Plastome organization and evolution of chloroplast genes in Cardamine species adapted to contrasting habitats

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Hu, Shiliang ^a   Sablok, Gaurav ^a   Wang, Bo ^a   Qu, Dong ^a,b   Barbaro, Enrico ^a   Viola, Roberto ^a   Li, Mingai ^a   Varotto, Claudio ^a  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

^b NORTHWEST A F UNIVERSITY   (China)

Author keywords

Cardamine; Codon usage; Large single copy region (LSC); Molecular adaptation; Plastomes; Positive selection; Repeats; Small single copy region (SSC)

Indexed keywords

RIBOSOME RNA; TRANSFER RNA;

ANGIOSPERM; ARTICLE; CARDAMINE; CARDAMINE IMPATIENS; CARDAMINE RESEDIFOLIA; CHLOROPLAST; CHLOROPLAST GENOME; CLPP GENE; CODON USAGE; DNA BASE COMPOSITION; DNA POLYMORPHISM; ENZYME ACTIVITY; GENE FUNCTION; GENE LOSS; GENE MUTATION; GYMNOSPERM; HABITAT; INTRON; MATK GENE; MOLECULAR EVOLUTION; NDHD GENE; PHYLOGENY; PLANT GENE; PSBC GENE; RNA EDITING; RPS19 GENE; SIMPLE SEQUENCE REPEAT; START CODON; YCF1 GENE; YCF3 GENE; YCF68 GENE; ADAPTATION; CLASSIFICATION; COMPARATIVE STUDY; CYTOLOGY; DNA SEQUENCE; GENETIC SELECTION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROCEDURES; SPECIES DIFFERENCE;

BRASSICACEAE; CARDAMINE; CARDAMINE IMPATIENS;

ADAPTATION, BIOLOGICAL; CARDAMINE; CHLOROPLASTS; EVOLUTION, MOLECULAR; GENOME, CHLOROPLAST; MOLECULAR SEQUENCE DATA; PHYLOGENY; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EID: 85019254561     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1498-0     Document Type: Article

References (90)

1. Wu J, Liu B, Cheng F, Ramchiary N, Choi SR, Lim YP, et al. Sequencing of chloroplast genome using whole cellular DNA and Solexa sequencing technology. Front Plant Sci. 2012;3:243.
2. Waters DLE, Nock CJ, Ishikawa R, Rice N, Henry RJ. Chloroplast genome sequence confirms distinctness of Australian and Asian wild rice. Ecol Evol. 2012;2:211-7.
3. Plant C, Group W. A DNA barcode for land plants. Proc Natl Acad Sci U S A. 2009;106:12794-7.
4. Sugiura M. The chloroplast genome. Plant Mol Biol. 1992;19:149-68.
5. Kim K-J, Lee H-L. Complete chloroplast genome sequences from Korean ginseng (Panax schinseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Res. 2004;11:247-61.
6. Yang M, Zhang X, Liu G, Yin Y, Chen K, Yun Q, et al. The complete chloroplast genome sequence of date palm (Phoenix dactylifera L.). PLoS One. 2010;5:e12762.
7. Green BR. Chloroplast genomes of photosynthetic eukaryotes. Plant J. 2011;66:34-44.
8. Huang Y-Y, Matzke AJM, Matzke M. Complete sequence and comparative analysis of the chloroplast genome of coconut palm (Cocos nucifera). PLoS One. 2013;8:e74736.
9. Braukmann T, Kuzmina M, Stefanović S. Plastid genome evolution across the genus Cuscuta (Convolvulaceae): two clades within subgenus Grammica exhibit extensive gene loss. J Exp Bot. 2013;64:977-89.
10. Ku C, Hu JM, Kuo CH. Complete plastid genome sequence of the basal asterid Ardisia polysticta Miq. and comparative analyses of asterid plastid genomes. PLoS One. 2013;8:e62548.
11. Westhoff P, Herrmann RG. Complex RNA maturation in chloroplasts: the psbB operon from spinach. Eur J Biochem. 1988;171:551-64.
12. Barkan A. Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol. 2011;155:1520-32.
13. Kugita M. RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res. 2003;31:2417-23.
14. Wolf PG, Hasebe M, Rowe CA. High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. Gene. 2004;339:89-97.
15. Carlsen T, Bleeker W, Hurka H, Elven R, Brochmann C. Biogeography and phylogeny of Cardamine (Brassicaceae). Ann Missouri Bot Gard. 2009;96:215-36.
16. Marhold K, Lihová J. Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae. Plant Syst Evol. 2006;259:143-74.
17. Lihová J, Marhold K. Worldwide phylogeny and biogeography of Cardamine flexuosa (Brassicaceae) and its relatives. Am J Bot. 2006;93:1206-21.
18. Huffman KM. Investigation into the potential invasiveness of the exotic narrow-leaved bittercress, (Cardamine impatiens L.), Brassicaceae. Master's Thesis. Virginia Polytechnic Institute and State University, Biological Sciences Department. 2008.
19. Canales C, Barkoulas M, Galinha C, Tsiantis M. Weeds of change: Cardamine hirsuta as a new model system for studying dissected leaf development. J Plant Res. 2010;123:25-33.
20. Zhou C-M, Zhang T-Q, Wang X, Yu S, Lian H, Tang H, et al. Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science. 2013;340:1097-100.
21. Morinaga SI, Nagano AJ, Miyazaki S, Kubo M, Demura T, Fukuda H, et al. Ecogenomics of cleistogamous and chasmogamous flowering: genome-wide gene expression patterns from cross-species microarray analysis in Cardamine kokaiensis (Brassicaceae). J Ecol. 2008;96:1086-97.
22. Ometto L, Li M, Bresadola L, Varotto C. Rates of evolution in stress-related genes are associated with habitat preference in two Cardamine lineages. BMC Evol Biol. 2012;12:7.
23. Qian J, Song J, Gao H, Zhu Y, Xu J, Pang X, et al. The complete chloroplast genome sequence of the medicinal plant Salvia miltiorrhiza. PLoS One. 2013;8:e57607.
24. Hildebrand M, Hallick RB, Passavant CW, Bourque DP. Trans-splicing in chloroplasts: the rps 12 loci of Nicotiana tabacum. Proc Natl Acad Sci U S A. 1988;85:372-6.
25. Liu Y, Huo N, Dong L, Wang Y, Zhang S, Young HA, et al. Complete Chloroplast genome sequences of Mongolia medicine Artemisia frigida and phylogenetic relationships with other plants. PLoS One. 2013;8:e57533.
26. Sweeney PW, Price RA. Polyphyly of the genus Dentaria (Brassicaceae): evidence from trnL intron and ndhF sequence data. Syst Bot. 2000;25:468-78.
27. Kuroda H, Suzuki H, Kusumegi T, Hirose T, Yukawa Y, Sugiura M. Translation of psbC mRNAs starts from the downstream GUG, not the upstream AUG, and requires the extended Shine-Dalgarno sequence in tobacco chloroplasts. Plant Cell Physiol. 2007;48:1374-8.
28. Moore MJ, Bell CD, Soltis PS, Soltis DE. Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci U S A. 2007;104:19363-8.
29. Rohde W, Gramstat A, Schmitz J, Tacke E, Prüfer D. Plant viruses as model systems for the study of non-canonical translation mechanisms in higher plants. J Gen Virol. 1994;75:2141-9.
30. Neckermann K, Zeltz P, Igloi GL, Kössel H, Maier RM. The role of RNA editing in conservation of start codons in chloroplast genomes. Gene. 1994;146:177-82.
31. Hirose T, Sugiura M. Both RNA editing and RNA cleavage are required for translation of tobacco chloroplast ndhD mRNA: a possible regulatory mechanism for the expression of a chloroplast operon consisting of functionally unrelated genes. EMBO J. 1997;16:6804-11.
32. Sasaki T, Yukawa Y, Miyamoto T, Obokata J, Sugiura M. Identification of RNA editing sites in chloroplast transcripts from the maternal and paternal progenitors of tobacco (Nicotiana tabacum): comparative analysis shows the involvement of distinct trans-factors for ndhB editing. Mol Biol Evol. 2003;20:1028-35.
33. Zandueta-Criado A, Bock R. Surprising features of plastid ndhD transcripts: addition of non-encoded nucleotides and polysome association of mRNAs with an unedited start codon. Nucleic Acids Res. 2004;32:542-50.
34. Kawabe A, Miyashita NT. Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet Syst. 2003;78:343-52.
35. Plotkin JB, Kudla G. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet. 2011;12:32-42.
36. Liu Q, Feng Y, Xue Q. Analysis of factors shaping codon usage in the mitochondrion genome of Oryza sativa. Mitochondrion. 2004;4:313-20.
37. Liu Q, Xue Q. Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species. J Genet. 2005;84:55-62.
38. Zhang W, Zhou J, Li Z, Wang L, Gu X, Zhong Y. Comparative analysis of codon usage patterns among mitochondrion, chloroplast and nuclear genes in Triticum aestivum L. Acta Botanica Sinica. 2007;49:246-54.
39. 3, and evolutionary patterns across plastomes of three pooid model species: emerging grass genome models for monocots. Mol Biotechnol. 2011;49:116-28.
40. Zhou M, Li X. Analysis of synonymous codon usage patterns in different plant mitochondrial genomes. Mol Biol Rep. 2009;36:2039-46.
41. Nair RR, Nandhini MB, Monalisha E, Murugan K, Nagarajan S, Surya N, et al. Synonymous codon usage in chloroplast genome of Coffea arabica. Bioinformation. 2012;8:1096-104.
42. Morton BR, So BG. Codon usage in plastid genes is correlated with context, position within the gene, and amino acid content. J Mol Evol. 2000;50:184-93.
43. Kučera J, Lihová J, Marhold K. Taxonomy and phylogeography of Cardamine impatiens and C. pectinata (Brassicaceae). Bot J Linn Soc. 2006;152:169-95.
44. Sablok G, Mudunuri SB, Patnana S, Popova M, Fares MA, La Porta N. Chloromitossrdb: open source repository of perfect and imperfect repeats in organelle genomes for evolutionary genomics. DNA Res. 2013;20:127-33.
45. Schlötterer C, Harr B. Microsatellite instability. Encycl life Sci. 2001:1-4.
46. Gandhi SG, Awasthi P, Bedi YS. Analysis of SSR dynamics in chloroplast genomes of Brassicaceae family. Bioinformation. 2010;5:1-5.
47. Couvreur TLP, Franzke A, Al-shehbaz IA, Bakker FT, Koch A, Mummenhoff K. Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol Biol Evol. 2010;27:55-71.
48. Franzke A, Lysak MA, Al-Shehbaz IA, Koch MA, Mummenhoff K. Cabbage family affairs: the evolutionary history of Brassicaceae. Trends Plant Sci. 2011;16:108-16.
49. Duchene D, Bromham L. Rates of molecular evolution and diversification in plants: chloroplast substitution rates correlated with species-richness in the Proteaceae. BMC Evol Biol. 2013;13:65.
50. Wicke S, Schäferhoff B, Depamphilis CW, Müller KF. Disproportional plastome-wide increase of substitution rates and relaxed purifying selection in genes of carnivorous Lentibulariaceae. Mol Biol Evol. 2014;31:529-45.
51. Drescher A, Stephanie R, Calsa T, Carrer H, Bock R. The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. Plant J. 2000;22:97-104.
52. Huang JL, Sun GL, Zhang DM. Molecular evolution and phylogeny of the angiosperm ycf2 gene. J Syst Evol. 2010;48:240-8.
53. Kikuchi S, Bédard J, Hirano M, Hirabayashi Y, Oishi M, Imai M, et al. Uncovering the protein translocon at the chloroplast inner envelope membrane. Science. 2013;339:571-4.
54. Kode V, Mudd EA, Iamtham S, Day A. The tobacco plastid accD gene is essential and is required for leaf development. Plant J. 2005;44:237-44.
55. Rousseau-Gueutin M, Huang X, Higginson E, Ayliffe M, Day A, Timmis JN. Potential functional replacement of the plastidic acetyl-CoA carboxylase subunit (accD) gene by recent transfers to the nucleus in some angiosperm lineages. Plant Physiol. 2013;161:1918-29.
56. Ohlrogge J, Browse J. Lipid biosynthesis. Plant Cell. 1995;7:957-70.
57. Sasaki Y, Nagano Y. Plant acetyl-CoA carboxylase: structure, biosynthesis, regulation, and gene manipulation for plant breeding. Biosci Biotechnol Biochem. 2004;68:1175-84.
58. Feria Bourrellier AB, Valot B, Guillot A, Ambard-Bretteville F, Vidal J, Hodges M. Chloroplast acetyl-CoA carboxylase activity is 2-oxoglutarate-regulated by interaction of PII with the biotin carboxyl carrier subunit. Proc Natl Acad Sci U S A. 2010;107:502-7.
59. Madoka Y, Tomizawa K, Mizoi J, Nishida I, Nagano Y, Sasaki Y. Chloroplast transformation with modified accD operon increases acetyl- CoA carboxylase and causes extension of leaf longevity and increase in seed yield in tobacco. Plant Cell Physiol. 2002;43:1518-25.
60. Allen JF, de Paula WBM, Puthiyaveetil S, Nield J. A structural phylogenetic map for chloroplast photosynthesis. Trends Plant Sci. 2011;16:645-55.
61. Sen L, Fares M, Su Y-J, Wang T. Molecular evolution of psbA gene in ferns: unraveling selective pressure and co-evolutionary pattern. BMC Evol Biol. 2012;12:145.
62. Wang M, Kapralov MV, Anisimova M. Coevolution of amino acid residues in the key photosynthetic enzyme Rubisco. BMC Evol Biol. 2011;11:266.
63. Sen L, Fares MA, Liang B, Gao L, Wang B, Wang T, et al. Molecular evolution of rbcL in three gymnosperm families: identifying adaptive and coevolutionary patterns. Biol Direct. 2011;6:29.
64. Kapralov MV, Smith JAC, Filatov DA. Rubisco evolution in C4 eudicots: an analysis of Amaranthaceae sensu lato. PLoS One. 2012;7:e52974.
65. Tabita FR, Hanson TE, Satagopan S, Witte BH, Kreel NE. Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms. Philos Trans R Soc Lond B Biol Sci. 2008;363:2629-40.
66. Tabita FR, Hanson TE, Li H, Satagopan S, Singh J, Chan S. Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol Mol Biol Rev. 2007;71:576-99.
67. Studer RA, Christin P-A, Williams MA, Orengo CA. Stability-activity tradeoffs constrain the adaptive evolution of RubisCO. Proc Natl Acad Sci U S A. 2014;111:2223-8.
68. Parry MAJ. Manipulation of Rubisco: the amount, activity, function and regulation. J Exp Bot. 2003;54:1321-33.
69. Greiner S, Bock R. Tuning a ménage à trois: co-evolution and co-adaptation of nuclear and organellar genomes in plants. Bioessays. 2013;35:354-65.
70. Romiguier J, Figuet E, Galtier N, Douzery EJP, Boussau B, Dutheil JY, et al. Fast and robust characterization of time-heterogeneous sequence evolutionary processes using substitution mapping. PLoS One. 2012;7:e33852.
71. Gale J. Plants and altitude-revisited. Ann Bot. 2004;94:199.
72. 13C of butterfly bush (Buddleja davidii) plants growing at high elevations. Physiol Plant. 2006;128:722-31.
73. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078-9.
74. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18:821-9.
75. Gao S, Sung WK, Nagarajan N. Opera: reconstructing optimal genomic scaffolds with high-throughput paired-end sequences. J Comput Biol. 2011;18:1681-91.
76. Ronen R, Boucher C, Chitsaz H, Pevzner P. sEQuel: improving the accuracy of genome assemblies. Bioinformatics. 2012;28:i188-96.
77. Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol. 2012;13:R56.
78. Delcher AL, Phillippy A, Carlton J, Salzberg SL. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 2002;30:2478-83.
79. Grant JR, Arantes AS, Stothard P. Comparing thousands of circular genomes using the CGView Comparison Tool. BMC Genomics. 2012;13:202.
80. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004;32:W273-9.
81. Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 2001;29:4633-42.
82. Liu C, Shi L, Zhu Y, Chen H, Zhang J, Lin X, et al. CpGAVAS, an integrated web server for the annotation, visualization, analysis, and GenBank submission of completely sequenced chloroplast genome sequences. BMC Genomics. 2012;13:715.
83. Wyman SK, Jansen RK, Boore JL. Automatic annotation of organellar genomes with DOGMA. Bioinformatics. 2004;20:3252-5.
84. Conant GC, Wolfe KH. GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics. 2008;24:861-2.
85. Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 2005;33:W686-9.
86. Wright F. The "effective number of codons" used in a gene. Gene. 1990;87:23-9.
87. Ranwez V, Harispe S, Delsuc F, Douzery EJP. MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS One. 2011;6:e22594.
88. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772.
89. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688-90.
90. Stern A, Doron-Faigenboim A, Erez E, Martz E, Bacharach E, Pupko T. Selecton 2007: advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res. 2007;35:W506-11.