Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea

Genome Biology

Volumn 15, Issue 6, 2014, Pages

  Parkin, Isobel A P ^a   Koh, Chushin ^b   Tang, Haibao ^c   Robinson, Stephen J ^a   Kagale, Sateesh ^a,b   Clarke, Wayne E ^a   Town, Chris D ^c   Nixon, John ^a   Krishnakumar, Vivek ^c   Bidwell, Shelby L ^c   Denoeud, France ^d,e,f   Belcram, Harry ^g   Links, Matthew G ^a   Just, Jérémy ^g   Clarke, Carling ^b   Bender, Tricia ^a   Huebert, Terry ^a   Mason, Annaliese S ^h   Chris Pires, J ⁱ   Barker, Guy ^j   Moore, Jonathan ^j   Walley, Peter G ^j   Manoli, Sahana ^h   Batley, Jacqueline ^h   Edwards, David ^h   Nelson, Matthew N ^k   Wang, Xiyin ^l   Paterson, Andrew H ^l   King, Graham ^m   Bancroft, Ian ⁿ   Chalhoub, Boulos ^g   Sharpe, Andrew G ^b   more..

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c J CRAIG VENTER INSTITUTE   (United States)

^d DIF   (France)

^e CNRS   (France)

^f UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^g INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^h UNIVERSITY OF QUEENSLAND   (Australia)

ⁱ UNIVERSITY OF MISSOURI   (United States)

^j UNIVERSITY OF WARWICK   (United Kingdom)

^k UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^l UNIVERSITY OF GEORGIA   (United States)

^m SOUTHERN CROSS UNIVERSITY   (Australia)

ⁿ UNIVERSITY OF YORK   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRASSICA OLERACEA; BRASSICA RAPA; CONTROLLED STUDY; DNA METHYLATION; GENE DOSAGE; GENE EXPRESSION; GENE MAPPING; GENOME SIZE; HEXAPLOIDY; NONHUMAN; PLANT GENOME; PLANT LEAF; POLYPLOIDY; TRANSCRIPTOMICS; ANEUPLOIDY; BRASSICA; CHROMOSOMAL MAPPING; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS;

BRASSICA OLERACEA;

TRANSCRIPTOME;

ANEUPLOIDY; BRASSICA; CHROMOSOME MAPPING; DNA METHYLATION; EPIGENESIS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME;

EID: 84905978616     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-6-r77     Document Type: Article

References (52)

1. Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, et al: The genome of the mesopolyploid crop species Brassica rapa. Nat Gen 2011, 43:1035-1039.
2. Navabi ZK, Huebert T, Sharpe AG, O'Neill CM, Bancroft I, Parkin IA: Conserved microstructure of the Brassica B Genome of Brassica nigra in relation to homologous regions of Arabidopsis thaliana, B. rapa and B. oleracea. BMC Genomics 2013, 14:250.
3. Leitch AR, Leitch IJ: Genomic plasticity and the diversity of polyploid plants. Science 2008, 320:481-483.
4. Bowers JE, Chapman BA, Rong J, Paterson AH: Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 2003, 422:433-438.
5. Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S: Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci U S A 2010, 107:18724-18728.
6. Tang H, Woodhouse MR, Cheng F, Schnable JC, Pedersen BS, Conant G, Wang X, Freeling M, Pires JC: Altered patterns of fractionation and exon deletions in Brassica rapa support a two-step model of paleohexaploidy. Genetics 2012, 190:1563-1574.
7. Cheng F, Wu J, Fang L, Sun S, Liu B, Lin K, Bonnema G, Wang X: Biased gene fractionation and dominant gene expression among the subgenomes of Brassica rapa. PLoS One 2012, 7:e36442.
8. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C, Cheung DW, Yiu SM, Peng S, Xiaoqian Z, Liu G, Liao X, Li Y, Yang H, Wang J, Lam TW, Wang J: SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 2012, 1:18.
9. Pop M, Kosack DS, Salzberg SL: Hierarchical scaffolding with Bambus. Genome Res 2004, 14:149-159.
10. Parra G, Bradnam K, Korf I: CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics (Oxford, England) 2007, 23:1061-1067.
11. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA: Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 2008, 3:e3376.
12. Poland JA, Brown PJ, Sorrells ME, Jannink JL: Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One 2012, 7:e32253.
13. Cantarel BL, Korf I, Robb SM, Parra G, Ross E, Moore B, Holt C, Sanchez Alvarado A, Yandell M: MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 2008, 18:188-196.
14. Town CD, Cheung F, Maiti R, Crabtree J, Haas BJ, Wortman JR, Hine EE, AlthoffR, Arbogast TS, Tallon LJ, Vigouroux M, Trick M, Bancroft I: Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 2006, 18:1348-1359.
15. Lespinet O, Wolf YI, Koonin EV, Aravind L: The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 2002, 12:1048-1059.
16. Kawabe A, Hansson B, Hagenblad J, Forrest A, Charlesworth D: Centromere locations and associated chromosome rearrangements in Arabidopsis lyrata and A. thaliana. Genetics 2006, 173:1613-1619.
17. Parkin IA, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ: Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 2005, 171:765-781.
18. Schranz ME, Lysak MA, Mitchell-Olds T: The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 2006, 11:535-542.
19. Cheng F, Mandakova T, Wu J, Xie Q, Lysak MA, Wang X: Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa. Plant Cell 2013, 25:1541-1554.
20. Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Halpern ME, Ukomadu C, Sadler KC, Pradhan S, Pellegrini M, Jacobsen SE: Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A 2010, 107:8689-8694.
21. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE: Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 2008, 452:215-219.
22. Schmitz RJ, He Y, Valdes-Lopez O, Khan SM, Joshi T, Urich MA, Nery JR, Diers B, Xu D, Stacey G, Ecker JR: Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res 2013, 23:1663-1674.
23. Schnable JC, Springer NM, Freeling M: Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci U S A 2011, 108:4069-4074.
24. Wang X, Torres MJ, Pierce G, Lemke C, Nelson LK, Yuksel B, Bowers JE, Marler B, Xiao Y, Lin L, Epps E, Sarazen H, Rogers C, Karunakaran S, Ingles J, Giattina E, Mun JH, Seol YJ, Park BS, Amasino RM, Quiros CF, Osborn TC, Pires JC, Town C, Paterson AH: A physical map of Brassica oleracea shows complexity of chromosomal changes following recursive paleopolyploidizations. BMC Genomics 2011, 12:470.
25. Iniguez-Luy FL, Lukens L, Farnham MW, Amasino RM, Osborn TC: Development of public immortal mapping populations, molecular markers and linkage maps for rapid cycling Brassica rapa and B. oleracea. Theor Appl Genet 2009, 120:31-43.
26. Himelblau E, Gilchrist EJ, Buono K, Bizzell C, Mentzer L, Vogelzang R, Osborn T, Amasino RM, Parkin IA, Haughn GW: Forward and reverse genetics of rapid-cycling Brassica oleracea. Theor Appl Genet 2009, 118:953-961.
27. Cheung F, Trick M, Drou N, Lim YP, Park JY, Kwon SJ, Kim JA, Scott R, Pires JC, Paterson AH, Town C, Bancroft I: Comparative analysis between homoeologous genome segments of Brassica napus and its progenitor species reveals extensive sequence-level divergence. Plant Cell 2009, 21:1912-1928.
28. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, de Pamphilis CW: Ancestral polyploidy in seed plants and angiosperms. Nature 2011, 473:97-100.
29. Innan H, Kondrashov F: The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 2010, 11:97-108.
30. Conant GC, Wolfe KH: Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 2008, 9:938-950.
31. Madlung A, Wendel JF: Genetic and epigenetic aspects of polyploid evolution in plants. Cytogenet Genome Res 2013, 140:270-285.
32. Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, Osborn T: Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiol 2006, 140:336-348.
33. Takuno S, Gaut BS: Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. Proc Natl Acad Sci U S A 2013, 110:1797-1802.
34. Kagale S, Koh C, Nixon J, Bollina V, Clarke WE, Tuteja R, Spillane C, Robinson SJ, Links MG, Clarke C, Higgins E, Huebert T, Sharpe AG, Parkin IAP: The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure. Nat Comm 2014, 5:3706.
35. Short Oligonucleotide Analysis Package. In [http://soap.genomics.org.cn/soapdenovo.html]
36. Wu TD, Watanabe CK: GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 2005, 21:1859-1875.
37. Mason AS, Nelson MN, Castello M-C, Yan G, Cowling WA: Genotypic effects on the frequency of homoeologous and homologous recombination in Brassica napus × B. carinata hybrids. Theor Appl Genetics 2011, 122:543-553.
38. Park TH, Kim JB, Hutten RC, van Eck HJ, Jacobsen E, Visser RG: Genetic positioning of centromeres using half-tetrad analysis in a 4×-2× cross population of potato. Genetics 2007, 176:85-94.
39. Trapnell C, Roberts A, GoffL, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L: Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012, 7:562-578.
40. Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, Salzberg SL, White O: Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 2003, 31:5654-5666.
41. Stanke M, Tzvetkova A, Morgenstern B: AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biol 2006, 7:S11 11. 18.
42. Automated Assignment of Human Readable Descriptions (AHRD). In [https://github.com/groupschoof/AHRD/]
43. Zhao M, Du J, Lin F, Tong C, Yu J, Huang S, Wang X, Liu S, Ma J: Shifts in the evolutionary rate and intensity of purifying selection between two Brassica genomes revealed by analyses of orthologous transposons and relics of a whole genome triplication. Plant J 2013, 76:211-222.
44. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH: A unified classification system for eukaryotic transposable elements. Nat Rev Genet 2007, 8:973-982.
45. RepeatMasker. In [http://www.repeatmasker.org]
46. Haas BJ, Delcher AL, Wortman JR, Salzberg SL: DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics 2004, 20:3643-3646.
47. R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2010 [http://www. R-project.org/]
48. Tukey JW: One degree of freedom for non-additivity. Biometrics 1949, 5:232-242.
49. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mole Biol 1990, 215:403-410.
50. Enright AJ, Van Dongen S, Ouzounis CA: An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002, 30:1575-1584.
51. Zhang H-B, Zhao X, Ding X, Paterson AH, Wing RA: Preparation of megabase-size DNA from plant nuclei. Plant J 1995, 7:175-184.
52. Xi Y, Li W: BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics 2009, 10:232.