The first complete chloroplast genome of the Genistoid legume Lupinus luteus: Evidence for a novel major lineage-specific rearrangement and new insights regarding plastome evolution in the legume family

Annals of Botany

Volumn 113, Issue 7, 2014, Pages 1197-1210

  Martin, Guillaume E ^a,c   Rousseau Gueutin, Mathieu ^a   Cordonnier, Solenn ^a   Lima, Oscar ^a   Michon Coudouel, Sophie ^b   Naquin, Delphine ^a,d   De Carvalho, Julie Ferreira ^a   Aïnouche, Malika ^a   Salmon, Armel ^a   Aïnouche, Abdelkader ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UMR AGAP   (France)

^d CNRS   (France)

Author keywords

36 kb inversion; chloroplast genome evolution; European yellow lupine; Fabaceae phylogeny; flip flop recombination; functional gene transfer; Genistoid clade; inverted repeats; legume; lineage specific marker; Lupinus luteus; Papilionoidae; plastome hotspots; repeated plastid sequences; sequence divergence; structural plastid rearrangement

Indexed keywords

AMINO ACID; CHLOROPLAST; COMPARATIVE STUDY; DIVERGENCE; GENE TRANSFER; GENOME; LEGUME; PHYLOGENETICS; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN; RECOMBINATION;

CHLOROPLAST GENOME; CLASSIFICATION; DNA SEQUENCE; GENETICS; LUPIN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; POLYMERASE CHAIN REACTION;

EVOLUTION, MOLECULAR; GENOME, CHLOROPLAST; LUPINUS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA;

EID: 84901405949     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcu050     Document Type: Article

References (80)

1. Ainouche A, Bayer RJ. 1999. Phylogenetic relationships in Lupinus (Fabaceae: Papilionoideae) based on internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA. American Journal of Botany 86: 590-607.
2. Ainouche A, Bayer RJ, Misset MT. 2004. Molecular phylogeny, diversification and character evolution in Lupinus (Fabaceae) with special attention to Mediterranean and African lupines. Plant Systematics and Evolution 246: 211-222.
3. Bartha L, Dragos N, Molnár V, Sramkó G. 2013. Molecular evidence for reticulate speciation in Astragalus (Fabaceae) as revealed by a case study from sect. Dissitiflori. Botany 91: 702-714.
4. Bruneau A, Doyle JJ, Palmer JD. 1990. Achloroplast DNAstructural mutation as a subtribal character in the Phaseoleae (Leguminosae). Systematic Botany 15: 378-386.
5. Cai Z, Guisinger M, Kim HG, et al. 2008. Extensive reorganization of the plastid genome ofTrifolium subterraneum (Fabaceae) is associated with numerous repeated sequences and novelDNAinsertions. Journal of Molecular Evolution 67: 696-704.
6. Cardoso D, de Queiroz LP, Pennington RT, et al. 2012. Revisiting the phylogeny of papilionoid legumes: new insights from comprehensively sampled early-branching lineages. American Journal of Botany 99: 1991-2013.
7. Chevreux B, Wetter T, Suhai S. 1999. Genome sequence assembly using trace signals and additional sequence information. In: Computer Science and Biology. Proceedings of the German Conference on Bioinformatics, GCB '99., Germany, 45-56.
8. Clegg M, Zurawski G. 1991. Chloroplast DNAand the study of plant phylogeny: present status and future prospects. In: Soltis PS, Soltis DE, Doyle JJ, eds. Molecular systematics of plants. New York: Chapman & Hall, 1-13.
9. Clegg MT, Gaut BS, Learn GHJr, Morton BR. 1994. Rates and patterns of chloroplast DNA evolution. Proceedings of the National Academy of Sciences, USA 91: 6795-6801.
10. Cosner ME, Raubeson LA, Jansen RK. 2004. Chloroplast DNA rearrangements in Campanulaceae: phylogenetic utility of highly rearranged genomes. BMC Evolutionary Biology 4: 27.
11. Crisp M, Gilmore S, van Wyk B. 2000. Molecular phylogeny of the Genistoid tribes of Papilionoid legumes. London: Royal Botanic Gardens, Kew.
12. Cronk Q, Ojeda I, Pennington RT. 2006. Legume comparative genomics: progress in phylogenetics and phylogenomics. Current Opinion in Plant Biology 9: 99-103.
13. Cui L, Veeraraghavan N, Richter A, et al. 2006. Chloroplast DB: the Chloroplast Genome Database. Nucleic Acids Research 34: 692-696.
14. Downie SR, Palmer JD. 1992. Use of chloroplast DNA re arrangements in reconstructing plant phylogeny. In: Soltis PS, Soltis DE, Doyle JJ, eds. Molecular systematics of plants. New York: Chapman & Hall, 14-35.
15. Doyle JJ, Doyle JL, Ballenger JA, Palmer JD. 1996. The distribution and phylogenetic significance of a 50-kb chloroplastDNAinversion in the flowering plant family Leguminosae. Molecular Phylogenetics and Evolution 5: 429-438.
16. Drescher A, Ruf S, Calsa TJr, Carrer H, Bock R. 2000. The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. The Plant Journal 22: 97-104.
17. Drummond CS. 2008. Diversification of Lupinus (Leguminosae) in thewestern NewWorld: derived evolution of perennial life history and colonization of montane habitats. Molecular Phylogenetics and Evolution 48: 408-421.
18. Eastwood RJ, Drummond CS, Schifino-Wittmann MT, Hughes CE. 2008. Diversity and evolutionary history of lupins - insights from new phylogenies. Proceedings of the 12th International Lupin Conference - Lupins for Health andWealth. Fremantle, Australia.
19. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
20. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology 300: 1005-1016.
21. Felsenstein J. 1985. Confidence-limits on phylogenies - an approach using the bootstrap. Evolution 39: 783-791.
22. Gantt JS, Baldauf SL, Calie PJ, Weeden NF, Palmer JD. 1991. Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO Journal 10: 3073-3078.
23. Garcinuno RM, Fernandez-Hernando P, Camara C. 2003. Evaluation of pesticide uptake by Lupinus seeds. Water Research 37: 3481-3489.
24. Guillon F, Champ MM. 2002. Carbohydrate fractions of legumes: uses in human nutrition and potential for health. British Journal of Nutrition 88: 293-306.
25. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696-704.
26. Guisinger MM, Kuehl JV, Boore JL, Jansen RK. 2011. Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage. Molecular Biology and Evolution 28: 583-600.
27. Guo X, Castillo-Ramirez S, Gonzalez V, et al. 2007. Rapid evolutionary change of common bean (Phaseolus vulgaris L) plastome, and the genomic diversification of legume chloroplasts. BMC Genomics 8: 228.
28. Hughes C, Eastwood R. 2006. Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proceedings of the National Academy of Sciences, USA 103: 10334-10339.
29. Jansen RK, Palmer JD. 1987. A chloroplast DNA inversion marks an ancient evolutionary split in the sunflower family (Asteraceae). Proceedings of the National Academy of Sciences, USA 84: 5818-5822.
30. Jansen RK, Ruhlman TA. 2012. Plastid genomes of seed plants. In: Bock R, Knoop V, eds. Genomics of chloroplast and mitochondria. New York: Springer, 103-126.
31. Jansen RK, Cai Z, Raubeson LA, et al. 2007. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proceedings of the National Academy of Sciences, USA 104: 19369-19374.
32. Jansen RK, Wojciechowski MF, Sanniyasi E, Lee SB, Daniell H. 2008. Complete plastid genome sequence of the chickpea (Cicer arietinum) and the phylogenetic distribution of rps12 and clpP intron losses among legumes (Leguminosae). Molecular Phylogenetics and Evolution 48: 1204-1217.
33. Kato T, Kaneko T, Sato S, Nakamura Y, Tabata S. 2000. Complete structure of the chloroplast genome of a legume, Lotus japonicus. DNA Research 7: 323-330.
34. Kazakoff SH, Imelfort M, Edwards D, et al. 2012. Capturing the biofuel wellhead and powerhouse: the chloroplast and mitochondrial genomes of the leguminous feedstock tree Pongamia pinnata. PLoS One 7: e51687.
35. Kim KJ, Choi KS, Jansen RK. 2005. Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Molecular Biology and Evolution 22: 1783-1792.
36. Kimura M. 1977. Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267: 275-276.
37. Kimura M. 1980. Asimple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111-120.
38. Krumsiek J, Arnold R, Rattei T. 2007. Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23: 1026-1028.
39. Krzywinski M, Schein J, Birol I, et al. 2009. Circos: an information aesthetic for comparative genomics. Genome Research 19: 1639-1645.
40. Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R. 2001. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Reasearch 29: 4633-4642.
41. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25.
42. Lavin M, Doyle JJ, Palmer JD. 1990. Evolutionarysignificance of the loss of the chloroplast -DNA inverted repeat in the Leguminosae subfamily Papilionoideae. Evolution 44: 390-402.
43. Lee 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: 1161-1180.
44. Lewis G, Schrire B, MacKinder B, Lock M. 2005. Legumes of the world. London, Royal Botanical Gardens, Kew.
45. Magee AM, Aspinall S, Rice DW, et al. 2010. Localized hypermutation and associated gene losses in legume chloroplast genomes. Genome Research 20: 1700-1710.
46. Magni C, Sessa F, Accardo E, et al. 2004. Conglutin gamma, a lupin seed protein, binds insulin in vitro and reduces plasma glucose levels of hyperglycemic rats. Journal of Nutritional Biochemistry 15: 646-650.
47. Mahé F, Markova D, Pasquet R, Misset MT, Ainouche A. 2011a. Isolation, phylogeny and evolution of the Sym RK gene in the legume genus Lupinus L. Molecular Phylogenetics and Evolution 60: 49-61.
48. Mahé F, Pascual H, Coriton O, et al. 2011b. New data and phylogenetic placement of the enigmatic old world lupin: Lupinus mariae-josephi H. Pascual. Genetic Resources and Crop Evolution 58: 101-114.
49. Maul JE, Lilly JW, Cui L, et al. 2002. The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. The Plant Cell 14: 2659-2679.
50. Maréchal A, Brisson N. 2010. Recombination and the maintenance of plant organelle genome stability. New Phytologist 186: 299-317.
51. Messier W, Stewart C-B. 1997. Episodic adaptive evolution of primate lysozymes. Nature 385: 151-154.
52. Millen RS, Olmstead RG, Adams KL, et al. 2001. Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. The Plant Cell 13: 645-658.
53. Moore MJ, Bell CD, Soltis PS, Soltis DE. 2007. Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proceedings of the National Academy of Sciences, USA 104: 19363-19368.
54. Moore MJ, Soltis PS, Bell CD, Burleigh JG, Soltis DE. 2010. Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proceedings of the National Academy of Sciences, USA 107: 4623-4628.
55. Palmer JD. 1985. Comparative organization of chloroplast genomes. Annual Review of Genetics 19: 325-354.
56. Palmer JD, Herbon LA. 1988. Plant mitochondrial-DNA evolves rapidly in structure, but slowly in sequence. Journal of Molecular Evolution 28: 87-97.
57. Palmer JD, Thompson WF. 1982. Chloroplast DNA rearrangements are more frequent when a large inverted repeat sequence is lost. Cell 29: 537-50.
58. Paradis E, Bolker B, Claude J, et al. 2011. Package 'ape'. Available at: http://cran.r-project.org/web/packages/ape/ape.pdf.
59. Perry AS, Brennan S, Murphy DJ, Kavanagh TA, Wolfe KH. 2002. Evolutionary re-organisation of a large operon in adzuki bean chloroplast DNA caused by inverted repeat movement. DNA Research 9: 157-162.
60. Pierleoni A, Martelli PL, Fariselli P, Casadio R. 2006. BaCelLo: a balanced subcellular localization predictor. Bioinformatics 22: e408-e416. (Pubitemid 44288310)
61. Pilvi TK, Jauhiainen T, Cheng ZJ, Mervaala EM, Vapaatalo H, Korpela R. 2006. Lupin protein attenuates the development of hypertension and normalises the vascular function of NaCl-loaded Goto-Kakizaki rats. Journal of Physiology and Pharmacology 57: 167-176.
62. Pombert JF, Otis C, Lemieux C, Turmel M. 2005. The chloroplast genome sequence of the green alga Pseudendocloniumakinetum(Ulvophyceae) reveals unusual structural features andnewinsights into the branchingorderofchlorophyte lineages. Molecular Biology and Evolution 22: 1903-1918.
63. Raubeson LA, Jansen RK. 2005. Chloroplast genomes of plants. Wallingford, UK: CABI Publishing.
64. Raubeson LA, Peery R, Chumley TW, et al. 2007. Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genomics 8: 174.
65. Rogalski M, Ruf S, Bock R. 2006. Tobacco plastid ribosomal protein S18 is essential for cell survival. Nucleic Acids Research 34: 4537-4545.
66. Ruf S, Kössel H, Bock R. 1997. Targeted inactivation of a tobacco intron-containing open reading frame reveals a novel chloroplast-encoded photosystem I-related gene. Journal of Cell Biology 139: 95-102.
67. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425.
68. Saski C, Lee SB, Daniell H, et al. 2005. Complete chloroplast genome sequence of Glycinemaxand comparative analyses with other legume genomes. Plant Molecular Biology 59: 309-322.
69. Small I, Peeters N, Legeai F, Lurin C. 2004. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4: 1581-1590.
70. Sprent JI. 2007. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174: 11-25.
71. Stefanovic S, Pfeil BE, Palmer JD, Doyle JJ. 2009. Relationships among phaseolid legumes based on sequences from eight chloroplast regions. Systematic Botany 34: 115-128.
72. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
73. Tangphatsornruang S, Sangsrakru D, Chanprasert J, et al. 2010. The chloroplast genome sequence of mungbean (Vigna radiata) determined by highthroughput pyrosequencing: structural organization and phylogenetic relationships. DNA Research 17: 11-22.
74. Timmis JN, Ayliffe MA, Huang CY, Martin W. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Review Genetics 5: 123-135.
75. Tsumura Y, Suyama Y, Yoshimura K. 2000. Chloroplast DNAinversion polymorphism in populations of Abies and Tsuga. Molecular Biology and Evolution 17: 1302-1312.
76. Ueda M, Fujimoto M, Arimura SI, Tsutsumi N, Kadowaki KI. 2008. Presence of a latent mitochondrial targeting signal in gene on mitochondrial genome. Molecular Biology and Evolution 25: 1791-1793.
77. Wojciechowski MF, Lavin M, Sanderson MJ. 2004. A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. American Journal of Botany 91: 1846-1862.
78. Wyman SK, Jansen RK, Boore JL. 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20: 3252-3255.
79. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24: 1586-1591.
80. Yang Z, Nielsen R. 2000. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Molecular Biology and Evolution 17: 32-43.