Environmental and epigenetic regulation of Rider retrotransposons in tomato
Autoři:
Matthias Benoit aff001; Hajk-Georg Drost aff001; Marco Catoni aff001; Quentin Gouil aff002; Sara Lopez-Gomollon aff002; David Baulcombe aff002; Jerzy Paszkowski aff001
Působiště autorů:
The Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
aff001; Department of Plant Sciences, University of Cambridge, Cambridg, United Kingdom
aff002
Vyšlo v časopise:
Environmental and epigenetic regulation of Rider retrotransposons in tomato. PLoS Genet 15(9): e1008370. doi:10.1371/journal.pgen.1008370
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008370
Souhrn
Transposable elements in crop plants are the powerful drivers of phenotypic variation that has been selected during domestication and breeding programs. In tomato, transpositions of the LTR (long terminal repeat) retrotransposon family Rider have contributed to various phenotypes of agronomical interest, such as fruit shape and colour. However, the mechanisms regulating Rider activity are largely unknown. We have developed a bioinformatics pipeline for the functional annotation of retrotransposons containing LTRs and defined all full-length Rider elements in the tomato genome. Subsequently, we showed that accumulation of Rider transcripts and transposition intermediates in the form of extrachromosomal DNA is triggered by drought stress and relies on abscisic acid signalling. We provide evidence that residual activity of Rider is controlled by epigenetic mechanisms involving siRNAs and the RNA-dependent DNA methylation pathway. Finally, we demonstrate the broad distribution of Rider-like elements in other plant species, including crops. Our work identifies Rider as an environment-responsive element and a potential source of genetic and epigenetic variation in plants.
Klíčová slova:
Biology and life sciences – Organisms – Eukaryota – Plants – Fruits – Tomatoes – Solanum – Genetics – Gene expression – Gene regulation – Small interfering RNAs – Epigenetics – DNA modification – DNA – Genetic elements – Retrotransposons – Genomics – Mobile genetic elements – Transposable elements – Plant genomics – Plant genetics – Biochemistry – Nucleic acids – RNA – Non-coding RNA – Cell biology – Chromosome biology – Chromatin – Chromatin modification – DNA methylation – Bioengineering – Biotechnology – Plant biotechnology – Plant science – Research and analysis methods – Database and informatics methods – Bioinformatics – Sequence analysis – Sequence motif analysis – Sequence alignment – Engineering and technology
Zdroje
1. Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14: 49–61. doi: 10.1038/nrg3374 23247435
2. Lisch D (2009) Epigenetic Regulation of Transposable Elements in Plants. Annu Rev Plant Biol 60: 43–66. doi: 10.1146/annurev.arplant.59.032607.092744 19007329
3. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8: 272–285. doi: 10.1038/nrg2072 17363976
4. Zhang H, Zhu J-K (2011) RNA-directed DNA methylation. Curr Opin Plant Biol 14: 142–147. doi: 10.1016/j.pbi.2011.02.003 21420348
5. Rigal M, Mathieu O (2011) A ‘mille-feuille’ of silencing: Epigenetic control of transposable elements. Biochim Biophys Acta—Gene Regul Mech 1809: 452–458.
6. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204–220. doi: 10.1038/nrg2719 20142834
7. Matzke M, Kanno T, Huettel B, Daxinger L, Matzke AJM (2007) Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10: 512–519. doi: 10.1016/j.pbi.2007.06.007 17702644
8. Wendte JM, Pikaard CS (2017) The RNAs of RNA-directed DNA methylation. Biochim Biophys Acta 1860: 140–148.
9. Mirouze M, Reinders J, Bucher E, Nishimura T, Schneeberger K, Ossowski S, Cao J, Weigel D, Paszkowski J, Mathieu O (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461: 1–5.
10. Kato M, Miura A, Bender J, Jacobsen SE, Kakutani T (2003) Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13: 421–426. doi: 10.1016/s0960-9822(03)00106-4 12620192
11. Lanciano S, Carpentier MC, Llauro C, Jobet E, Robakowska-Hyzorek D, Lasserre E, Ghesquière A, Panaud O, Mirouze M (2017) Sequencing the extrachromosomal circular mobilome reveals retrotransposon activity in plants. PLoS Genet 13: 1–20.
12. Hu L, Li N, Xu C, Zhong S, Lin X, Yang J, Zhou T, Yuliang A, Wu Y, Chen Y-R, et al. (2014) Mutation of a major CG methylase in rice causes genome-wide hypomethylation, dysregulated genome expression, and seedling lethality. Proc Natl Acad Sci 111: 10642–10647. doi: 10.1073/pnas.1410761111 25002488
13. Cheng C, Tarutani Y, Miyao A, Ito T, Yamazaki M, Sakai H, Fukai E, Hirochika H (2015) Loss of function mutations in the rice chromomethylase OsCMT3a cause a burst of transposition. Plant J 83: 1069–1081. doi: 10.1111/tpj.12952 26243209
14. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411: 212–214. doi: 10.1038/35075612 11346800
15. Lippman Z, Gendrel A-V, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, et al. (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471–476. doi: 10.1038/nature02651 15269773
16. Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461: 423–426. doi: 10.1038/nature08351 19734880
17. Griffiths J, Catoni M, Iwasaki M, Paszkowski J (2018) Sequence-Independent Identification of Active LTR Retrotransposons in Arabidopsis. Mol Plant 11: 508–511. doi: 10.1016/j.molp.2017.10.012 29107035
18. Tan F, Zhou C, Zhou Q, Zhou S, Yang W, Zhao Y, Li G, Zhou D-X (2016) Analysis of Chromatin Regulators Reveals Specific Features of Rice DNA Methylation Pathways. Plant Physiol 171: 2041–2054. doi: 10.1104/pp.16.00393 27208249
19. Chuong EB, Elde NC, Feschotte C (2017) Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet 18: 71–86. doi: 10.1038/nrg.2016.139 27867194
20. McClintock B (1951) Chromosome Organization and Genic Expression. Cold Spring Harb Symp Quant Biol 16: 13–47. doi: 10.1101/sqb.1951.016.01.004 14942727
21. Grandbastien MA (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3: 181–187.
22. Grandbastien MA, Audeon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa APP, Le QH, Melayah D, Petit M, Poncet C, et al. (2005) Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet Genome Res 110: 229–241. doi: 10.1159/000084957 16093677
23. 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. doi: 10.1105/tpc.111.095232 22427337
24. Johns M a, Mottinger J, Freeling M (1985) A low copy number, copia-like transposon in maize. EMBO J 4: 1093–1101. 2988938
25. Cho J, Benoit M, Catoni M, Drost H-G, Brestovitsky A, Oosterbeek M, Paszkowski J (2018) Sensitive detection of pre-integration intermediates of long terminal repeat retrotransposons in crop plants. Nat Plants 5: 317479.
26. Tittel-Elmer M, Bucher E, Broger L, Mathieu O, Paszkowski J, Vaillant I (2010) Stress-Induced Activation of Heterochromatic Transcription. PLoS Genet 6: e1001175. doi: 10.1371/journal.pgen.1001175 21060865
27. Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Scheid OM (2010) Epigenetic Regulation of Repetitive Elements Is Attenuated by Prolonged Heat Stress in Arabidopsis. Plant Cell 22: 3118–3129. doi: 10.1105/tpc.110.078493 20876829
28. Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472: 115–119. doi: 10.1038/nature09861 21399627
29. Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler SR (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461: 1130–1134. doi: 10.1038/nature08479 19847266
30. Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN, Ross-Ibarra J, Springer NM (2015) Transposable Elements Contribute to Activation of Maize Genes in Response to Abiotic Stress. PLoS Genet 11: e1004915. doi: 10.1371/journal.pgen.1004915 25569788
31. Tenaillon MI, Hollister JD, Gaut BS (2010) A triptych of the evolution of plant transposable elements. Trends Plant Sci 15: 471–478. doi: 10.1016/j.tplants.2010.05.003 20541961
32. Sato S, Tabata S, Hirakawa H, Asamizu E, Shirasawa K, Isobe S, Kaneko T, Nakamura Y, Shibata D, Aoki K, et al. (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635–641. doi: 10.1038/nature11119 22660326
33. Xiao H, Jiang N, Schaffner E, Stockinger EJ, van der Knaap E (2008) A Retrotransposon-Mediated Gene Duplication Underlies Morphological Variation of Tomato Fruit. Science (80-) 319: 1527–1530. doi: 10.1126/science.1153040 18339939
34. Jiang N, Gao D, Xiao H, van der Knaap E (2009) Genome organization of the tomato sun locus and characterization of the unusual retrotransposon Rider. Plant J 60: 181–193. doi: 10.1111/j.1365-313X.2009.03946.x 19508380
35. Rodríguez GR, Muños S, Anderson C, Sim S-C, Michel A, Causse M, Gardener BBM, Francis D, van der Knaap E (2011) Distribution of SUN, OVATE, LC, and FAS in the tomato germplasm and the relationship to fruit shape diversity. Plant Physiol 156: 275–285. doi: 10.1104/pp.110.167577 21441384
36. Reynard GB (1961) New source of the j2 gene governing Jointless pedicel in tomato. Science (80-) 134: 2102.
37. Rick CM (1956) A new jointless gene from the Galapagos L. pimpinellifolium. TGC Rep 23.
38. Rick CM (1956) Genetic and Systematic Studies on Accessions of Lycospersicon from the Galapagos Islands. Am J Bot 43: 687.
39. Soyk S, Lemmon ZH, Oved M, Fisher J, Liberatore KL, Park SJ, Goren A, Jiang K, Ramos A, van der Knaap E, et al. (2017) Bypassing Negative Epistasis on Yield in Tomato Imposed by a Domestication Gene. Cell 169: 1142–1155.e12. doi: 10.1016/j.cell.2017.04.032 28528644
40. Fray RG, Grierson D (1993) Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant Mol Biol 22: 589–602. doi: 10.1007/bf00047400 8343597
41. Jiang N, Visa S, Wu S, Knaap E Van Der(2012) Rider Transposon Insertion and Phenotypic Change in Tomato. Springer Berlin Heidelberg, Berlin, Heidelberg.
42. Busch BL, Schmitz G, Rossmann S, Piron F, Ding J, Bendahmane A, Theres K (2011) Shoot Branching and Leaf Dissection in Tomato Are Regulated by Homologous Gene Modules. Plant Cell 23: 3595–3609. doi: 10.1105/tpc.111.087981 22039213
43. Brown JC, Chaney RL, Ambler JE (1971) A New Tomato Mutant Inefficient in the Transport of Iron. Physiol Plant 25: 48–53.
44. Ling H-Q, Bauer P, Bereczky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci U S A 99: 13938–13943. doi: 10.1073/pnas.212448699 12370409
45. Cheng X, Zhang D, Cheng Z, Keller B, Ling H-Q (2009) A New Family of Ty1-copia-Like Retrotransposons Originated in the Tomato Genome by a Recent Horizontal Transfer Event. Genetics 181: 1183–1193. doi: 10.1534/genetics.108.099150 19153256
46. Wang Y, Diehl A, Wu F, Vrebalov J, Giovannoni J, Siepel A, Tanksley SD (2008) Sequencing and comparative analysis of a conserved syntenic segment in the Solanaceae. Genetics 180: 391–408. doi: 10.1534/genetics.108.087981 18723883
47. Gilbert C, Feschotte C (2018) Horizontal acquisition of transposable elements and viral sequences: patterns and consequences. Curr Opin Genet Dev 49: 15–24. doi: 10.1016/j.gde.2018.02.007 29505963
48. Galindo-González L, Mhiri C, Deyholos MK, Grandbastien M-AA (2017) LTR-retrotransposons in plants: Engines of evolution. Gene 626: 14–25. doi: 10.1016/j.gene.2017.04.051 28476688
49. Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J Biol Chem 277: 45049–45058. doi: 10.1074/jbc.M207941200 12218065
50. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15: 63–78. doi: 10.1105/tpc.006130 12509522
51. Yang A, Dai X, Zhang W-H (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63: 2541–2556. doi: 10.1093/jxb/err431 22301384
52. Gómez-Porras JL, Riaño-Pachón D, Dreyer I, Mayer JE, Mueller-Roeber B (2007) Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. BMC Genomics 8: 260. doi: 10.1186/1471-2164-8-260 17672917
53. Timmerhaus G, Hanke ST, Buchta K, Rensing SA (2011) Prediction and validation of promoters involved in the abscisic acid response in physcomitrella patens. Mol Plant 4: 713–729. doi: 10.1093/mp/ssr009 21398384
54. Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, et al. (2017) Abscisic Acid Signaling and Abiotic Stress Tolerance in Plants: A Review on Current Knowledge and Future Prospects. Front Plant Sci 08: 1–12.
55. Sagi M, Fluhr R, Lips SH (1999) Aldehyde oxidase and xanthine dehydrogenase in a flacca tomato mutant with deficient abscisic acid and wilty phenotype. Plant Physiol 120: 571–578. doi: 10.1104/pp.120.2.571 10364409
56. Parry AD, Neill SJ, Horgan R (1988) Xanthoxin levels and metabolism in the wild-type and wilty mutants of tomato. Planta 173: 397–404. doi: 10.1007/BF00401027 24226547
57. Burbidge A, Grieve TM, Jackson A, Thompson A, Mccarty DR, Taylor IB (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17: 427–431. doi: 10.1046/j.1365-313x.1999.00386.x 10205899
58. Harrison E, Burbidge A, Okyere JP, Thompson AJ, Taylor IB (2011) Identification of the tomato ABA-deficient mutant sitiens as a member of the ABA-aldehyde oxidase gene family using genetic and genomic analysis. Plant Growth Regul 64: 301–309.
59. Maruyama KY, Todaka DA, Mizoi JU, Yoshida TA, Kidokoro SA, Matsukura SA, Takasaki HI, Sakurai TE, Yamamoto YOY, Yoshiwara KY (2012) Identification of Cis -Acting Promoter Elements in Cold- and Dehydration- Induced Transcriptional Pathways in Arabidopsis, Rice, and Soybean. DNA Res 19: 37–49. doi: 10.1093/dnares/dsr040 22184637
60. Gouil Q, Baulcombe DC (2016) DNA Methylation Signatures of the Plant Chromomethyltransferases. PLoS Genet 12: 1–17.
61. Perlman PS, Boeke JD (2004) Ring around the retroelement. Science 303: 182–184. doi: 10.1126/science.1093514 14716001
62. Kilzer JM, Stracker T, Beitzel B, Meek K, Weitzman M, Bushman FD (2003) Roles of host cell factors in circularization of retroviral DNA. Virology 314: 460–467. doi: 10.1016/s0042-6822(03)00455-0 14517098
63. Li L, Olvera JM, Yoder KE, Mitchell RS, Butler SL, Lieber M, Martin SL, Bushman FD (2001) Role of the non-homologous DNA end joining pathway in the early steps of retroviral infection. EMBO J 20: 3272–3281. doi: 10.1093/emboj/20.12.3272 11406603
64. Flavell AJ, Ish-Horowicz D (1981) Extrachromosomal circular copies of the eukaryotic transposable element copia in cultured Drosophila cells. Nature 292: 591–595. doi: 10.1038/292591a0 6265802
65. Flavell AJ, Ish-Horowicz D (1981) Extrachromosomal circular copies of the eukaryotic transposable element copia in cultured Drosophila cells. Nature 292: 591–595. doi: 10.1038/292591a0 6265802
66. Tam SM, Causse M, Garchery C, Burck H, Mhiri C, Grandbastien M-A (2007) The distribution of copia-type retrotransposons and the evolutionary history of tomato and related wild species. J Evol Biol 20: 1056–1072. doi: 10.1111/j.1420-9101.2007.01293.x 17465916
67. Yin H, Liu J, Xu Y, Liu X, Zhang S, Ma J, Du J (2013) TARE1, a Mutated Copia-Like LTR Retrotransposon Followed by Recent Massive Amplification in Tomato. PLoS One 8: e68587. doi: 10.1371/journal.pone.0068587 23861922
68. Wang Y, Tang X, Cheng Z, Mueller L, Giovannoni J, Tanksley SD (2006) Euchromatin and pericentromeric heterochromatin: comparative composition in the tomato genome. Genetics 172: 2529–2540. doi: 10.1534/genetics.106.055772 16489216
69. Gaubert H, Sanchez DH, Drost H-G, Paszkowski J (2017) Developmental Restriction of Retrotransposition Activated in Arabidopsis by Environmental Stress. Genetics 207: 813–821. doi: 10.1534/genetics.117.300103 28774882
70. Cavrak V V., Lettner N, Jamge S, Kosarewicz A, Bayer LM, Mittelsten Scheid O(2014) How a Retrotransposon Exploits the Plant’s Heat Stress Response for Its Activation. PLoS Genet 10: e1004115. doi: 10.1371/journal.pgen.1004115 24497839
71. Strand DJ, Mcdonald JF (1985) Copia is transcriptionally responsive to environmental stress. Nucleic Acids Res 13: 4401–4410. doi: 10.1093/nar/13.12.4401 2409535
72. Li Z, Peng R, Tian Y, Han H, Xu J, Yao Q (2016) Genome-Wide Identification and Analysis of the MYB Transcription Factor Superfamily in Solanum lycopersicum. Plant Cell Physiol 57: 1657–1677. doi: 10.1093/pcp/pcw091 27279646
73. Seo PJ, Xiang F, Qiao M, Park J-Y, Lee YN, Kim S-G, Lee Y-H, Park WJ, Park C-M (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol 151: 275–289. doi: 10.1104/pp.109.144220 19625633
74. Zhu N, Cheng S, Liu X, Du H, Dai M, Zhou D-X, Yang W, Zhao Y (2015) The R2R3-type MYB gene OsMYB91 has a function in coordinating plant growth and salt stress tolerance in rice. Plant Sci 236: 146–156. doi: 10.1016/j.plantsci.2015.03.023 26025528
75. Sugimoto K, Takeda S, Hirochika H (2000) MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defense-related genes. Plant Cell 12: 2511–2528. doi: 10.1105/tpc.12.12.2511 11148294
76. Corem S, Doron-Faigenboim A, Jouffroy O, Maumus F, Arazi T, Bouché N (2018) Redistribution of CHH Methylation and Small Interfering RNAs across the Genome of Tomato ddm1 Mutants. Plant Cell 30: tpc.00167.2018.
77. Kravchik M, Damodharan S, Stav R, Arazi T (2014) Generation and characterization of a tomato DCL3-silencing mutant. Plant Sci 221–222: 81–89. doi: 10.1016/j.plantsci.2014.02.007 24656338
78. Panda K, Ji L, Neumann DA, Daron J, Schmitz RJ, Slotkin RK (2016) Full-length autonomous transposable elements are preferentially targeted by expression-dependent forms of RNA-directed DNA methylation. Genome Biol 17: 170. doi: 10.1186/s13059-016-1032-y 27506905
79. McCue AD, Panda K, Nuthikattu S, Choudury SG, Thomas EN, Slotkin RK (2015) ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. EMBO J 34: 20–35. doi: 10.15252/embj.201489499 25388951
80. Nuthikattu S, McCue AD, Panda K, Fultz D, DeFraia C, Thomas EN, Slotkin RK (2013) The Initiation of Epigenetic Silencing of Active Transposable Elements Is Triggered by RDR6 and 21–22 Nucleotide Small Interfering RNAs. Plant Physiol 162: 116–131. doi: 10.1104/pp.113.216481 23542151
81. Herr AJ, Jensen MB, Dalmay T, Baulcombe DC (2005) RNA polymerase IV directs silencing of endogenous DNA. Science (80-) 308: 118–120. doi: 10.1126/science.1106910 15692015
82. Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E, Daxinger L, Kreil DP, Matzke M, Matzke AJM (2005) Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37: 761–765. doi: 10.1038/ng1580 15924141
83. Cuerda-Gil D, Slotkin RK (2016) Non-canonical RNA-directed DNA methylation. Nat Plants 2: 16163. doi: 10.1038/nplants.2016.163 27808230
84. Matzke M a, Mosher R a(2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15: 394–408. doi: 10.1038/nrg3683 24805120
85. Deaton A, Bird A (2011) CpG islands and the regulation of transcription. Genes Dev 25: 1010–1022. doi: 10.1101/gad.2037511 21576262
86. Ashikawa I (2001) Gene-associated CpG islands in plants as revealed by analyses of genomic sequences. Plant J 26: 617–625. doi: 10.1046/j.1365-313x.2001.01062.x 11489175
87. Tanksley SD, Ganal MW, Prince JP, De Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, et al. (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132: 1141–1160. 1360934
88. Catoni M, Griffiths J, Becker C, Zabet NR, Bayon C, Dapp M, Lieberman‐Lazarovich M, Weigel D, Paszkowski J (2017) DNA sequence properties that predict susceptibility to epiallelic switching. EMBO J 36: 617–628. doi: 10.15252/embj.201695602 28069706
89. Catoni M, Tsang JM, Greco AP, Zabet NR (2018) DMRcaller: a versatile R/Bioconductor package for detection and visualization of differentially methylated regions in CpG and non-CpG contexts. Nucleic Acids Res 1–11. doi: 10.1093/nar/gkx1156
90. Lawrence M, Huber W, Pagès H, Aboyoun P, Carlson M, Gentleman R, Morgan MT, Carey VJ (2013) Software for Computing and Annotating Genomic Ranges. PLoS Comput Biol 9: 1–10.
91. Pruitt KD, Tatusova T, Maglott DR (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35: D61–5. doi: 10.1093/nar/gkl842 17130148
92. Drost H-G, Paszkowski J (2017) Biomartr: genomic data retrieval with R. Bioinformatics 33: 1216–1217. doi: 10.1093/bioinformatics/btw821 28110292
93. Fernandez-Pozo N, Menda N, Edwards JD, Saha S, Tecle IY, Strickler SR, Bombarely A, Fisher-York T, Pujar A, Foerster H, et al. (2015) The Sol Genomics Network (SGN)—from genotype to phenotype to breeding. Nucleic Acids Res 43: D1036–D1041. doi: 10.1093/nar/gku1195 25428362
94. Lowe TM, Eddy SR (1996) TRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955–964.
95. Michaud M, Cognat V, Duchêne AM, Maréchal-Drouard L (2011) A global picture of tRNA genes in plant genomes. Plant J 66: 80–93. doi: 10.1111/j.1365-313X.2011.04490.x 21443625
96. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, et al. (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44: D279–D285. doi: 10.1093/nar/gkv1344 26673716
97. Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4: e2584. doi: 10.7717/peerj.2584 27781170
98. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410. doi: 10.1016/S0022-2836(05)80360-2 2231712
Štítky
Genetika Reprodukční medicínaČlánek vyšel v časopise
PLOS Genetics
2019 Číslo 9
- Primární hyperoxalurie – aktuální možnosti diagnostiky a léčby
- Srdeční frekvence embrya může být faktorem užitečným v předpovídání výsledku IVF
- Akutní intermitentní porfyrie
- Vztah užívání alkoholu a mužské fertility
- Šanci na úspěšný průběh těhotenství snižují nevhodné hladiny progesteronu vznikající při umělém oplodnění
Nejčtenější v tomto čísle
- Origins of DNA replication
- Environmental and epigenetic regulation of Rider retrotransposons in tomato
- Integrating transcriptomic network reconstruction and eQTL analyses reveals mechanistic connections between genomic architecture and Brassica rapa development
- Temperature preference can bias parental genome retention during hybrid evolution