Characterization of the Poplar Pan-Genome by Genome-Wide Identification of Structural Variation

Molecular Biology and Evolution

Volumn 33, Issue 10, 2016, Pages 2706-2719

  Pinosio, Sara ^a,b   Giacomello, Stefania ^b,c,h   Faivre Rampant, Patricia ^d   Taylor, Gail ^e   Jorge, Veronique ^f   Le Paslier, Marie Christine ^d   Zaina, Giusi ^c   Bastien, Catherine ^f   Cattonaro, Federica ^g   Marroni, Fabio ^b,c   Morgante, Michele ^b,c  

^a Institute of Biosciences and BioResources   (Italy)

^b Istituto di Genomica Applicata (IGA)   (Italy)

^c UNIVERSITY OF UDINE   (Italy)

^d DIF   (France)

^e UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^f National Institute for Agricultural Research   (France)

^g Applied Genomics Institute   (Italy)

^h SCIENCE FOR LIFE LABORATORY   (Sweden)

Author keywords

pan genome; poplar; structural variation; transposable elements

Indexed keywords

ARTICLE; CONTROLLED STUDY; COPY NUMBER VARIATION; GENE DELETION; GENE FUNCTION; GENE INSERTION; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; INDEL MUTATION; NONHUMAN; PAN GENOME; PLANT GENOME; POPULUS; POPULUS DELTOIDES; POPULUS NIGRA; POPULUS TRICHOCARPA; RETROPOSON; TELOMERE; TRANSPOSON; GENETICS; GENOMICS; PLANT GENE; STRUCTURE ACTIVITY RELATION;

DNA COPY NUMBER VARIATIONS; GENES, PLANT; GENOME, PLANT; GENOME-WIDE ASSOCIATION STUDY; GENOMICS; INDEL MUTATION; POPULUS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84994104585     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw161     Document Type: Article

References (75)

1. Alkan C, Coe BP, Eichler EE. 2011. Genome structural variation discovery and genotyping. Nat Rev Genet. 12:363-376
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410
3. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106
4. Anders S, Pyl PT, HuberW. 2014. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 31:166-169
5. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289-300
6. Bennetzen JL,Wang H. 2014. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol. 65:505-530
7. Bennetzen JL. 2000. Transposable element contributions to plant gene and genome evolution. Plant Mol Biol. 42:251-269
8. Blüthgen N, Brand K, Cajavec B, Swat M, Herzel H, Beule D. 2005. Biological profiling of gene groups utilizing Gene Ontology. Genome Inform. 16:106-115
9. Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A. 2005. Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17:343-360
10. Bush SJ, Castillo-Morales A, Tovar-Corona JM, Chen L, Kover PX, Urrutia AO. 2014. Presence-absence variation in A. thaliana is primarily associated with genomic signatures consistent with relaxed selective constraints.Mol Biol Evol. 31:59-69
11. Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C. 2012. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24:1242-1255
12. Cannon SB, Mitra A, Baumgarten A, Young ND, May G. 2004. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 4:10
13. CerveraM-T, Storme V, Ivens B, Gusmao J, Liu BH, Hostyn V, Van Slycken J, Van Montagu M, Boerjan W. 2001. Dense genetic linkage maps of three populus species (Populus deltoides, P. nigra and P. trichocarpa) based on AFLP and microsatellite markers. Genetics 158:787-809
14. Cervera MT, Storme V, Soto A, Ivens B, Van Montagu M, Rajora OP, Boerjan W. 2005. Intraspecific and interspecific genetic and phylogenetic relationships in the genus Populus based on AFLP markers. Theor Appl Genet. 111:1440-1456
15. Chia J-M, Song C, Bradbury PJ,CostichD, LeonN, Doebley J, Elshire RJ, Gaut B, Geller L, Glaubitz JC, et al. 2012. Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet. 44:803-807
16. Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, Shinn P, Warthmann N, Hu TT, Fu G, Hinds DA, et al. 2007. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317:338-342
17. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-3676
18. Cossu RM, Buti M, Giordani T, Natali L, Cavallini A. 2011. A computational study of the dynamics of LTR retrotransposons in the Populus trichocarpa genome. Tree Genet Genomes 8:61-75
19. Eichler EE, Flint J, Gibson G, Kong A, Leal SM, Moore JH, Nadeau JH. 2010. Missing heritability and strategies for finding the underlying causes of complex disease. Nat Rev Genet. 11:446-450
20. Eichler EE, Sankoff D. 2003. Structural dynamics of eukaryotic chromosome evolution. Science 301:793-797
21. Einspahr DW, Benson MK. 1964. Production and evaluation of Aspen hybrids. J For 62:806-809. (4)
22. Faivre-Rampant P, Zaina G, Jorge V, Giacomello S, Segura V, Scalabrin S, Guerin V, De Paoli E, Aluome C, Viger M, et al. 2016. New resources for genetic studies in Populus nigra: genome wide SNP discovery and development of a 12k Infinium array. Mol Ecol Resour. 16:1023-1036
23. Feschotte C, Jiang N, Wessler SR. 2002. Plant transposable elements: where genetics meets genomics. Nat Rev Genet. 3:329-341
24. Flutre T, Duprat E, Feuillet C, Quesneville H. 2011. Considering transposable element diversification in de novo annotation approaches. PLoS One 6:e16526
25. Fossati T, Zapelli I, Bisoffi S, Micheletti A, Vietto L, Sala F, Castiglione S. 2005. Genetic relationships and clonal identity in a collection of commercially relevant poplar cultivars assessed by AFLP and SSR. Tree Genet Genomes 1:11-20
26. Gaines TA, Zhang W, Wang D, Bukun B, Chisholm ST, Shaner DL, Nissen SJ, Patzoldt WL, Tranel PJ, Culpepper AS, et al. 2010. Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci USA. 107:1029-1034
27. Hurwitz BL, Kudrna D, Yu Y, Sebastian A, Zuccolo A, Jackson SA, Ware D, Wing RA, Stein L. 2010. Rice structural variation: a comparative analysis of structural variation between rice and three of its closest relatives in the genus Oryza. Plant J. 63:990-1003
28. Jiang J, Birchler JA, ParrottWA, Kelly Dawe R. 2003. A molecular view of plant centromeres. Trends Plant Sci. 8:570-575
29. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O,Walichiewicz J. 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 110:462-467
30. Kidwell MG, Lisch D. 1997. Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci USA. 94:7704-7711
31. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14:R36
32. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16:111-120
33. Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin F. 2008. Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol. 66:619-636
34. Lai J, Li R,Xu X, JinW, XuM, ZhaoH, Xiang Z, SongW, Ying K,ZhangM, et al. 2010. Genome-wide patterns of genetic variation among elite maize inbred lines. Nat Genet. 42:1027-1030
35. Lam H-M, Xu X, Liu X, Chen W, Yang G,Wong F-L, Li M-W, He W, Qin N, Wang B, et al. 2010. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet. 42:1053-1059
36. Leister D. 2004. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet. 20:116-122
37. Li B, Wyckoff GW, Einspahr DW. 1993. Hybrid Aspen performance and genetic gains. North J Appl For 10:117-122
38. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760
39. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079
40. Li W-H. 1993. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol Evol. 36:96-99
41. Li Y, Zhou G, Ma J, JiangW, Jin L, Zhang Z, Guo Y, Zhang J, Sui Y, Zheng L, et al. 2014. De novo assembly of soybean wild relatives for pangenome analysis of diversity and agronomic traits. Nat Biotechnol. 32:1045-1052
42. Lu P, Han X, Qi J, Yang J, Wijeratne AJ, Li T, Ma H. 2012. Analysis of Arabidopsis genome-wide variations before and after meiosis and meiotic recombination by resequencing Landsberg erecta and all four products of a single meiosis. Genome Res. 22:508-518
43. Ma J, Bennetzen JL. 2004. Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA. 101:12404-12410
44. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, et al. 2009. Finding the missing heritability of complex diseases. Nature 461:747-753
45. Marcais G, Kingsford C. 2011. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27:764-770
46. Maron LG, Guimaraes CT, Kirst M, Albert PS, Birchler JA, Bradbury PJ, Buckler ES, Coluccio AE, Danilova TV, Kudrna D, et al. 2013. Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci USA. 110:5241-5246
47. Marroni F, Pinosio S, Di Centa E, Jurman I, Boerjan W, Felice N, Cattonaro F, Morgante M. 2011. Large scale detection of rare variants via pooled multiplexed next generation sequencing: towards next generation Ecotilling. Plant J. 67:736-745
48. Marroni F, Pinosio S, Morgante M. 2014. Structural variation and genome complexity: is dispensable really dispensable? Curr Opin Plant Biol. 18:31-36
49. Martin M. 2011. Cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet J. 17:10-12
50. McHale LK, Haun WJ, Xu WW, Bhaskar PB, Anderson JE, Hyten DL, Gerhardt DJ, Jeddeloh JA, Stupar RM. 2012. Structural variants in the soybean genome localize to clusters of biotic stress-response genes. Plant Physiol. 159:1295-1308
51. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. 2003. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809-834
52. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A. 2005. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet. 37:997-1002
53. Morgante M, De Paoli E, Radovic S. 2007. Transposable elements and the plant pan-genomes. Curr Opin Plant Biol. 10:149-155
54. Nguyen D-Q, Webber C, Ponting CP. 2006. Bias of selection on human copy-number variants. PLoS Genet. 2:e20
55. Olson SA. 2002. EMBOSS opens up sequence analysis. European Molecular Biology Open Software Suite. Brief Bioinform. 3:87-91
56. Rausch T, Zichner T, Schlattl A, Stütz AM, Benes V, Korbel JO. 2012. DELLY: structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics 28:i333-i339
57. Ray DA, Batzer MA. 2011. Reading TE leaves: new approaches to the identification of transposable element insertions. Genome Res. 21:813-820
58. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16:276-277
59. Riethman H. 2008. Human subtelomeric copy number variations. Cytogenet Genome Res. 123:244-252
60. Rohde A, Storme V, Jorge V, Gaudet M, Vitacolonna N, Fabbrini F, Ruttink T, Zaina G, Marron N, Dillen S, et al. 2011. Bud set in poplar-genetic dissection of a complex trait in natural and hybrid populations. New Phytol. 189:106-121
61. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL. 1998. The paleontology of intergene retrotransposons of maize. Nat Genet. 20:43-45
62. SanseverinoW, Henaff E, VivesC, Pinosio S, Burgos-PazW, MorganteM, Ramos-Onsins SE, Garcia-Mas J, Casacuberta JM. 2015. Transposon insertions, structural variations, and SNPs contribute to the evolution of the melon genome. Mol Biol Evol. 32:2760-2774
63. Saxena RK, Edwards D, Varshney RK. 2014. Structural variations in plant genomes. Brief Funct Genomics 13:296-307
64. Sindi S, Helman E, Bashir A, Raphael BJ. 2009. A geometric approach for classification and comparison of structural variants. Bioinformatics 25:i222-i230
65. Smith SM, Pryor AJ, Hulbert SH. 2004. Allelic and haplotypic diversity at the rp1 rust resistance locus of maize. Genetics 167:1939-1947
66. Stettler RF, Bradshaw T, Heilman P. 1996. Biology of Populus and its implications for management and conservation. Ottawa: NRC Research Press
67. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. &Gray). Science 313:1596-1604
68. Vineis P, Pearce N. 2010. Missing heritability in genome-wide association study research. Nat Rev Genet. 11:589
69. Wang H, Xu Z, Yu H. 2008. LTR retrotransposons reveal recent extensive inter-subspecies nonreciprocal recombination in Asian cultivated rice. BMC Genomics 9:565
70. Xu X, Liu X, Ge S, Jensen JD, Hu F, Li X, Dong Y, Gutenkunst RN, Fang L, Huang L, et al. 2012. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol. 30:105-111
71. Yang L, Bennetzen JL. 2009. Distribution, diversity, evolution, and survival of Helitrons in the maize genome. Proc Natl Acad Sci USA. 106:19922-19927
72. Zhang HB, Zhao X, Ding X, Paterson AH,Wing RA. 1995. Preparation of megabase-size DNA from plant nuclei. Plant J. 7:175-184
73. Zhang Z, Mao L, Chen H, Bu F, Li G, Sun J, Li S, Sun H, Jiao C, Blakely R, et al. 2015. Genome-wide mapping of structural variations reveals a copy number variant that determines reproductive morphology in cucumber. Plant Cell 27:1595-1604
74. Zheng L-Y, Guo X-S, He B, Sun L-J, Peng Y, Dong S-S, Liu T-F, Jiang S, Ramachandran S, Liu C-M, et al. 2011. Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor). Genome Biol. 12:R114
75. Zmieńko A, Samelak A, Kozłowski P, Figlerowicz M. 2013. Copy number polymorphism in plant genomes. Theor Appl Genet. 127:1-18