Whole genome and tandem duplicate retention facilitated glucosinolate pathway diversification in the mustard family

Genome Biology and Evolution

Volumn 5, Issue 11, 2013, Pages 2155-2173

  Hofberger, Johannes A ^a,b   Lyons, Eric ^c   Edger, Patrick P ^d   Chris Pires, J ^d   Eric Schranz, M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF ARIZONA   (United States)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

Brassicaceae; Comparative genomics; Functional diversification; Systems biology; Whole genome duplication

Indexed keywords

GLUCOSINOLATE;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; BRASSICACEAE; COMPARATIVE GENOMICS; FUNCTIONAL DIVERSIFICATION; GENETIC VARIABILITY; GENETICS; MOLECULAR EVOLUTION; MUSTARD; PLANT GENOME; SEQUENCE HOMOLOGY; SYNTENY; SYSTEMS BIOLOGY; TANDEM REPEAT; WHOLE-GENOME DUPLICATION;

BRASSICACEAE; COMPARATIVE GENOMICS; FUNCTIONAL DIVERSIFICATION; SYSTEMS BIOLOGY; WHOLE-GENOME DUPLICATION;

ARABIDOPSIS; EVOLUTION, MOLECULAR; GENOME, PLANT; GENOMIC STRUCTURAL VARIATION; GLUCOSINOLATES; MUSTARD PLANT; SEQUENCE HOMOLOGY; SYNTENY; TANDEM REPEAT SEQUENCES;

EID: 84892641918     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt162     Document Type: Article

References (77)

1. Bednarek P, et al. 2009. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101-106.
2. Beekwilder J, et al. 2008. The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis. PLoS One 3:e2068.
3. Bellieny-Rabelo D, Oliveira AE, Venancio TM. 2013. Impact of wholegenome and tandem duplications in the expansion and functional diversification of the F-box family in legumes (Fabaceae). PLoS One 8:e55127.
4. Bones AM, Rossiter JT. 2006. The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry 67:1053-1067.
5. Bowers JE, Chapman BA, Rong J, Paterson AH. 2003. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433-438.
6. Celenza JL, et al. 2005. The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol. 137:253-262.
7. Cheng S, et al. 2013. The Tarenaya hassleriana genome provides insight into reproductive trait and genome evolution of crucifers. Plant Cell 25:2813-2830.
8. Cheong J-J, Choi YD. 2003. Methyl jasmonate as a vital substance in plants. Trends Genet. 19:409-413.
9. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM. 2009. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95-101.
10. Couvreur TL, et al. 2010. Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol Biol Evol. 27:55-71.
11. De Bodt S, Maere S, Van de Peer Y. 2005. Genome duplication and the origin of angiosperms. Trends Ecol Evol. 20:591-597.
12. Fahey JW, Zalcmann AT, Talalay P. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5-51.
13. Fawcett JA, Maere S, 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 U S A. 106:5737-5742.
14. 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.
15. Freeling M, Thomas BC. 2006. Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 16:805-814.
16. Freeling M, et al. 2008. Many or most genes in Arabidopsis transposed after the origin of the order Brassicales. Genome Res. 18:1924-1937.
17. Gigolashvili T, Engqvist M, Yatusevich R, Muller C, Flugge UI. 2008. HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytol. 177:627-642.
18. Gigolashvili T, et al. 2007. The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 50:886-901.
19. Gigolashvili T, et al. 2009. The plastidic bile acid transporter 5 is required for the biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana. Plant Cell 21:1813-1829.
20. Guindon S, et al. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 59:307-321.
21. Hansen BG, Kliebenstein DJ, Halkier BA. 2007. Identification of a flavinmonooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J. 50:902-910.
22. Hansen BG, et al. 2008. A novel 2-oxoacid-dependent dioxygenase involved in the formation of the goiterogenic 2-hydroxybut-3-enyl glucosinolate and generalist insect resistance in Arabidopsis. Plant Physiol. 148:2096-2108.
23. Hartmann T. 2007. From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68:2831-2846.
24. Haudry A, et al. 2013. An atlas of over 90, 000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat Genet. 45:891-898.
25. Hayes JD, Kelleher MO, Eggleston IM. 2008. The cancer chemopreventive actions of phytochemicals derived from glucosinolates. Eur J Nutr. 47(2 Suppl):73-88.
26. He Y, Chen B, Pang Q, Strul JM, Chen S. 2010. Functional specification of Arabidopsis isopropylmalate isomerases in glucosinolate and leucine biosynthesis. Plant Cell Physiol. 51:1480-1487.
27. Hecht SS. 2000. Inhibition of carcinogenesis by isothiocyanates. Drug Metab Rev. 32:395-411.
28. Heidel AJ, Clauss MJ, Kroymann J, Savolainen O, Mitchell-Olds T. 2006. Natural variation in MAM within and between populations of Arabidopsis lyrata determines glucosinolate phenotype. Genetics 173:1629-1636.
29. Hirai MY, et al. 2007. Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci U S A. 104:6478-6483.
30. Huang CR, Burns KH, Boeke JD. 2012. Active transposition in genomes. Annu Rev Genet. 46:651-675.
31. Hughes AL, Friedman R, Ekollu V, Rose JR. 2003. Non-random association of transposable elements with duplicated genomic blocks in Arabidopsis thaliana. Mol Phylogenet Evol. 29:410-416.
32. Irish VF, Litt A. 2005. Flower development and evolution: gene duplication, diversification and redeployment. Curr Opin Genet Dev. 15:454-460.
33. Jiao Y, et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473:97-100.
34. Kane J, Freeling M, Lyons E. 2010. The evolution of a high copy gene array in Arabidopsis. J Mol Evol. 70:531-544.
35. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059-3066.
36. Kliebenstein DJ. 2008. A role for gene duplication and natural variation of gene expression in the evolution of metabolism. PLoS One 3:e1838.
37. Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, Mitchell-Olds T. 2001. Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:681-693.
38. Kroymann J, Donnerhacke S, Schnabelrauch D, Mitchell-Olds T. 2003. Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proc Natl Acad Sci U S A. 100(2 Suppl):14587-14592.
39. Krzywinski M, et al. 2009. Circos: an information aesthetic for comparative genomics. Genome Res. 19:1639-1645.
40. Leister D. 2004. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet. 20:116-122.
41. Li J, Hansen BG, Ober JA, Kliebenstein DJ, Halkier BA. 2008. Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol. 148:1721-1733.
42. Lyons E, Freeling M. 2008. How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J. 53:661-673.
43. Malacarne G, et al. 2012. Deconstruction of the (paleo) polyploid grapevine genome based on the analysis of transposition events involving NBS resistance genes. PLoS One 7:e29762.
44. Mithen R, Bennett R, Marquez J. 2010. Glucosinolate biochemical diversity and innovation in the Brassicales. Phytochemistry 71:2074-2086.
45. Nakajima M, Yoshida R, Shimada N, Yamazaki H, Yokoi T. 2001. Inhibition and inactivation of human cytochrome P450 isoforms by phenethyl isothiocyanate. Drug Metab Dispos. 29:1110-1113.
46. Nakano T, Suzuki K, Fujimura T, Shinshi H. 2006. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140:411-432.
47. Naur P, et al. 2003. CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol. 133:63-72.
48. Ohno S. 1970. Evolution by gene duplication. New York: Springer Publishing Group, p. 160.
49. Parniske M, et al. 1999. Homologues of the Cf-9 disease resistance gene (Hcr9s) are present at multiple loci on the short arm of tomato chromosome 1. Mol Plant Microbe Interact. 12:93-102.
50. Pfalz M, Vogel H, Kroymann J. 2009. The gene controlling the indole glucosinolate modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 21:985-999.
51. Piotrowski M, et al. 2004. Desulfoglucosinolate sulfotransferases from Arabidopsis thaliana catalyze the final step in the biosynthesis of the glucosinolate core structure. J Biol Chem. 279:50717-50725.
52. Prasad KV, et al. 2012. A gain-of-function polymorphism controlling complex traits and fitness in nature. Science 337:1081-1084.
53. Rask L, et al. 2000. Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol. 42:93-113.
54. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16:276-277.
55. Rizzon C, Ponger L, Gaut BS. 2006. Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Comput Biol. 2:e115.
56. Rodman J. 1998. Parallel evolution of glucosinolate biosynthesis inferred from congruent nuclear and plastid gene phylogenies. Am J Bot. 85:997.
57. Rodman JE, Karol KG, Price RA, Sytsma KJ. 1996. Molecules, morphology, and Dahlgren's expanded order capparales. Syst Bot. 21:289-307.
58. Roth C, et al. 2007. Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms. J Exp Zool B Mol Dev Evol. 308:58-73.
59. Sawada Y, et al. 2009. Omics-based approaches to methionine side chain elongation in Arabidopsis: characterization of the genes encoding methylthioalkylmalate isomerase and methylthioalkylmalate dehydrogenase. Plant Cell Physiol. 50:1181-1190.
60. Schranz ME, Edger PP, Pires JC, van Dam NM, Wheat CW. 2011. Comparative genomics in the Brassicales: ancient genome duplications, glucosinolate diversification and pierinae herbivore radiation. In: Edwards D, Batley J, Parkin I, Kole C, editors. Genetics, genomics and breeding in crop plants. Boca Raton (FL): CRC press. p. 206-218.
61. Schranz ME, Mohammadin S, Edger PP. 2012. Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model. Curr Opin Plant Biol. 15:147-153.
62. Sonderby IE, Geu-Flores F, Halkier BA. 2010. Biosynthesis of glucosinolates-gene discovery and beyond. Trends Plant Sci. 15:283-290.
63. Stehle F, Brandt W, Schmidt J, Milkowski C, Strack D. 2008. Activities of Arabidopsis sinapoylglucose: malate sinapoyltransferase shed light on functional diversification of serine carboxypeptidase-like acyltransferases. Phytochemistry 69:1826-1831.
64. Tang H, Lyons E. 2012. Unleashing the genome of Brassica rapa. Front Plant Sci. 3:172.
65. Textor S, de Kraker JW, Hause B, Gershenzon J, Tokuhisa JG. 2007. MAM3 catalyzes the formation of all aliphatic glucosinolate chain lengths in Arabidopsis. Plant Physiol. 144:60-71.
66. Thomas BC, Pedersen B, Freeling M. 2006. Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res. 16:934-946.
67. Vlad D, Rappaport F, Simon M, Loudet O. 2010. Gene transposition causing natural variation for growth in Arabidopsis thaliana. PLoS Genet. 6:e1000945.
68. Wang H, et al. 2011a. Glucosinolate biosynthetic genes in Brassica rapa. Gene 487:135-142.
69. Wang X, Weigel D, Smith LM. 2013. Transposon variants and their effects on gene expression in Arabidopsis. PLoS Genet. 9:e1003255.
70. Wang X, et al. 2011b. The genome of the mesopolyploid crop species Brassica rapa. Nat Genet. 43:1035-1039.
71. Wang Y, et al. 2011c. Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms. PLoS One 6:e28150.
72. Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 10:57-63.
73. Wentzell AM, et al. 2007. Linking metabolic QTLs with network and cis-eQTLs controlling biosynthetic pathways. PLoS Genet. 3:1687-1701.
74. Wicker T, Buchmann JP, Keller B. 2010. Patching gaps in plant genomes results in gene movement and erosion of colinearity. Genome Res. 20:1229-1237.
75. Windsor AJ, et al. 2005. Geographic and evolutionary diversification of glucosinolates among near relatives of Arabidopsis thaliana (Brassicaceae). Phytochemistry 66:1321-1333.
76. Wittstock U, Kliebenstein DJ, Lambrix V, Reichelt M, Gershenzon J. 2003. Glucosinolate hydrolysis and its impact on generalist and specialist insect herbivores. In: Romeo JT, editor. Integrative phytochemistry: from ethnobotany to molecular ecology. Amsterdam (The Netherlands): Elsevier. p. 101-126.
77. Woodhouse MR, Tang H, Freeling M. 2011. Different gene families in Arabidopsis thaliana transposed in different epochs and at different frequencies throughout the rosids. Plant Cell 23:4241-4253.