Repeated whole-genome duplication, karyotype reshuffling, and biased retention of stress-responding genes in buckler mustard

Plant Cell

Volumn 28, Issue 1, 2016, Pages 17-27

  Geiser, Céline ^a   Mandáková, Terezie ^b   Arrigo, Nils ^c   Lysak, Martin A ^b   Parisod, Christian ^a  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^b MASARYK UNIVERSITY   (Czech Republic)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

BIOLOGICAL MODEL; FLUORESCENCE; GENE DUPLICATION; GENE ONTOLOGY; GENETIC SELECTION; GENETICS; KARYOTYPE; MUSTARD; PHYSIOLOGICAL STRESS; PLANT GENE;

FLUORESCENCE; GENE DUPLICATION; GENE ONTOLOGY; GENES, PLANT; KARYOTYPE; MODELS, GENETIC; MUSTARD PLANT; SELECTION, GENETIC; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84957837182     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.15.00791     Document Type: Article

References (75)

1. Al-Shahrour, F., Díaz-Uriarte, R., and Dopazo, J. (2004). FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20: 578-580.
2. Arrigo, N., and Barker, M.S. (2012). Rarely successful polyploids and their legacy in plant genomes. Curr. Opin. Plant Biol. 15: 140-146.
3. Babst-Kostecka, A.A., Parisod, C., Godé, C., Vollenweider, P., and Pauwels, M. (2014). Patterns of genetic divergence among populations of the pseudometallophyte Biscutella laevigata from southern Poland. Plant Soil 383: 245-256.
4. Bardil, A., Tayalé, A., and Parisod, C. (2015). Evolutionary dynamics of retrotransposons following autopolyploidy in the Buckler Mustard species complex. Plant J. 82: 621-631.
5. 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.
6. Benaglia, T., Chauveau, D., Hunter, D.R., and Young, D.S. (2009). mixtools: An R package for analyzing finite mixture models. J. Stat. Softw. 32: 1-29.
7. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate-a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289-300.
8. Birchler, J.A., and Veitia, R.A. (2012). Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc. Natl. Acad. Sci. USA 109: 14746-14753.
9. 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.
10. Blondel, J., Aronson, J., Bodiou, J.-Y., and Boeuf, G. (2010). The Mediterranean Region: Biological Diversity in Space and Time. (Oxford, UK: Oxford University Press).
11. 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.
12. Burgess, A., Vigneron, S., Brioudes, E., Labbé, J.-C., Lorca, T., and Castro, A. (2010). Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/ PP2A balance. Proc. Natl. Acad. Sci. USA 107: 12564-12569.
13. Chalhoub, B., et al. (2014). Plant genetics. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345: 950-953.
14. Chao, D.-Y., Dilkes, B., Luo, H., Douglas, A., Yakubova, E., Lahner, B., and Salt, D.E. (2013). Polyploids exhibit higher potassium up-take and salinity tolerance in Arabidopsis. Science 341: 658-659.
15. Chevreux, B., Pfisterer, T., Drescher, B., Driesel, A.J., Müller, W.E.G., Wetter, T., and Suhai, S. (2004). Using the miraEST as-sembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 14: 1147-1159.
16. Conant, G.C., Birchler, J.A., and Pires, J.C. (2014). Dosage, duplication, and diploidization: clarifying the interplay of multiple models for duplicate gene evolution over time. Curr. Opin. Plant Biol. 19: 91-98.
17. Couvreur, T.L.P., Franzke, A., Al-Shehbaz, I.A., Bakker, F.T., Koch, M.A., and Mummenhoff, K. (2010). Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol. Biol. Evol. 27: 55-71.
18. De Smet, R., Adams, K.L., Vandepoele, K., Van Montagu, M.C.E., Maere, S., and Van de Peer, Y. (2013). Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants. Proc. Natl. Acad. Sci. USA 110: 2898-2903.
19. Doyle, J.J., Flagel, L.E., Paterson, A.H., Rapp, R.A., Soltis, D.E., Soltis, P.S., and Wendel, J.F. (2008). Evolutionary genetics of genome merger and doubling in plants. Annu. Rev. Genet. 42: 443-461.
20. Edger, P.P., et al. (2015). The butterfly plant arms-race escalated by gene and genome duplications. Proc. Natl. Acad. Sci. USA 112: 8362-8366.
21. Favarger, C. (1971). Relations entre la flore méditerranéenne et celle des enclaves à végétation subméditerranéenne d’Europe centrale. Boissiera 19: 149-168.
22. 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.
23. Flagel, L.E., and Wendel, J.F. (2009). Gene duplication and evolutionary novelty in plants. New Phytol. 183: 557-564.
24. 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.
25. Freeling, M., Woodhouse, M.R., Subramaniam, S., Turco, G., Lisch, D., and Schnable, J.C. (2012). Fractionation mutagenesis and similar consequences of mechanisms removing dispensable or less-expressed DNA in plants. Curr. Opin. Plant Biol. 15: 131-139.
26. Garsmeur, O., Schnable, J.C., Almeida, A., Jourda, C., D’Hont, A., and Freeling, M. (2014). Two evolutionarily distinct classes of paleopolyploidy. Mol. Biol. Evol. 31: 448-454.
27. Gasser, M. (1986). Genetic-ecological investigations in Biscutella laevigata L. Veröff. Geobot. Inst. ETH. 86: 7-86.
28. Hazel, J., Krutkramelis, K., Mooney, P., Tomschik, M., Gerow, K., Oakey, J., and Gatlin, J.C. (2013). Changes in cytoplasmic volume are sufficient to drive spindle scaling. Science 342: 853-856.
29. Hohmann, N., Wolf, E.M., Lysak, M.A., and Koch, M.A. (2015). A time-calibrated road map of Brassicaceae species radiation and evolutionary history. Plant Cell 27: 2770-2784.
30. Innan, H., and Kondrashov, F. (2010). The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11: 97-108.
31. Jalas, J., Suominen, J., and Lampinen, R. (1996). Atlas Florae Europaeae. (Helsinki, Finland: The Academic Bookstore).
32. Jiao, Y., et al. (2011). Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
33. Kagale, S., Robinson, S.J., Nixon, J., Xiao, R., Huebert, T., Condie, J., Kessler, D., Clarke, W.E., Edger, P.P., Links, M.G., Sharpe, A.G., and Parkin, I.A.P. (2014). Polyploid evolution of the Brassicaceae during the Cenozoic era. Plant Cell 26: 2777-2791.
34. Kocsis, E., Trus, B.L., Steer, C.J., Bisher, M.E., and Steven, A.C. (1991). Image averaging of flexible fibrous macromolecules: the clathrin triskelion has an elastic proximal segment. J. Struct. Biol. 107: 6-14.
35. Körner, C. (2003). Alpine Plant Life. (Heidelberg, Germany: Springer Verlag).
36. Lamesch, P., et al. (2012). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40: D1202-D1210.
37. Lim, K.Y., Kovarik, A., Matyasek, R., Chase, M.W., Clarkson, J.J., Grandbastien, M.A., and Leitch, A.R. (2007). Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol. 175: 756-763.
38. Lynch, M., and Conery, J.S. (2000). The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
39. Lysak, M.A., and Koch, M.A. (2011). Phylogeny, genome, and kar-yotype evolution of Crucifers (Brassicaceae). In Genetics and Genomics of the Brassicaceae, R. Schmidt and I. Bancroft, eds (New York: Springer-Verlag), pp 31.
40. 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.
41. Mandáková, T., Joly, S., Krzywinski, M., Mummenhoff, K., and Lysak, M.A. (2010). Fast diploidization in close mesopolyploid relatives of Arabidopsis. Plant Cell 22: 2277-2290.
42. Mandáková, T., and Lysak, M.A. (2008). Chromosomal phylogeny and karyotype evolution in x=7 crucifer species (Brassicaceae). Plant Cell 20: 2559-2570.
43. Manton, I. (1937). The problem of Biscutella laevigata L. II. The evidence from meiosis. Ann. Bot. (Lond.) 51: 439-465.
44. McGrath, C.L., and Lynch, M. (2012). Evolutionary significance of whole-genome duplication. In Polyploidy and Genome Evolution, P.S. Soltis and D.E. Soltis, eds (Berlin, Heidelberg, Germany: Springer-Verlag), pp 20.
45. Nei, M. (2013). Mutation-Driven Evolution. (Oxford, UK: Oxford University Press).
46. Ohno, S. (1970). Evolution by Gene Duplication. (Berlin, Germany: Springer).
47. Olowokudejo, J.D. (1986). The infrageneric classification of Biscutella (Cruciferae). Brittonia 38: 86-88.
48. Parisod, C., and Besnard, G. (2007). Glacial in situ survival in the Western Alps and polytopic autopolyploidy in Biscutella laevigata L. (Brassicaceae). Mol. Ecol. 16: 2755-2767.
49. Parisod, C., and Christin, P.A. (2008). Genome-wide association to fine-scale ecological heterogeneity within a continuous population of Biscutella laevigata (Brassicaceae). New Phytol. 178: 436-447.
50. Parisod, C., Holderegger, R., and Brochmann, C. (2010). Evolutionary consequences of autopolyploidy. New Phytol. 186: 5-17.
51. Potapova, T.A., Sivakumar, S., Flynn, J.N., Li, R., and Gorbsky, G.J. (2011). Mitotic progression becomes irreversible in prometaphase and collapses when Wee1 and Cdc25 are inhibited. Mol. Biol. Cell 22: 1191-1206.
52. Price, M.N., Dehal, P.S., and Arkin, A.P. (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26: 1641-1650.
53. Primmer, C.R., Papakostas, S., Leder, E.H., Davis, M.J., and Ragan, M.A. (2013). Annotated genes and nonannotated genomes: cross-species use of Gene Ontology in ecology and evolution research. Mol. Ecol. 22: 3216-3241.
54. Ramsey, J., and Schemske, D.W. (2002). Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33: 589-639.
55. Ranwez, V., Harispe, S., Delsuc, F., and Douzery, E.J.P. (2011). MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS One 6: e22594.
56. Schmieder, R., and Edwards, R. (2011). Quality control and pre-processing of metagenomic datasets. Bioinformatics 27: 863-864.
57. Schönfelder, P. (1968). Chromozomenzahlen einiger Arten des Gattung Biscutella L. Österreichische Botanische Zeitschrift 115: 363-371.
58. Schranz, M.E., Lysak, M.A., and Mitchell-Olds, T. (2006). The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci. 11: 535-542.
59. Schranz, M.E., Mohammadin, S., and Edger, P.P. (2012). Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model. Curr. Opin. Plant Biol. 15: 147-153.
60. Slater, G.S., and Birney, E. (2005). Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6: 31.
61. Soltis, D.E., Segovia-Salcedo, M.C., Jordon-Thaden, I., Majure, L., Miles, N.M., Mavrodiev, E.V., Mei, W., Cortez, M.B., Soltis, P.S., and Gitzendanner, M.A. (2014). Are polyploids really evolutionary dead-ends (again)? A critical reappraisal of Mayrose et al. New Phytol. 202: 1105-1117.
62. Tang, H., Woodhouse, M.R., Cheng, F., Schnable, J.C., Pedersen, B.S., Conant, G., Wang, X., Freeling, M., and Pires, J.C. (2012). Altered patterns of fractionation and exon deletions in Brassica rapa support a two-step model of paleohexaploidy. Genetics 190: 1563-1574.
63. Tank, D.C., Eastman, J.M., Pennell, M.W., Soltis, P.S., Soltis, D.E., Hinchliff, C.E., Brown, J.W., Sessa, E.B., and Harmon, L.J. (2015). Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytol. 207: 454-467.
64. Tayalé, A., and Parisod, C. (2013). Natural pathways to polyploidy in plants and consequences for genome reorganization. Cytogenet. Genome Res. 140: 79-96.
65. Tremetsberger, K., Konig, C., Samuel, R., Pinsker, W., and Stuessy, T.F. (2002). Infraspecific genetic variation in Biscutella laevigata (Brassicaceae): new focus on Irene Manton’s hypothesis. Plant Syst. Evol. 233: 163-181.
66. Van de Peer, Y., Maere, S., and Meyer, A. (2009). The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10: 725-732.
67. Vanneste, K., Baele, G., Maere, S., and Van de Peer, Y. (2014b). Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res. 24: 1334-1347.
68. Vanneste, K., Maere, S., and Van de Peer, Y. (2014a). Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369: 20130353.
69. Vanneste, K., Van de Peer, Y., and Maere, S. (2013). Inference of genome duplications from age distributions revisited. Mol. Biol. Evol. 30: 177-190.
70. Veitia, R.A., Bottani, S., and Birchler, J.A. (2013). Gene dosage effects: nonlinearities, genetic interactions, and dosage compensation. Trends Genet. 29: 385-393.
71. Wagner, A. (2011). The Origins of Evolutionary Innovations. (Oxford, UK: Oxford University Press).
72. Wolfe, K.H. (2001). Yesterday’s polyploids and the mystery of diploidization. Nat. Rev. Genet. 2: 333-341.
73. Wood, T.E., Takebayashi, N., Barker, M.S., Mayrose, I., Greenspoon, P.B., and Rieseberg, L.H. (2009). The frequency of polyploid speciation in vascular plants. Proc. Natl. Acad. Sci. USA 106: 13875-13879.
74. Woodhouse, M.R., Cheng, F., Pires, J.C., Lisch, D., Freeling, M., and Wang, X. (2014). Origin, inheritance, and gene regulatory consequences of genome dominance in polyploids. Proc. Natl. Acad. Sci. USA 111: 5283-5288.
75. Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likeli-hood. Mol. Biol. Evol. 24: 1586-1591.