization barriers shape the origin of a new polyploid species and its hybrid ancestor. , 2016, American journal of botany.

[31]  A. Liston,et al.  Horizontal Transfer of DNA from the Mitochondrial to the Plastid Genome and Its Subsequent Evolution in Milkweeds (Apocynaceae) , 2013, Genome biology and evolution.

[32]  Matthew A. Gitzendanner,et al.  Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America , 1997, Plant Systematics and Evolution.

[33]  Mark Fishbein,et al.  Hyb-Seq: Combining target enrichment and genome skimming for plant phylogenomics , 2014, Applications in plant sciences.

[34]  C. Cox,et al.  Analyses of Charophyte Chloroplast Genomes Help Characterize the Ancestral Chloroplast Genome of Land Plants , 2014, Genome biology and evolution.

[35]  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.

[36]  S. Jackson,et al.  Cytogenomic Analyses Reveal the Structural Plasticity of the Chloroplast Genome in Higher Plants , 2001, Plant Cell.

[37]  De-Zhu Li,et al.  Evidence for horizontal transfer of mitochondrial DNA to the plastid genome in a bamboo genus , 2015, Scientific Reports.

[38]  David C. Tank,et al.  A Phylogenomic Approach Based on PCR Target Enrichment and High Throughput Sequencing: Resolving the Diversity within the South American Species of Bartsia L. (Orobanchaceae) , 2016, PloS one.

[39]  W. John Kress,et al.  A DNA barcode for land plants , 2009, Proceedings of the National Academy of Sciences.

[40]  Kui Lin,et al.  Sequencing Angiosperm Plastid Genomes Made Easy: A Complete Set of Universal Primers and a Case Study on the Phylogeny of Saxifragales , 2013, Genome biology and evolution.

[41]  C. Specht The rise of evo-devo: Pan-American Society for Evolutionary Developmental Biology sets the stage. , 2016, American journal of botany.

[42]  Nam V. Hoang,et al.  Next Generation Sequencing of total DNA from sugarcane provides no evidence for chloroplast heteroplasmy , 2015 .

[43]  Peng-Fei Ma,et al.  High-Throughput Sequencing of Six Bamboo Chloroplast Genomes: Phylogenetic Implications for Temperate Woody Bamboos (Poaceae: Bambusoideae) , 2011, PloS one.

[44]  Jerrold I. Davis,et al.  Resolving relationships within the palm subfamily Arecoideae (Arecaceae) using plastid sequences derived from next-generation sequencing. , 2015, American journal of botany.

[45]  Jerrold I. Davis,et al.  The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation. , 2012, American journal of botany.

[46]  David C. Tank,et al.  A long PCR–based approach for DNA enrichment prior to next-generation sequencing for systematic studies1 , 2014, Applications in plant sciences.

[47]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[48]  Gregory W. Stull,et al.  A targeted enrichment strategy for massively parallel sequencing of angiosperm plastid genomes , 2013, Applications in plant sciences.

[49]  A. Lemmon,et al.  High-Throughput Genomic Data in Systematics and Phylogenetics , 2013 .

[50]  D. Smith,et al.  The (in)complete organelle genome: exploring the use and nonuse of available technologies for characterizing mitochondrial and plastid chromosomes , 2016, Molecular ecology resources.

[51]  A. J. Bendich Why do chloroplasts and mitochondria contain so many copies of their genome? , 1987, BioEssays : news and reviews in molecular, cellular and developmental biology.

[52]  V. Savolainen,et al.  The use of herbarium specimens in DNA phylogenetics: Evaluation and improvement , 1995, Plant Systematics and Evolution.

[53]  Burke,et al.  A target enrichment method for gathering phylogenetic information from hundreds of loci: An example from the Compositae , 2014, Applications in plant sciences.

[54]  Bernd Weisshaar,et al.  SMRT sequencing only de novo assembly of the sugar beet (Beta vulgaris) chloroplast genome , 2015, BMC Bioinformatics.

[55]  D. Spooner,et al.  Against the traffic , 2012, Mobile genetic elements.

[56]  P. Šmarda,et al.  Measurements of genomic GC content in plant genomes with flow cytometry: a test for reliability. , 2012, The New phytologist.

[57]  P. Taberlet,et al.  Understanding the evolution of holoparasitic plants: the complete plastid genome of the holoparasite Cytinus hypocistis (Cytinaceae). , 2016, Annals of botany.

[58]  Jeffrey D. Palmer,et al.  Chloroplast DNA Evolution and Biosystematic Uses of Chloroplast DNA Variation , 1987, The American Naturalist.

[59]  Rens Holmer,et al.  Herbarium genomics: plastome sequence assembly from a range of herbarium specimens using an Iterative Organelle Genome Assembly pipeline , 2016 .

[60]  R. Petit,et al.  Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. , 2005, Molecular ecology.

[61]  R. Kolodner,et al.  Inverted repeats in chloroplast DNA from higher plants. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Peter M Hollingsworth,et al.  Telling plant species apart with DNA: from barcodes to genomes , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[63]  Z. Quan,et al.  A precise chloroplast genome of Nelumbo nucifera (Nelumbonaceae) evaluated with Sanger, Illumina MiSeq, and PacBio RS II sequencing platforms: insight into the plastid evolution of basal eudicots , 2014, BMC Plant Biology.

[64]  J. Tomkins,et al.  Complete chloroplast genome sequences of Hordeum vulgare, Sorghum bicolor and Agrostis stolonifera, and comparative analyses with other grass genomes , 2007, Theoretical and Applied Genetics.

[65]  M. Pellegrini,et al.  Conservation and divergence of methylation patterning in plants and animals , 2010, Proceedings of the National Academy of Sciences.

[66]  Y. Vigouroux,et al.  A Set of 100 Chloroplast DNA Primer Pairs to Study Population Genetics and Phylogeny in Monocotyledons , 2011, PloS one.

[67]  Paul R. Sesink Clee,et al.  Environmental variation and rivers govern the structure of chimpanzee genetic diversity in a biodiversity hotspot , 2015, BMC Evolutionary Biology.

[68]  C. dePamphilis,et al.  Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants , 2016, Proceedings of the National Academy of Sciences.

[69]  Shu-Yan Mao,et al.  Thirteen Camelliachloroplast genome sequences determined by high-throughput sequencing: genome structure and phylogenetic relationships , 2014, BMC Evolutionary Biology.

[70]  De‐Zhu Li,et al.  Highly effective sequencing whole chloroplast genomes of angiosperms by nine novel universal primer pairs , 2014, Molecular ecology resources.

[71]  T. Mockler,et al.  Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by-synthesis technology , 2008, Nucleic acids research.

[72]  Gregory L. Wheeler,et al.  A review of the prevalence, utility, and caveats of using chloroplast simple sequence repeats for studies of plant biology , 2014, Applications in plant sciences.

[73]  Dario Leister,et al.  Chloroplast research in the genomic age. , 2003, Trends in genetics : TIG.

[74]  Kai F. Müller,et al.  The evolution of the plastid chromosome in land plants: gene content, gene order, gene function , 2011, Plant Molecular Biology.

[75]  Linda A. Raubeson,et al.  Does complete plastid genome sequencing improve species discrimination and phylogenetic resolution in Araucaria? , 2015, Molecular ecology resources.

[76]  P. Keeling,et al.  Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes , 2015, Proceedings of the National Academy of Sciences.

[77]  P. Keeling,et al.  Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives , 2015, Proceedings of the National Academy of Sciences.

[78]  N. Brisson,et al.  Recombination and the maintenance of plant organelle genome stability. , 2010, The New phytologist.

[79]  K. Sjölander,et al.  The Arabidopsis thaliana Chloroplast Proteome Reveals Pathway Abundance and Novel Protein Functions , 2004, Current Biology.

[80]  Ingolf Steffan-Dewenter,et al.  Increased efficiency in identifying mixed pollen samples by meta-barcoding with a dual-indexing approach , 2015, BMC Ecology.

[81]  J. Chave,et al.  Genome skimming by shotgun sequencing helps resolve the phylogeny of a pantropical tree family , 2014, Molecular ecology resources.

[82]  Richard Cronn,et al.  Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes , 2009, BMC Biology.

[83]  Dan G. Bock,et al.  Genome skimming reveals the origin of the Jerusalem Artichoke tuber crop species: neither from Jerusalem nor an artichoke. , 2014, The New phytologist.

[84]  N. Colegrave,et al.  Direct estimate of the spontaneous mutation rate uncovers the effects of drift and recombination in the Chlamydomonas reinhardtii plastid genome , 2015, bioRxiv.

[85]  Y. Li,et al.  Chloroplast genome of Aconitum barbatum var. puberulum (Ranunculaceae) derived from CCS reads using the PacBio RS platform , 2015, Front. Plant Sci..

[86]  Yan Zhang,et al.  Mechanisms of Functional and Physical Genome Reduction in Photosynthetic and Nonphotosynthetic Parasitic Plants of the Broomrape Family[W][OPEN] , 2013, Plant Cell.

[87]  G. McFadden,et al.  PRIMARY AND SECONDARY ENDOSYMBIOSIS AND THE ORIGIN OF PLASTIDS , 2001 .

[88]  C. Lemieux,et al.  The Exceptionally Large Chloroplast Genome of the Green Alga Floydiella terrestris Illuminates the Evolutionary History of the Chlorophyceae , 2010, Genome biology and evolution.

[89]  Páll Melsted,et al.  Efficient counting of k-mers in DNA sequences using a bloom filter , 2011, BMC Bioinformatics.

[90]  José L. Oliver,et al.  Chloroplast genes transferred to the nuclear plant genome have adjusted to nuclear base composition and codon usage , 1990, Nucleic Acids Res..

[91]  S. Malfatti,et al.  The Complete Plastid Genome Sequence of the Secondarily Nonphotosynthetic Alga Cryptomonas paramecium: Reduction, Compaction, and Accelerated Evolutionary Rate , 2009, Genome biology and evolution.

[92]  R. Petit,et al.  Plant phylogeography based on organelle genes: an introduction , 2007 .

[93]  J. V. Van Etten,et al.  The GC-Rich Mitochondrial and Plastid Genomes of the Green Alga Coccomyxa Give Insight into the Evolution of Organelle DNA Nucleotide Landscape , 2011, PLoS ONE.

[94]  J. Wolf,et al.  A field guide to whole-genome sequencing, assembly and annotation , 2014, Evolutionary applications.

[95]  G. Vendramin,et al.  Complete Chloroplast Genome of the Multifunctional Crop Globe Artichoke and Comparison with Other Asteraceae , 2015, PloS one.