Gene duplications and the time thereafter - examples from plant secondary metabolism

Plant Biology

Volumn 12, Issue 4, 2010, Pages 570-577

  Ober, D ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

Bifunctionality; Gene recruitment; Neofunctionalisation; Pathway evolution; Plant secondary metabolism; Subfunctionalisation

Indexed keywords

BENZOXAZINE DERIVATIVE; PYRROLIZIDINE ALKALOID;

ALKALOID; GENETIC ANALYSIS; PHYTOCHEMISTRY; SECONDARY METABOLITE;

BIOLOGICAL MODEL; GENE DUPLICATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PLANT; REVIEW;

BENZOXAZINES; EVOLUTION, MOLECULAR; GENE DUPLICATION; MODELS, GENETIC; PLANTS; PYRROLIZIDINE ALKALOIDS;

EID: 77955935755     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2009.00317.x     Document Type: Review

References (77)

1. Abdelhady MIS, Beuerle T, Ober D. Homospermidine in transgenic tobacco results in considerably reduced spermidine levels but is not converted to pyrrolizidine alkaloid precursors. Plant Molecular Biology 2009, 71:145-155.
2. Achaz G, Netter P, Coissac E. Study of intrachromosomal duplications among the eukaryote genomes. Molecular Biology and Evolution 2001, 18:2280-2288.
3. Anke S, Niemüller D, Moll S, Hänsch R, Ober D. Polyphyletic origin of pyrrolizidine alkaloids within the Asteraceae. Evidence from differential tissue expression of homospermidine synthase. Plant Physiology 2004, 136:4037-4047.
4. Anke S, Gonde D, Kaltenegger E, Hansch R, Theuring C, Ober D. Pyrrolizidine alkaloid biosynthesis in Phalaenopsis orchids: developmental expression of alkaloid-specific homospermidine synthase in root tips and young flower buds. Plant Physiology 2008, 148:751-760.
5. Bak S, Paquette SM, Morant M, Vinther Moranth A, Saito S, Bjarnholt N, Zagrobelny M, Jorgensen K, Osmani S, Hamann T, Toft Simonsen H, Sanchez Pérez R, Bordier van Heeswijck T, Jorgensen B, Moller BL. Cyanogenic glycosides: a case study for evolution and application of cytochromes P450. Phytochemistry Reviews 2006, 5:309-329.
6. Benderoth M, Textor S, Windsor AJ, Mitchell-Olds T, Gershenzon J, Kroymann J. Positive selection driving diversification in plant secondary metabolism. Proceedings of the National Academy of Sciences USA 2006, 103:9118-9123.
7. Biastoff S, Brandt W, Dräger B. Putrescine N-methyltransferase - The start for alkaloids. Phytochemistry 2009, 70(1-16):1708-1718.
8. Bowers JE, Chapman BA, Rong J, Paterson AH. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 2003, 422:433-438.
9. Brosius J. Retroposons - seeds of evolution. Science 1991, 251:753.
10. Brosius J. The contribution of RNAs and retroposition to evolutionary novelties. Genetica 2003, 118:99-116.
11. Cannon S, Mitra A, Baumgarten A, Young N, May G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology 2004, 4:10.
12. Chen F, Ro D-K, Petri J, Gershenzon J, Bohlmann J, Pichersky E, Tholl D. Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiology 2004, 135:1956-1966.
13. DePristo MA. The subtle benefits of being promiscuous: adaptive evolution potentiated by enzyme promiscuity. HFSP Journal 2007, 1:94-98.
14. Drouin G, Dover GA. A plant processed pseudogene. Nature 1987, 328:557-558.
15. Durbin ML, McCaig B, Clegg MT. Molecular evolution of the chalcone synthase multigene family in the morning glory genome. Plant Molecular Biology 2000, 42:79-92.
16. Force A, Lynch M, Pickett FB, Amores A, Yan Y-l, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545.
17. Frey M, Chomet P, Glawischnig E, Stettner C, Gruen S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A. Analysis of a chemical plant defense mechanism in grasses. Science 1997, 277:696-699.
18. Frey M, Stettner C, Pare PW, Schmelz EA, Tumlinson JH, Gierl A. An herbivore elicitor activates the gene for indole emission in maize. Proceedings of the National Academy of Sciences USA 2000, 97:14801-14806.
19. Frey M, Schullehner K, Dick R, Fiesselmann A, Gierl A. Benzoxazinoid biosynthesis, a model for evolution of secondary metabolic pathways in plants. Phytochemistry 2009, 70(15-16):1645-51.
20. Frölich C, Hartmann T, Ober D. Tissue distribution and biosynthesis of 1,2-saturated pyrrolizidine alkaloids in Phalaenopsis hybrids (Orchidaceae). Phytochemistry 2006, 67:1493-1502.
21. Graur D, Li W-H. Fundamentals of molecular evolution 1999, Sinauer, Sunderland, MA, USA
22. Grotewold E. Plant metabolic diversity: a regulatory perspective. Trends in Plant Science 2005, 10:57-62.
23. Gu Z, Nicolae D, Lu HHS, Li W-H. Rapid divergence in expression between duplicate genes inferred from microarray data. Trends in Genetics 2002, 18:609-613.
24. Hartmann T. Diversity and variability of plant secondary metabolism: a mechanistic view. Entomologia Experimentalis et Applicata 1996, 80:177-188.
25. Hartmann T, Ober D. Biosynthesis and metabolism of pyrrolizidine alkaloids in plants and specialized insect herbivores. Topics in current chemistry 2000, 207-244. Leeper FJ, Vederas JC. Eds, Springer, Berlin, Heidelberg, Germany, pp
26. Hartmann T, Ober D. Defense by pyrrolizidine alkaloids: developed by plants and recruited by insects. Induced plant resistance to herbivory 2008, 213-231. Schaller A, Ed, Springer Science+Business Media B.V, Berlin, Germany, pp
27. Hartmann T, Kutchan TM, Strack D. Evolution of metabolic diversity. Phytochemistry 2005, 66:1198-1199.
28. Hashimoto T, Tamaki K, Suzuki KI, Yamada Y. Molecular cloning of plant spermidine synthases. Plant and Cell Physiology 1998, 39:73-79.
29. He X, Zhang J. Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 2005, 169:1157-1164.
30. Hinman VF, Davidson EH. Evolutionary plasticity of developmental gene regulatory network architecture. Proceedings of the National Academy of Sciences USA 2007, 104:19404-19409.
31. Horowitz NH. On the evolution of biochemical syntheses. Proceedings of the National Academy of Sciences USA 1945, 31:153-157.
32. Hughes AL. The evolution of functionally novel proteins after gene duplication. Proceedings of the Royal Society of London, Series B: biological Sciences 1994, 256:119-124.
33. Hughes AL. Adaptive evolution after gene duplication. Trends in Genetics 2002, 18:433-434.
34. Hughes MK, Hughes AL. Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. Molecular Biology and Evolution 1993, 10:1360-1369.
35. Jensen RA. Enzyme recruitment in evolution of new function. Annual Review of Microbiology 1976, 30:409-425.
36. Jonczyk R, Schmidt H, Osterrieder A, Fiesselmann A, Schullehner K, Haslbeck M, Sicker D, Hofmann D, Yalpani N, Simmons C, Frey M, Gierl A. Elucidation of the final reactions of DIMBOA-glucoside biosynthesis in maize: characterization of Bx6 and Bx7. Plant Physiology 2008, 146:1053-1063.
37. Jones CG, Firn RD. On the evolution of plant secondary chemical diversity. Philosophical Transactions of the Royal Society of London B Biological Sciences 1991, 333:273-280.
38. Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, Mitchell-Olds T. Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 2001, 13:681-693.
39. Kliebenstein DJ, Kroymann J, Mitchell-Olds T. The glucosinolate-myrosinase system in an ecological and evolutionary context. Current Opinion in Plant Biology 2005, 8:264-271.
40. Kriechbaumer V, Weigang L, Fiesselmann A, Letzel T, Frey M, Gierl A, Glawischnig E. Characterisation of the tryptophan synthase alpha subunit in maize. BMC Plant Biology 2008, 8:44.
41. Long M, Betran E, Thornton K, Wang W. The origin of new genes: glimpses from the young and old. Nature Reviews Genetics 2003, 4:865-875.
42. Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science 2000, 290:1151-1155.
43. Lynch M, Conery JS. The evolutionary demography of duplicate genes. Journal of Structural and Functional Genomics 2003, 3:35-44.
44. Lynch M, Force A. The probability of duplicate gene preservation by subfunctionalization. Genetics 2000, 154:459-473.
45. Mayr E. This is biology 1997, Belknap Press, Cambridge, MA
46. Mighell AJ, Smith NR, Robinson PA, Markham AF. Vertebrate pseudogenes. FEBS Letters 2000, 468:109-114.
47. Miles EW. Tryptophan synthase: a multienzyme complex with an intramolecular tunnel. Chemical Record 2001, 1:140-151.
48. Moll S, Anke S, Kahmann U, Hänsch R, Hartmann T, Ober D. Cell-specific expression of homospermidine synthase, the entry enzyme of the pyrrolizidine alkaloid pathway in Senecio vernalis, in comparison with its ancestor, deoxyhypusine synthase. Plant Physiology 2002, 130:47-57.
49. Niemeyer HM. Hydroxamic acids (4-hydroxy-1,4benzoxazin-3-ones), defence chemicals in the Gramineae. Phytochemistry 1988, 27:3349-3358.
50. Nurhayati N, Gondé D, Ober D. Evolution of pyrrolizidine alkaloids in Phalaenopsis orchids and other monocotyledons: identification of deoxyhypusine synthase, homospermidine synthase and related pseudogenes. Phytochemistry 2009, 70:508-516.
51. Ober D. Seeing double: gene duplication and diversification in plant secondary metabolism. Trends in Plant Science 2005, 10:444-449.
52. Ober D, Hartmann T. Homospermidine synthase, the first pathway-specific enzyme of pyrrolizidine alkaloid biosynthesis, evolved from deoxyhypusine synthase. Proceedings of the National Academy of Sciences USA 1999a, 96:14777-14782.
53. Ober D, Hartmann T. Deoxyhypusine synthase from tobacco: cDNA isolation, characterization, and bacterial expression of an enzyme with extended substrate specificity. Journal of Biological Chemistry 1999b, 274:32040-32047.
54. Ober D, Hartmann T. Phylogenetic origin of a secondary pathway: the case of pyrrolizidine alkaloids. Plant Molecular Biology 2000, 44:445-450.
55. Ober D, Kaltenegger E. Pyrrolizidine alkaloid biosynthesis, evolution of a pathway in plant secondary metabolism. Phytochemistry 2009, 70:1687-1695.
56. Ober D, Harms R, Witte L, Hartmann T. Molecular evolution by change of function: alkaloid-specific homospermidine synthase retained all properties of deoxyhypusine synthase except binding the eIF5A precursor protein. Journal of Biological Chemistry 2003, 278:12805-12812.
57. Ohno S. Evolution by gene duplication 1970, Springer, Berlin, Germany
58. Ohno S. Ancient linkage groups and frozen accidents. Nature 1973, 244:259-262.
59. Parker HG, VonHoldt BM, Quignon P, Margulies EH, Shao S, Mosher DS, Spady TC, Elkahloun A, Cargill M, Jones PG, Maslen CL, Acland GM, Sutter NB, Kuroki K, Bustamante CD, Wayne RK, Ostrander EA. An expressed Fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science 2009, 325:995-998.
60. Pichersky E, Gang DR. Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. Trends in Plant Science 2000, 5:439-445.
61. Reimann A, Nurhayati N, Backenköhler A, Ober D. Repeated evolution of the pyrrolizidine alkaloid-mediated defense system in separate angiosperm lineages. Plant Cell 2004, 16:2772-2784.
62. Rodin SN, Riggs AD. Epigenetic silencing may aid evolution by gene duplication. Journal of Molecular Evolution 2003, 56:718-729.
63. Rogers J. Retroposons defined. Nature 1983, 301:460.
64. Roth C, Rastogi S, Arvestad L, Dittmar K, Light S, Ekman D, Liberles DA. Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms. Journal of Experimental Zoology. Part B. Molecular and Developmental Evolution 2007, 308:58-73.
65. Schuster J, Knill T, Reichelt M, Gershenzon J, Binder S. BRANCHED-CHAIN AMINOTRANSFERASE4 is part of the chain elongation pathway in the biosynthesis of methionine-derived glucosinolates in Arabidopsis. The Plant Cell 2006, 18:2664-2679.
66. Sicker D, Frey M, Schulz M, Gierl A. Role of natural benzoxazinones in the survival strategy of plants. International Review of Cytology 2000, 198:319-346.
67. Simillion C, Vandepoele K, Van Montagu MC, Zabeau M, Van De Peer Y. The hidden duplication past of Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA 2002, 99:13627-13632.
68. Soltis PS. Ancient and recent polyploidy in angiosperms. New Phytologist 2005, 166:5-8.
69. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-815.
70. Tholl D. Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Current Opinion in Plant Biology 2006, 9:297-304.
71. Vanin EF. Processed pseudogenes: characteristics and evolution. Annual Review of Genetics 1985, 19:253-272.
72. Vision TJ, Brown DG, Tanksley SD. The origins of genomic duplications in Arabidopsis. Science 2000, 290:2114-2117.
73. Wang W, Zheng H, Fan C, Li J, Shi J, Cai Z, Zhang G, Liu D, Zhang J, Vang S, Lu Z, Wong GK-S, Long M, Wang J. High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell 2006, 18:1791-1802.
74. Wapinski I, Pfeffer A, Friedman N, Regev A. Natural history and evolutionary principles of gene duplication in fungi. Nature 2007, 449:54-61.
75. Zhang J. Evolution by gene duplication: an update. Trends in Ecology and Evolution 2003, 18:292-298.
76. Zhang Y, Wu Y, Liu Y, Han B. Computational identification of 69 retroposons in Arabidopsis. Plant Physiology 2005, 138:935-948.
77. Zimmer EA, Martin SL, Beverley SM, Kan YW, Wilson AC. Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Proceedings of the National Academy of Sciences USA 1980, 77:2158-2162.