Large-scale evolutionary analysis of genes and supergene clusters from terpenoid modular pathways provides insights into metabolic diversification in flowering plants

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Hofberger, Johannes A ^a,b   Ramirez, Aldana M ^c   Van Den Bergh, Erik ^a   Zhu, Xinguang ^b   Bouwmeester, Harro J ^a   Schuurink, Robert C ^c   Schranz, M Eric ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b MAX PLANCK INSTITUTE   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DIMETHYLALLYLTRANSFERASE; ISOPENTENYL DIPHOSPHATE DELTA ISOMERASE; ISOPRENOID; METHYLERYTHRITOL; MEVALONIC ACID; POLYOL; SYNTHETASE; TERPENE SYNTHASE; TERPENOID; TRITERPENE SYNTHASE; UNCLASSIFIED DRUG; ISOENZYME; ISOMERASE; ISOPENTENYLDIPHOSPHATE DELTA-ISOMERASE; PLANT PROTEIN; TERPENE; TRANSFERASE;

ANGIOSPERM; ARTICLE; BIOINFORMATICS; BIOSYNTHESIS; CONTROLLED STUDY; GENE; GENE CLUSTER; GENE DUPLICATION; HIDDEN MARKOV MODEL; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NONHUMAN; PHYLOGENY; PLANT DEFENSE; PLANT ENVIRONMENT INTERACTION; PLANT GENOME; PLANT METABOLISM; PLEIOTROPY; POLLINATOR; POLYMERASE CHAIN REACTION; PROTEIN FAMILY; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SUPERGENE; SYNTENY; TRANSCRIPTOMICS; CLASSIFICATION; EVOLUTION; GENETICS; METABOLISM; METABOLOMICS; MOLECULAR GENETICS;

MAGNOLIOPHYTA;

ALKYL AND ARYL TRANSFERASES; ANGIOSPERMS; BIOLOGICAL EVOLUTION; CARBON-CARBON DOUBLE BOND ISOMERASES; DIMETHYLALLYLTRANSTRANSFERASE; GENOME, PLANT; ISOENZYMES; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MEVALONIC ACID; MOLECULAR SEQUENCE ANNOTATION; MULTIGENE FAMILY; PHYLOGENY; PLANT PROTEINS; TERPENES;

EID: 84934955600     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128808     Document Type: Article

References (149)

1. Lyons E, Freeling M (2008) How to usefully compare homologous plant genes and chromosomes as DNA sequences. The Plant Journal 53: 661-673. doi: 10.1111/j.1365-313X.2007.03326.x PMID: 18269575
2. Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics 1. Annu Rev Genet 39: 309-338. PMID: 16285863
3. Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Zool 19: 99-113. PMID: 5449325
4. Lyons E, Pedersen B, Kane J, Alam M, Ming R, Tang H, et al. (2008) Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiol 148: 1772-1781. doi: 10.1104/pp.108.124867 PMID: 18952863
5. Ohno S (1970) Evolution by gene duplication. New York: Springer Publishing Group. 160 p.
6. 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. doi: 10.1146/annurev.arplant.043008.092122 PMID: 19575588
7. Wolfe K (2000) Robustness - it's not where you think it is. Nat Genet 25: 3-4. PMID: 10802639
8. Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438. PMID: 12660784
9. Joron M, Papa R, Beltran M, Chamberlain N, Mavarez J, Baxter S, et al. (2006) A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol 4: e303. PMID: 17002517
10. Smith JM (1989) Evolutionary genetics: Oxford University Press.
11. 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. PMID: 16948529
12. 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. PMID: 11251105
13. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 20: 116-122. PMID: 15049302
14. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, et al. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100. doi: 10.1038/nature09916 PMID: 21478875
15. 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. doi: 10.1016/j.pbi.2012.03.011 PMID: 22480429
16. Haudry A, Platts AE, Vello E, Hoen DR, Leclercq M, Williamson RJ, et al. (2013) An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat Genet 45: 891-898. doi: 10.1038/ng.2684 PMID: 23817568
17. Barker MS, Vogel H, Schranz ME (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. doi: 10.1093/gbe/evp040 PMID: 20333207
18. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, et al. (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452: 991-996. doi: 10.1038/nature06856 PMID: 18432245
19. Vekemans D, Proost S, Vanneste K, Coenen H, Viaene T, Ruelens P, et al. (2012) Gamma Paleohexaploidy in the Stem Lineage of Core Eudicots: Significance for MADS-Box Gene and Species Diversification. Mol Biol Evol 29: 3793-3806. doi: 10.1093/molbev/mss183 PMID: 22821009
20. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467. PMID: 17721507
21. Tang H, Lyons E (2012) Unleashing the genome of brassica rapa. Front Plant Sci 3: 172. doi: 10.3389/fpls.2012.00172 PMID: 22866056
22. Consortium TTG (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641. doi: 10.1038/nature11119 PMID: 22660326
23. Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16: 805-814. PMID: 16818725
24. Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68: 2831-2846. PMID: 17980895
25. Hofberger JA, Lyons E, Edger PP, Pires JC, Schranz ME (2013) Whole genome and tandem duplicate retention facilitated glucosinolate pathway diversification in the mustard family. Genome Biol Evol 5: 2155-2173. doi: 10.1093/gbe/evt162 PMID: 24171911
26. Hofberger JA, Zhou B, Tang H, Jones JD, Schranz ME (2014) A novel approach for multi-domain and multi-gene family identification provides insights into evolutionary dynamics of disease resistance genes in core eudicot plants. BMC Genomics 15: 966. doi: 10.1186/1471-2164-15-966 PMID: 25380807
27. van den Bergh E, Külahoglu C, Bräutigam A, Hibberd JM, Weber AP, Zhu X-G, et al. (2014) Gene and genome duplications and the origin of C 4 photosynthesis: Birth of a trait in the Cleomaceae. Current Plant Biology 1: 2-9.
28. Phillips MA, Leon P, Boronat A, Rodriguez-Concepcion M (2008) The plastidial MEP pathway: unified nomenclature and resources. Trends Plant Sci 13: 619-623. doi: 10.1016/j.tplants.2008.09.003 PMID: 18948055
29. Aubourg S, Lecharny A, Bohlmann J (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol Genet Genomics 267: 730-745. PMID: 12207221
30. Benveniste P (2002) Sterol metabolism. Arabidopsis Book 1: e0004. doi: 10.1199/tab.0004 PMID: 22303189
31. Cheng A-X, Lou Y-G, Mao Y-B, Lu S, Wang L-J, Chen X-Y (2007) Plant Terpenoids: Biosynthesis and Ecological Functions. Journal of Integrative Plant Biology 49: 179-186.
32. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3: 408-414. PMID: 17576428
33. Boutanaev AM, Moses T, Zi J, Nelson DR, Mugford ST, Peters RJ, et al. (2015) Investigation of terpene diversification across multiple sequenced plant genomes. Proc Natl Acad Sci U S A 112: E81-88. doi: 10.1073/pnas.1419547112 PMID: 25502595
34. Matsuba Y, Nguyen TT, Wiegert K, Falara V, Gonzales-Vigil E, Leong B, et al. (2013) Evolution of a complex locus for terpene biosynthesis in solanum. Plant Cell 25: 2022-2036. doi: 10.1105/tpc.113.111013 PMID: 23757397
35. Tholl D, Lee S (2011) Terpene Specialized Metabolism in Arabidopsis thaliana. Arabidopsis Book 9: e0143. doi: 10.1199/tab.0143 PMID: 22303268
36. Phillips MA, D'Auria JC, Gershenzon J, Pichersky E (2008) The Arabidopsis thaliana type I isopentenyl diphosphate isomerases are targeted to multiple subcellular compartments and have overlapping functions in isoprenoid biosynthesis. The Plant Cell Online 20: 677-696. doi: 10.1105/tpc.107.053926 PMID: 18319397
37. Vranová E, Coman D, GruissemW(2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annual review of plant biology 64: 665-700. doi: 10.1146/annurev-arplant-050312-120116 PMID: 23451776
38. Gruchattka E, Hädicke O, Klamt S, Schütz V, Kayser O (2013) In silico profiling of Escherichia coli and Saccharomyces cerevisiae as terpenoid factories. Microbial cell factories 12: 84. doi: 10.1186/1475-2859-12-84 PMID: 24059635
39. Shack S, Gorospe M, Fawcett TW, Hudgins WR, Holbrook NJ (1999) Activation of the cholesterol pathway and Ras maturation in response to stress. Oncogene 18: 6021-6028. PMID: 10557091
40. Campos N, Rodriguez-Concepcion M, Sauret-Gueto S, Gallego F, Lois L, Boronat A (2001) Escherichia coli engineered to synthesize isopentenyl diphosphate and dimethylallyl diphosphate from mevalonate: a novel system for the genetic analysis of the 2-C-methyl-D-erythritol 4-phosphate pathway for isoprenoid biosynthesis. Biochem J 353: 59-67. PMID: 11115399
41. Johnston JB (2007) Mechanistic Investigations of Types I and II Isopentenyl Diphosphate Isomerase: ProQuest.
42. Han K-H, Kang H-S, Oh S-K, Shin D-h, Yang J-M (2001) Isopentenyl diphosphate isomerase from Hevea brasiliensis and rubber producing method using the same. Google Patents.
43. Kang JH, Gonzales-Vigil E, Matsuba Y, Pichersky E, Barry CS (2014) Determination of residues responsible for substrate and product specificity of Solanum habrochaites short-chain cis-prenyltransferases. Plant Physiol 164: 80-91. doi: 10.1104/pp.113.230466 PMID: 24254315
44. Akhtar TA, Matsuba Y, Schauvinhold I, Yu G, Lees HA, Klein SE, et al. (2013) The tomato cis-prenyltransferase gene family. Plant J 73: 640-652. doi: 10.1111/tpj.12063 PMID: 23134568
45. Oldfield E, Lin FY (2012) Terpene biosynthesis: modularity rules. Angew Chem Int Ed Engl 51: 1124-1137. doi: 10.1002/anie.201103110 PMID: 22105807
46. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci U S A 95: 4126-4133. PMID: 9539701
47. Kolesnikova MD, Wilson WK, Lynch DA, Obermeyer AC, Matsuda SPT (2007) Arabidopsis camelliol C synthase evolved from enzymes that make pentacycles. Organic letters 9: 5223-5226. PMID: 17985917
48. Shibuya M, Xiang T, Katsube Y, Otsuka M, Zhang H, Ebizuka Y (2007) Origin of structural diversity in natural triterpenes: direct synthesis of seco-triterpene skeletons by oxidosqualene cyclase. J Am Chem Soc 129: 1450-1455. PMID: 17263431
49. Lodeiro S, Xiong Q, Wilson WK, Kolesnikova MD, Onak CS, Matsuda SP (2007) An oxidosqualene cyclase makes numerous products by diverse mechanisms: a challenge to prevailing concepts of triterpene biosynthesis. J Am Chem Soc 129: 11213-11222. PMID: 17705488
50. Moses T, Pollier J, Thevelein JM, Goossens A (2013) Bioengineering of plant (tri)terpenoids: from metabolic engineering of plants to synthetic biology in vivo and in vitro. New Phytol 200: 27-43. doi: 10.1111/nph.12325 PMID: 23668256
51. Laszczyk MN (2009) Pentacyclic triterpenes of the lupane, oleanane and ursane group as tools in cancer therapy. Planta Med 75: 1549-1560. doi: 10.1055/s-0029-1186102 PMID: 19742422
52. Paetzold H, Garms S, Bartram S, Wieczorek J, Uros-Gracia EM, Rodriguez-Concepcion M, et al. (2010) The isogene 1-deoxy-D-xylulose 5-phosphate synthase 2 controls isoprenoid profiles, precursor pathway allocation, and density of tomato trichomes. Mol Plant 3: 904-916. doi: 10.1093/mp/ssq032 PMID: 20591838
53. Carretero-Paulet L, Cairo A, Talavera D, Saura A, Imperial S, Rodriguez-Concepcion M, et al. (2013) Functional and evolutionary analysis of DXL1, a non-essential gene encoding a 1-deoxy-D-xylulose 5-phosphate synthase like protein in Arabidopsis thaliana. Gene 524: 40-53. doi: 10.1016/j.gene.2012.10.071 PMID: 23154062
54. Heyndrickx KS, Vandepoele K (2012) Systematic Identification of Functional Plant Modules through the Integration of Complementary Data Sources. Plant Physiology 159: 884-901. doi: 10.1104/pp. 112.196725 PMID: 22589469
55. Tissier A (2012) Glandular trichomes: what comes after expressed sequence tags? The Plant Journal 70: 51-68. doi: 10.1111/j.1365-313X.2012.04913.x PMID: 22449043
56. Markus Lange B, Turner GW (2013) Terpenoid biosynthesis in trichomes-current status and future opportunities. Plant biotechnology journal 11: 2-22. doi: 10.1111/j.1467-7652.2012.00737.x PMID: 22979959
57. Wagner GJ, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 93: 3-11. PMID: 14678941
58. Tholl D, Chen F, Petri J, Gershenzon J, Pichersky E (2005) Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J 42: 757-771. PMID: 15918888
59. Yamaguchi S, Sun T, Kawaide H, Kamiya Y (1998) The GA2 locus of Arabidopsis thaliana encodes ent-kaurene synthase of gibberellin biosynthesis. Plant Physiol 116: 1271-1278. PMID: 9536043
60. Bohlmann J, Martin D, Oldham NJ, Gershenzon J (2000) Terpenoid Secondary Metabolism in Arabidopsis thaliana: cDNA Cloning, Characterization, and Functional Expression of a Myrcene-β-Ocimene Synthase. Archives of Biochemistry and Biophysics 375: 261-269. PMID: 10700382
61. Chen F, Tholl D, D'Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15: 481-494. PMID: 12566586
62. Chen F, Ro DK, Petri J, Gershenzon J, Bohlmann J, Pichersky E, et al. (2004) Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiol 135: 1956-1966. PMID: 15299125
63. Fäldt J, Arimura G-i, Gershenzon J, Takabayashi J, Bohlmann J (2003) Functional identification of AtTPS03 as (E)-β-ocimene synthase: a monoterpene synthase catalyzing jasmonate-and wound-induced volatile formation in Arabidopsis thaliana. Planta 216: 745-751. PMID: 12624761
64. Herde M, Gartner K, Kollner TG, Fode B, Boland W, Gershenzon J, et al. (2008) Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile C16-homoterpene TMTT. Plant Cell 20: 1152-1168. doi: 10.1105/tpc.106.049478 PMID: 18398052
65. Huang M, Abel C, Sohrabi R, Petri J, Haupt I, Cosimano J, et al. (2010) Variation of herbivore-induced volatile terpenes among Arabidopsis ecotypes depends on allelic differences and subcellular targeting of two terpene synthases, TPS02 and TPS03. Plant Physiol 153: 1293-1310. doi: 10.1104/pp.110.154864 PMID: 20463089
66. Falara V, Akhtar TA, Nguyen TT, Spyropoulou EA, Bleeker PM, Schauvinhold I, et al. (2011) The tomato terpene synthase gene family. Plant Physiol 157: 770-789. doi: 10.1104/pp.111.179648 PMID: 21813655
67. Dornelas MC, Mazzafera P (2007) A genomic approach to characterization of the Citrus terpene synthase gene family. Genetics and Molecular Biology 30: 832-840.
68. Külheim C, Yeoh SH, Maintz J, Foley WJ, Moran GF (2009) Comparative SNP diversity among four Eucalyptus species for genes from secondary metabolite biosynthetic pathways. BMC Genomics 10: 452. doi: 10.1186/1471-2164-10-452 PMID: 19775472
69. Martin DM, Aubourg S, Schouwey MB, Daviet L, Schalk M, Toub O, et al. (2010) Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol 10: 226. doi: 10.1186/1471-2229-10-226 PMID: 20964856
70. Nieuwenhuizen NJ, Green SA, Chen XY, Bailleul EJD, Matich AJ, Wang MY, et al. (2013) Functional Genomics Reveals That a Compact Terpene Synthase Gene Family Can Account for Terpene Volatile Production in Apple. Plant Physiol 161: 787-804. doi: 10.1104/pp.112.208249 PMID: 23256150
71. Amborella Genome P (2013) The Amborella genome and the evolution of flowering plants. Science 342: 1241089. doi: 10.1126/science.1241089 PMID: 24357323
72. 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. PMID: 16760422
73. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410. PMID: 2231712
74. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40: D1178-D1186. doi: 10.1093/nar/gkr944 PMID: 22110026
75. Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, et al. (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36: D1009-D1014. PMID: 17986450
76. Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, et al. (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43: 1035-1039. doi: 10.1038/ng.919 PMID: 21873998
77. Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, et al. (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45: 59-66. doi: 10.1038/ng.2472 PMID: 23179022
78. Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, et al. (2014) The genome of Eucalyptus grandis. Nature 510: 356-362. doi: 10.1038/nature13308 PMID: 24919147
79. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, et al. (2010) Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183. doi: 10.1038/nature08670 PMID: 20075913
80. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, et al. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551-556. doi: 10.1038/nature07723 PMID: 19189423
81. Xu X, Pan S, Cheng S, Zhang B, Mu D, Ni P, et al. (2011) Genome sequence and analysis of the tuber crop potato. Nature 475: 189-195. doi: 10.1038/nature10158 PMID: 21743474
82. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115. doi: 10.1126/science.1178534 PMID: 19965430
83. Cheng S, van den Bergh E, Zeng P, Zhong X, Xu J, Liu X, et al. (2013) The Tarenaya hassleriana genome provides insight into reproductive trait and genome evolution of crucifers. Plant Cell 25: 2813-2830. doi: 10.1105/tpc.113.113480 PMID: 23983221
84. Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 25: 1523-1530. doi: 10.1094/MPMI-06-12-0148-TA PMID: 22876960
85. van Bakel H, Stout JM, Cote AG, Tallon CM, Sharpe AG, Hughes TR, et al. (2011) The draft genome and transcriptome of Cannabis sativa. Genome Biol 12: R102. doi: 10.1186/gb-2011-12-10-r102 PMID: 22014239
86. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2008) GenBank. Nucleic Acids Res 36: D25-D30. PMID: 18073190
87. Tang H, Lyons E, Pedersen B, Schnable JC, Paterson AH, Freeling M (2011) Screening synteny blocks in pairwise genome comparisons through integer programming. BMC Bioinformatics 12: 102. doi: 10.1186/1471-2105-12-102 PMID: 21501495
88. 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. doi: 10.1105/tpc.111.093567 PMID: 22180627
89. Haas BJ, Delcher AL, Wortman JR, Salzberg SL (2004) DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics 20: 3643-3646. PMID: 15247098
90. Dalquen DA, Dessimoz C (2013) Bidirectional best hits miss many orthologs in duplication-rich clades such as plants and animals. Genome Biol Evol 5: 1800-1806. doi: 10.1093/gbe/evt132 PMID: 24013106
91. Zdobnov EM, Apweiler R (2001) InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848. PMID: 11590104
92. 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. PMID: 12136088
93. Dai X, Wang G, Yang DS, Tang Y, Broun P, Marks MD, et al. (2010) TrichOME: a comparative omics database for plant trichomes. Plant Physiol 152: 44-54. doi: 10.1104/pp.109.145813 PMID: 19939948
94. Marks MD, Wenger JP, Gilding E, Jilk R, Dixon RA (2009) Transcriptome analysis of Arabidopsis wild-type and gl3-sst sim trichomes identifies four additional genes required for trichome development. Mol Plant 2: 803-822. doi: 10.1093/mp/ssp037 PMID: 19626137
95. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17. PMID: 16166256
96. Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2- ΔΔCT Method. methods 25: 402-408. PMID: 11846609
97. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61: 539-542. doi: 10.1093/sysbio/sys029 PMID: 22357727
98. Miller M, Holder M, Vos R, Midford P, Liebowitz T, Chan L, et al. (2009) The CIPRES Portals. CIPRES. Available: http://wwwphyloorg/sub-sections/portal.
99. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214. PMID: 17996036
100. Rambaut A (2009) FigTree version 1.3. 1. Computer program distributed by the author. Available: http://treebioedacuk/software/figtree/.
101. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277. PMID: 10827456
102. Xiang T, Shibuya M, Katsube Y, Tsutsumi T, Otsuka M, Zhang H, et al. (2006) A New Triterpene Synthase from Arabidopsis t haliana Produces a Tricyclic Triterpene with Two Hydroxyl Groups. Organic letters 8: 2835-2838. PMID: 16774269
103. Dvorakova L, Cvrckova F, Fischer L (2007) Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns. BMC Genomics 8: 412. PMID: 17997832
104. Abel S, Savchenko T, Levy M (2005) Genome-wide comparative analysis of the IQD gene families in Arabidopsis thaliana and Oryza sativa. BMC Evol Biol 5: 72. PMID: 16368012
105. Wall DP, Fraser HB, Hirsh AE (2003) Detecting putative orthologs. Bioinformatics 19: 1710-1711. PMID: 15593400
106. Dessimoz C, Gabaldon T, Roos DS, Sonnhammer EL, Herrero J, Quest for Orthologs Consortium (2012) Toward community standards in the quest for orthologs. Bioinformatics 28: 900-904. doi: 10.1093/bioinformatics/bts050 PMID: 22332236
107. Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, Biswas M, et al. (2001) The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res 29: 37-40. PMID: 11125043
108. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37: D211-215. doi: 10.1093/nar/gkn785 PMID: 18940856
109. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, et al. (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30: 1236-1240. doi: 10.1093/bioinformatics/btu031 PMID: 24451626
110. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, et al. (2004) The Pfam protein families database. Nucleic Acids Res 32: D138-141. PMID: 14681378
111. Soding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21: 951-960. PMID: 15531603
112. Yeats C, Maibaum M, Marsden R, Dibley M, Lee D, Addou S, et al. (2006) Gene3D: modelling protein structure, function and evolution. Nucleic Acids Res 34: D281-284. PMID: 16381865
113. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, et al. (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 13: 2129-2141. PMID: 12952881
114. Gough J, Karplus K, Hughey R, Chothia C (2001) Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. Journal of Molecular Biology 313: 903-919. PMID: 11697912
115. Lipka V, Panstruga R (2005) Dynamic cellular responses in plant-microbe interactions. Curr Opin Plant Biol 8: 625-631. PMID: 16182598
116. Hauser MT (2014) Molecular basis of natural variation and environmental control of trichome patterning. Front Plant Sci 5: 320. doi: 10.3389/fpls.2014.00320 PMID: 25071803
117. Pattanaik S, Patra B, Singh SK, Yuan L (2014) An overview of the gene regulatory network controlling trichome development in the model plant, Arabidopsis. Front Plant Sci 5: 259. doi: 10.3389/fpls.2014.00259 PMID: 25018756
118. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, et al. (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64-69. PMID: 18079367
119. Soltis PS, Soltis DE (2013) Angiosperm phylogeny: A framework for studies of genome evolution: Springer.
120. Estévez JM, Cantero A, Romero C, Kawaide H, Jiménez LF, Kuzuyama T, et al. (2000) Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-Cmethyl-D-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol 124: 95-104. PMID: 10982425
121. Mandel MA, Feldmann KA, Herrera?Estrella L, Rocha?Sosa M, León P (1996) CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. The Plant Journal 9: 649-658. PMID: 8653115
122. Guimil S, Dunand C (2007) Cell growth and differentiation in Arabidopsis epidermal cells. J Exp Bot 58: 3829-3840. PMID: 18162628
123. Plant Ontology Consortium (2002) The Plant Ontology consortium and plant ontologies. International Journal of Genomics 3: 137-142.
124. Avraham S, Tung CW, Ilic K, Jaiswal P, Kellogg EA, McCouch S, et al. (2008) The Plant Ontology Database: a community resource for plant structure and developmental stages controlled vocabulary and annotations. Nucleic Acids Res 36: D449-454. doi: 10.1093/nar/gkm908 PMID: 18194960
125. Jaiswal P, Avraham S, Ilic K, Kellogg EA, McCouch S, Pujar A, et al. (2005) Plant Ontology (PO): a Controlled Vocabulary of Plant Structures and Growth Stages. Comp Funct Genomics 6: 388-397. doi: 10.1002/cfg.496 PMID: 18629207
126. Wang X, Weigel D, Smith LM (2013) Transposon variants and their effects on gene expression in Arabidopsis. PLoS Genet 9: e1003255. doi: 10.1371/journal.pgen.1003255 PMID: 23408902
127. Adams KL (2007) Evolution of duplicate gene expression in polyploid and hybrid plants. J Hered 98: 136-141. PMID: 17208934
128. Qiu Y, Liu S-L, Adams KL (2014) Frequent changes in expression profile and accelerated sequence evolution of duplicated imprinted genes in Arabidopsis. Genome biology and evolution 6: 1830-1842. PMID: 25115008
129. Hofberger JA, Nsibo DL, Govers F, Bouwmeester K, Schranz ME (2015) A complex interplay of tandem- and whole-genome duplication drives expansion of the L-type lectin receptor kinase gene family in the brassicaceae. Genome Biol Evol 7: 720-734. doi: 10.1093/gbe/evv020 PMID: 25635042
130. Kamolsukyunyong W, Sukhaket W, Ruanjaichon V, Toojinda T, Vanavichit A (2013) Single-feature polymorphism mapping of isogenic rice lines identifies the influence of terpene synthase on brown planthopper feeding preferences. Rice (N Y) 6: 18. doi: 10.1186/1939-8433-6-18 PMID: 24280452
131. Sallaud C, Giacalone C, Topfer R, Goepfert S, Bakaher N, Rosti S, et al. (2012) Characterization of two genes for the biosynthesis of the labdane diterpene Z-abienol in tobacco (Nicotiana tabacum) glandular trichomes. Plant J 72: 1-17. doi: 10.1111/j.1365-313X.2012.05068.x PMID: 22672125
132. Mendes MD, Barroso JG, Oliveira MM, Trindade H (2014) Identification and characterization of a second isogene encoding γ-terpinene synthase in Thymus caespititius. J Plant Physiol.
133. Lawler I, Foley W, Eschler B, Pass D, Handasyde K (1998) Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116: 160-169.
134. Trontin C, Tisné S, Bach L, Loudet O (2011) What does Arabidopsis natural variation teach us (and does not teach us) about adaptation in plants? Curr Opin Plant Biol 14: 225-231. doi: 10.1016/j.pbi.2011.03.024 PMID: 21536479
135. Edger PP, Pires JC (2009) Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res 17: 699-717. doi: 10.1007/s10577-009-9055-9 PMID: 19802709
136. Bekaert M, Edger PP, Pires JC, Conant GC (2011) Two-phase resolution of polyploidy in the Arabidopsis metabolic network gives rise to relative and absolute dosage constraints. Plant Cell 23: 1719-1728. doi: 10.1105/tpc.110.081281 PMID: 21540436
137. 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. doi: 10.1073/pnas.0900906106 PMID: 19325131
138. Fang L, Cheng F, Wu J, Wang X (2012) The Impact of Genome Triplication on Tandem Gene Evolution in Brassica rapa. Front Plant Sci 3: 261. doi: 10.3389/fpls.2012.00261 PMID: 23226149
139. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, et al. (2013) The fate of duplicated genes in a polyploid plant genome. The Plant Journal 73: 143-153. doi: 10.1111/tpj.12026 PMID: 22974547
140. Mühlhausen S, Kollmar M (2013) Whole genome duplication events in plant evolution reconstructed and predicted using myosin motor proteins. BMC evolutionary biology 13: 202. doi: 10.1186/1471-2148-13-202 PMID: 24053117
141. Chen R, Harada Y, Bamba T, Nakazawa Y, Gyokusen K (2012) Overexpression of an isopentenyl diphosphate isomerase gene to enhance trans-polyisoprene production in Eucommia ulmoides Oliver. BMC Biotechnol 12: 78. doi: 10.1186/1472-6750-12-78 PMID: 23110380
142. Berthelot K, Estevez Y, Deffieux A, Peruch F (2012) Isopentenyl diphosphate isomerase: A checkpoint to isoprenoid biosynthesis. Biochimie 94: 1621-1634. doi: 10.1016/j.biochi.2012.03.021 PMID: 22503704
143. Okada K, Kasahara H, Yamaguchi S, Kawaide H, Kamiya Y, Nojiri H, et al. (2008) Genetic evidence for the role of isopentenyl diphosphate isomerases in the mevalonate pathway and plant development in Arabidopsis. Plant Cell Physiol 49: 604-616. doi: 10.1093/pcp/pcn032 PMID: 18303110
144. Schranz ME, Mitchell-Olds T (2006) Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae. Plant Cell 18: 1152-1165. PMID: 16617098
145. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, et al. (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43: 476-481. doi: 10.1038/ng.807 PMID: 21478890
146. Zhao YJ, Cheng QQ, Su P, Chen X, Wang XJ, Gao W, et al. (2014) Research progress relating to the role of cytochrome P450 in the biosynthesis of terpenoids in medicinal plants. Appl Microbiol Biotechnol 98: 2371-2383. doi: 10.1007/s00253-013-5496-3 PMID: 24413977
147. Naur P, Petersen BL, Mikkelsen MD, Bak S, Rasmussen H, Olsen CE, 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. PMID: 12970475
148. Glenn WS, Runguphan W, O'Connor SE (2013) Recent progress in the metabolic engineering of alkaloids in plant systems. Curr Opin Biotechnol 24: 354-365. doi: 10.1016/j.copbio.2012.08.003 PMID: 22954587
149. Carretero-Paulet L, Fares MA (2012) Evolutionary dynamics and functional specialization of plant paralogs formed by whole and small-scale genome duplications. Mol Biol Evol 29: 3541-3551. doi: 10.1093/molbev/mss162 PMID: 22734049