Highly rearranged and size-variable chloroplast genomes in conifers II clade (cupressophytes): Evolution towards shorter intergenic spacers

Plant Biotechnology Journal

Volumn 12, Issue 3, 2014, Pages 344-353

  Wu, Chung Shien ^a   Chaw, Shu Miaw ^a  

^a BIODIVERSITY RESEARCH CENTER   (Taiwan)

Author keywords

Chloroplast genome; Conifer; Cupressophyte; Genomic rearrangement; Genomic reduction; Gymnosperm

Indexed keywords

AGATHIS DAMMARA; CALOCEDRUS FORMOSANA; CONIFEROPHYTA; GYMNOSPERMAE; NAGEIA NAGI; PINACEAE;

CHLOROPLAST DNA; PLANT DNA; SPACER DNA;

ARTICLE; CHEMISTRY; CHLOROPLAST; CHLOROPLAST GENOME; CONIFER; CUPRESSOPHYTE; DNA SEQUENCE; GENE REARRANGEMENT; GENETIC VARIABILITY; GENETICS; GENOME SIZE; GENOMIC REARRANGEMENT; GENOMIC REDUCTION; GYMNOSPERM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MUTATION; PHYLOGENY; PLANT LEAF; SEQUENCE ALIGNMENT;

CHLOROPLAST GENOME; CONIFER; CUPRESSOPHYTE; GENOMIC REARRANGEMENT; GENOMIC REDUCTION; GYMNOSPERM;

CHLOROPLASTS; CONIFEROPHYTA; DNA, CHLOROPLAST; DNA, INTERGENIC; DNA, PLANT; EVOLUTION, MOLECULAR; GENE REARRANGEMENT; GENOME SIZE; GENOME, CHLOROPLAST; GENOMIC STRUCTURAL VARIATION; MOLECULAR SEQUENCE ANNOTATION; MUTATION; PHYLOGENY; PLANT LEAVES; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

EID: 84896401436     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12141     Document Type: Article

References (54)

1. Barrett, C.F. and Davis, J.I. (2012) The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation. Am. J. Bot. 99, 1513-1523.
2. Blazier, J.C., Guisinger, M.M. and Jansen, R.K. (2011) Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae). Plant Mol. Biol. 76, 263-272.
3. Bourque, G. and Pevzner, P.A. (2002) Genome-scale evolution: reconstructing gene orders in the ancestral species. Genome Res. 12, 26-36.
4. Bowe, L.M., Coat, G. and dePamphilis, C.W. (2000) Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. Proc. Natl Acad. Sci. USA, 97, 4092-4097.
5. Chang, C.C., Lin, H.C., Lin, I.P., Chow, T.Y., Chen, H.H., Chen, W.H., Cheng, C.H., Lin, C.Y., Liu, S.M., Chang, C.C. and Chaw, S.M. (2006) The chloroplast genome of Phalaenopsis aphrodite (Orchidaceae): comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Mol. Biol. Evol. 23, 279-291.
6. Chaw, S.M., Parkinson, C.L., Cheng, Y., Vincent, T.M. and Palmer, J.D. (2000) Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc. Natl Acad. Sci. USA, 97, 4086-4091.
7. Christensen, A.C. (2013) Plant mitochondrial genome evolution can be explained by DNA repair mechanisms. Genome Biol. Evol. 5, 1079-1086.
8. Chumley, T.W., Palmer, J.D., Mower, J.P., Fourcade, H.M., Calie, P.J., Boore, J.L. and Jansen, R.K. (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.
9. Cui, L., Leebens-Mack, J., Wang, L.S., Tang, J., Rymarquis, L., Stern, D.B. and dePamphilis, C.W. (2006) Adaptive evolution of chloroplast genome structure inferred using a parametric bootstrap approach. BMC Evol. Biol. 6, 13.
10. Dagan, T., Roettger, M., Stucken, K., Landan, G., Koch, R., Major, P., Gould, S.B., Goremykin, V.V., Rippka, R., Tandeau de Marsac, N., Gugger, M., Lockhart, P.J., Allen, J.F., Brune, I., Maus, I., Pühler, A. and Martin, W.F. (2013) Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol. Evol. 5, 31-44.
11. Darling, A.E., Mau, B. and Perna, N.T. (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE, 5, e11147.
12. Delannoy, E., Fujii, S., Colas des Francs-Small, C., Brundrett, M. and Small, I. (2011) Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol. Biol. Evol. 28, 2077-2086.
13. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797.
14. Guisinger, M.M., Kuehl, J.V., Boore, J.L. and Jansen, R.K. (2008) Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc. Natl Acad. Sci. USA, 105, 18424-18429.
15. Guisinger, M.M., Kuehl, J.V., Boore, J.L. and Jansen, R.K. (2011) Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage. Mol. Biol. Evol. 28, 583-600.
16. Haberle, R.C., Fourcade, H.M., Boore, J.L. and Jansen, R.K. (2008) Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. J. Mol. Evol. 66, 350-361.
17. Hirao, T., Watanabe, A., Kurita, M., Kondo, T. and 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.
18. Jansen, R.K. and Ruhlman, T.A. (2012) Plastid genomes in seed plants. In Genomics of Chloroplasts and Mitochondria (Bock, R. and Knoop, V., eds), pp. 103-126. Dordrecht, The Netherlands: Springer.
19. Knox, E.B. and Palmer, J.D. (1999) The chloroplast genome arrangement of Lobelia thuliana (Lobeliaceae): expansion of the inverted repeat in an ancestor of the Campanulales. Plant Syst. Evol. 214, 49-64.
20. Koskiniemi, S., Sun, S., Berg, O.G. and Andersson, D.I. (2012) Selection-driven gene loss in bacteria. PLoS Genet. 8, e1002787.
21. Kuo, C.H., Moran, N.A. and Ochman, H. (2009) The consequences of genetic drift for bacterial genome complexity. Genome Res. 19, 1450-1454.
22. Lee, H.L., Jansen, R.K., Chumley, T.W. and 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.
23. Leslie, A.B., Beaulieu, J.M., Rai, H.S., Crane, P.R., Donoghue, M.J. and Mathews, S. (2012) Hemisphere-scale differences in conifer evolutionary dynamics. Proc. Natl Acad. Sci. USA, 109, 16217-16221.
24. Lin, C.P., Huang, J.P., Wu, C.S., Hsu, C.Y. and Chaw, S.M. (2010) Comparative chloroplast genomics reveals the evolution of Pinaceae genera and subfamilies. Genome Biol. Evol. 2, 504-517.
25. Lin, C.P., Wu, C.S., Huang, Y.Y. and Chaw, S.M. (2012) The complete chloroplast genome of Ginkgo biloba reveals the mechanism of inverted repeat contraction. Genome Biol. Evol. 4, 374-381.
26. Logacheva, M.D., Schelkunov, M.I. and Penin, A.A. (2011) Sequencing and analysis of plastid genome in mycoheterotrophic orchid Neottia nidus-avis. Genome Biol. Evol. 3, 1296-1303.
27. Lynch, M., Koskella, B. and Schaack, S. (2006) Mutation pressure and the evolution of organelle genomic architecture. Science, 311, 1727-1730.
28. Mao, K., Milne, R.I., Zhang, L., Peng, Y., Liu, J., Thomas, P., Mill, R.R. and Renner, S.S. (2012) Distribution of living Cupressaceae reflects the breakup of Pangea. Proc. Natl Acad. Sci. USA, 109, 7793-7798.
29. Maréchal, A., Parent, J., Véronneau-Lafortune, F., Joyeux, A., Lang, B. and Brisson, N. (2009) Whirly proteins maintain plastid genome stability in Arabidopsis. Proc. Natl Acad. Sci. USA, 106, 14693-14698.
30. Martin, G., Baurens, F.C., Cardi, C., Aury, J.M. and D'Hont, A. (2013) The complete chloroplast genome of banana (Musa acuminata, Zingiberales): insight into plastid monocotyledon evolution. PLoS ONE, 8, e67350.
31. McCoy, S.R., Kuehl, J.V., Boore, J.L. and Raubeson, L.A. (2008) The complete plastid genome sequence of Welwitschia mirabilis: an unusually compact plastome with accelerated divergence rates. BMC Evol. Biol. 8, 130.
32. Miller-Messmer, M., Kühn, K., Bichara, M., Le Ret, M., Imbault, P. and Gualberto, J.M. (2012) RecA-dependent DNA repair results in increased heteroplasmy of the Arabidopsis mitochondrial genome. Plant Physiol. 159, 211-226.
33. Palmer, J.D. (1983) Chloroplast DNA exists in two orientations. Nature, 301, 92-93.
34. Ran, J.H., Gao, H. and Wang, X.Q. (2010) Fast evolution of the retroprocessed mitochondrial rps3 gene in Conifer II and further evidence for the phylogeny of gymnosperms. Mol. Phylogenet. Evol. 54, 136-149.
35. Raubeson, L.A. and Jansen, R.K. (1992) A rare chloroplast DNA structural mutation is shared by all conifers. Biochem. Syst. Ecol. 20, 17-24.
36. Regina, T.M. and Quagliariello, C. (2010) Lineage-specific group II intron gains and losses of the mitochondrial rps3 gene in gymnosperms. Plant Physiol. Biochem. 48, 646-654.
37. Rowan, B.A., Oldenburg, D.J. and Bendich, A.J. (2010) RecA maintains the integrity of chloroplast DNA molecules in Arabidopsis. J. Exp. Bot. 61, 2575-2588.
38. Schattner, P., Brooks, A.N. and Lowe, T.M. (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33, W686-W689.
39. Sloan, D.B., Alverson, A.J., Chuckalovcak, J.P., Wu, M., McCauley, D.E., Palmer, J.D. and Taylor, D.R. (2012) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 10, e1001241.
40. Stewart, C.N. Jr. and Via, L.E. (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques, 14, 748-751.
41. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739.
42. Wang, R.J., Cheng, C.L., Chang, C.C., Wu, C.L., Su, T.M. and Chaw, S.M. (2008) Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol. Biol. 8, 36.
43. Wicke, S., Schneeweiss, G.M., dePamphilis, C.W., Müller, K.F. and Quandt, D. (2011) The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol. Biol. 76, 273-297.
44. Williams, C.G. (2009) Conifer Reproductive Biology. Dordrecht, Heidelberg, London, New York: Springer, pp. 3-19.
45. Wolf, P.G. (2012) Plastid genome diversity. In Plant Genome Diversity, vol 1, Plant Genomes, Their Residents, and Their Evolutionary Dynamics (Wendel, J.F., Greilhuber, J., Doležel, J. and Leitch, I.J., eds), pp. 145-152. Wien, Heidelberg, New York, Dordrecht, London: Springer.
46. Wolfe, K.H., Morden, C.W. and Palmer, J.D. (1992) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc. Natl Acad. Sci. USA, 89, 10648-10652.
47. Wu, C.S., Lai, Y.T., Lin, C.P., Wang, Y.N. and Chaw, S.M. (2009) Evolution of reduced and compact chloroplast genomes (cpDNAs) in gnetophytes: selection toward a lower-cost strategy. Mol. Phylogenet. Evol. 52, 115-124.
48. Wu, C.S., Wang, Y.N., Hsu, C.Y., Lin, C.P. and Chaw, S.M. (2011a) Loss of different inverted repeat copies from the chloroplast genomes of Pinaceae and cupressophytes and influence of heterotachy on the evaluation of gymnosperm phylogeny. Genome Biol. Evol. 3, 1284-1295.
49. Wu, C.S., Lin, C.P., Hsu, C.Y., Wang, R.J. and Chaw, S.M. (2011b) Comparative chloroplast genomes of Pinaceae: insights into the mechanism of diversified genomic organizations. Genome Biol. Evol. 3, 309-319.
50. Wyman, S.K., Jansen, R.K. and Boore, J.L. (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics, 20, 3252-3255.
51. Yi, X., Gao, L., Wang, B., Su, Y.J. and Wang, T. (2013) The complete chloroplast genome sequence of Cephalotaxus oliveri (Cephalotaxaceae): evolutionary comparison of Cephalotaxus chloroplast DNAs and insights into the loss of inverted repeat copies in gymnosperms. Genome Biol. Evol. 5, 688-698.
52. Yue, F., Cui, L., dePamphilis, C.W., Moret, B.M. and Tang, J. (2008) Gene rearrangement analysis and ancestral order inference from chloroplast genomes with inverted repeat. BMC Genomics, 9, S25.
53. Zhong, B., Yonezawa, T., Zhong, Y. and Hasegawa, M. (2010) The position of gnetales among seed plants: overcoming pitfalls of chloroplast phylogenomics. Mol. Biol. Evol. 27, 2855-2863.
54. Zhong, B., Deusch, O., Goremykin, V.V., Penny, D., Biggs, P.J., Atherton, R.A., Nikiforova, S.V. and Lockhart, P.J. (2011) Systematic error in seed plant phylogenomics. Genome Biol. Evol. 3, 1340-1348.