Integrated syntenic and phylogenomic analyses reveal an ancient genome duplication in monocots

Plant Cell

Volumn 26, Issue 7, 2014, Pages 2792-2802

  Jiao, Yuannian ^a   Li, Jingping ^a   Tang, Haibao ^b,c   Paterson, Andrew H ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^c J CRAIG VENTER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOSPERM; DNA SEQUENCE; GENE DUPLICATION; GENETICS; GENOMICS; MOLECULAR EVOLUTION; PHYLOGENY; PLANT GENOME; POLYPLOIDY; SEQUENCE ALIGNMENT; SYNTENY;

ANGIOSPERMS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOME, PLANT; GENOMICS; PHYLOGENY; POLYPLOIDY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SYNTENY;

EID: 84907351551     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.127597     Document Type: Article

References (72)

1. Adams, K.L., and Wendel, J.F. (2005). Polyploidy and genome evolution in plants. Curr. Opin. Plant Biol. 8: 135-141.
2. Al-Mssallem, I.S., Hu, S., Zhang, X., Lin, Q., Liu, W., Tan, J., Yu, X., Liu, J., Pan, L., Zhang, T., Yin, Y., and Xin, C., et al. (2013). Genome sequence of the date palm Phoenix dactylifera L. Nat. Commun. 4: 2274.
3. Amborella Genome Project (2013). The Amborella genome and the evolution of flowering plants. Science 342: 1241089.
4. Arrigo, N., and Barker, M.S. (2012). Rarely successful polyploids and their legacy in plant genomes. Curr. Opin. Plant Biol. 15: 140-146.
5. Aury, J.M., et al. (2006). Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444: 171-178.
6. Barker, M.S., Vogel, H., and Schranz, M.E. (2009). Paleopolyploidy in the Brassicales: analyses of the Cleome transcriptome elucidate the history of genome duplications in Arabidopsis and other Brassicales. Genome Biol. Evol. 1: 391-399.
7. Bennetzen, J.L., et al. (2012). Reference genome sequence of the model plant Setaria. Nat. Biotechnol. 30: 555-561.
8. Blanc, G., and Wolfe, K.H. (2004). Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16: 1667-1678.
9. Bonierbale, M.W., Plaisted, R.L., and Tanksley, S.D. (1988). RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120: 1095-1103.
10. Bowers, J.E., Chapman, B.A., Rong, J., and Paterson, A.H. (2003). Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.
11. Capella-Gutiérrez, S., Silla-Martínez, J.M., and Gabaldón, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
12. Christoffels, A., Koh, E.G.L., Chia, J.M., Brenner, S., Aparicio, S., and Venkatesh, B. (2004). Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Mol. Biol. Evol. 21: 1146-1151.
13. Cui, L., et al. (2006). Widespread genome duplications throughout the history of flowering plants. Genome Res. 16: 738-749.
14. Dehal, P., and Boore, J.L. (2005). Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3: e314.
15. D'Hont, A., et al. (2012). The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488: 213-217.
16. Fawcett, J.A., Maere, S., and Van de Peer, Y. (2009). Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc. Natl. Acad. Sci. USA 106: 5737-5742.
17. Fitch, W.M., and Margoliash, E. (1967). Construction of phylogenetic trees. Science 155: 279-284.
18. Freeling, M. (2009). Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 60: 433-453.
19. Freeling, M., and Thomas, B.C. (2006). Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 16: 805-814.
20. Gaut, B., Yang, L., Takuno, S., and Eguiarte, L.E. (2011). The patterns and causes of variation in plant nucleotide substitution rates. Annu. Rev. Ecol. Evol. Syst. 42: 245-266.
21. Grant, D., Cregan, P., and Shoemaker, R.C. (2000). Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc. Natl. Acad. Sci. USA 97: 4168-4173.
22. Haas, B.J., Delcher, A.L., Wortman, J.R., and Salzberg, S.L. (2004). DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics 20: 3643-3646.
23. Harris, R.S. (2007). Improved Pairwise Alignment of Genomic DNA. PhD dissertation (The Pennsylvania State University).
24. Hedges, S.B., Dudley, J., and Kumar, S. (2006). TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22: 2971-2972.
25. International Brachypodium Initiative (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463: 763-768.
26. Jaillon, O., et al.; French-Italian Public Consortium for Grapevine Genome Characterization (2007). The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467.
27. Jaillon, O., et al. (2004). Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946-957.
28. Jiao, Y., et al. (2011). Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
29. Jiao, Y., et al. (2012). A genome triplication associated with early diversification of the core eudicots. Genome Biol. 13: R3.
30. Katoh, K., Kuma, K., Toh, H., and Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33: 511-518.
31. Kellis, M., Birren, B.W., and Lander, E.S. (2004). Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624.
32. Kowalski, S.P., Lan, T.H., Feldmann, K.A., and Paterson, A.H. (1994). Comparative mapping of Arabidopsis thaliana and Brassica oleracea chromosomes reveals islands of conserved organization. Genetics 138: 499-510.
33. Ku, H.M., Vision, T., Liu, J., and Tanksley, S.D. (2000). Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. Proc. Natl. Acad. Sci. USA 97: 9121-9126.
34. Larkin, M.A., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
35. Li, L., and Stoeckert, C.J., Jr., and Roos, D.S. (2003). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13: 2178-2189.
36. Lynch, M., and Conery, J.S. (2000). The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
37. Maere, S., De Bodt, S., Raes, J., Casneuf, T., Van Montagu, M., Kuiper, M., and Van de Peer, Y. (2005). Modeling gene and genome duplications in eukaryotes. Proc. Natl. Acad. Sci. USA 102: 5454-5459.
38. Mayrose, I., Zhan, S.H., Rothfels, C.J., Magnuson-Ford, K., Barker, M.S., Rieseberg, L.H., and Otto, S.P. (2011). Recently formed polyploid plants diversify at lower rates. Science 333: 1257.
39. Ming, R., et al. (2013). Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.). Genome Biol. 14: R41.
40. Ming, R., et al. (2008). The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452: 991-996.
41. Mower, J.P., Touzet, P., Gummow, J.S., Delph, L.F., and Palmer, J.D. (2007). Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants. BMC Evol. Biol. 7: 135.
42. Nei, M., and Gojobori, T. (1986). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3: 418-426.
43. Ohno, S. (1970). Evolution by Gene Duplication. (Berlin: Springer).
44. Otto, S.P., and Whitton, J. (2000). Polyploid incidence and evolution. Annu. Rev. Genet. 34: 401-437.
45. Paterson, A.H., et al. (1996). Toward a unified genetic map of higher plants, transcending the monocot-dicot divergence. Nat. Genet. 14: 380-382.
46. Paterson, A.H., Bowers, J.E., and Chapman, B.A. (2004). Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc. Natl. Acad. Sci. USA 101: 9903-9908.
47. Paterson, A.H., Freeling, M., Tang, H., and Wang, X. (2010). Insights from the comparison of plant genome sequences. Annu. Rev. Plant Biol. 61: 349-372.
48. Paterson, A.H., Chapman, B.A., Kissinger, J.C., Bowers, J.E., Feltus, F.A., and Estill, J.C. (2006). Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet. 22: 597-602.
49. Paterson, A.H., et al. (2009). The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551-556.
50. Prasad, V., Strömberg, C.A., Alimohammadian, H., and Sahni, A. (2005). Dinosaur coprolites and the early evolution of grasses and grazers. Science 310: 1177-1180.
51. Putnam, N.H., et al. (2008). The amphioxus genome and the evolution of the chordate karyotype. Nature 453: 1064-1071.
52. Schnable, P.S., et al. (2009). The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115.
53. Singh, R., et al. (2013). Oil palm genome sequence reveals divergence of interfertile species in old and new worlds. Nature 500: 335-339.
54. Smith, S.A., and Donoghue, M.J. (2008). Rates of molecular evolution are linked to life history in flowering plants. Science 322: 86-89.
55. Soltis, D.E., Albert, V.A., Leebens-Mack, J., Bell, C.D., Paterson, A.H., Zheng, C., Sankoff, D., Depamphilis, C.W., Wall, P.K., and Soltis, P.S. (2009). Polyploidy and angiosperm diversification. Am. J. Bot. 96: 336-348.
56. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
57. Suyama, M., Torrents, D., and Bork, P. (2006). PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34: W609-W612.
58. Tang, H., Bowers, J.E., Wang, X., and Paterson, A.H. (2010). Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc. Natl. Acad. Sci. USA 107: 472-477.
59. Tang, H., Bowers, J.E., Wang, X., Ming, R., Alam, M., and Paterson, A.H. (2008a). Synteny and collinearity in plant genomes. Science 320: 486-488.
60. Tang, H., Wang, X., Bowers, J.E., Ming, R., Alam, M., and Paterson, A.H. (2008b). Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res. 18: 1944-1954.
61. The Angiosperm Phylogeny Group (2009). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161: 105-121.
62. Van de Peer, Y. (2011). A mystery unveiled. Genome Biol. 12: 113.
63. Van de Peer, Y., Maere, S., and Meyer, A. (2009). The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10: 725-732.
64. Vandepoele, K., Saeys, Y., Simillion, C., Raes, J., and Van De Peer, Y. (2002). The automatic detection of homologous regions (ADHoRe) and its application to microcolinearity between Arabidopsis and rice. Genome Res. 12: 1792-1801.
65. Vision, T.J., Brown, D.G., and Tanksley, S.D. (2000). The origins of genomic duplications in Arabidopsis. Science 290: 2114-2117.
66. Wang, X., Shi, X., Hao, B., Ge, S., and Luo, J. (2005). Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol. 165: 937-946.
67. Wang, X., et al.; Brassica rapa Genome Sequencing Project Consortium (2011). The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43: 1035-1039.
68. Wang, Y., Tang, H., Debarry, J.D., Tan, X., Li, J., Wang, X., Lee, T.H., Jin, H., Marler, B., Guo, H., Kissinger, J.C., and Paterson, A.H. (2012). MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40: e49.
69. Wolfe, K.H., Li, W.H., and Sharp, P.M. (1987). Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 84: 9054-9058.
70. Yang, Z. (1997). PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13: 555-556.
71. Zhang, L., Vision, T.J., and Gaut, B.S. (2002). Patterns of nucleotide substitution among simultaneously duplicated gene pairs in Arabidopsis thaliana. Mol. Biol. Evol. 19: 1464-1473.
72. Zheng, C., Chen, E., Albert, V.A., Lyons, E., and Sankoff, D. (2013). Ancient eudicot hexaploidy meets ancestral eurosid gene order. BMC Genomics 14 (suppl. 7): S3.