Transcriptome-wide high-throughput deep m6A-seq reveals unique differential m6A methylation patterns between three organs in Arabidopsis thaliana

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Wan, Yizhen ^a,b   Tang, Kai ^b   Zhang, Dayong ^d   Xie, Shaojun ^b,c   Zhu, Xiaohong ^b,c   Wang, Zegang ^e   Lang, Zhaobo ^b,c  

^a NORTHWEST A F UNIVERSITY   (China)

^b PURDUE UNIVERSITY   (United States)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^d INSTITUTE OF PLANT PROTECTION   (China)

^e YANGZHOU UNIVERSITY   (China)

Author keywords

6 methyladenosine; M6A mapping; N; RNA differential methylation; Transcriptome wide patterns; Transposable element

Indexed keywords

MESSENGER RNA; PLANT RNA; TRANSCRIPTOME; UNTRANSLATED RNA; ADENOSINE; N(6)-METHYLADENOSINE; TRANSPOSON;

ARABIDOPSIS THALIANA; ARTICLE; CHEMICAL MODIFICATION; GENE EXPRESSION; GENETIC ASSOCIATION; HIGH THROUGHPUT SEQUENCING; NONHUMAN; OXIDATION REDUCTION REACTION; PLANT ORGANOGENESIS; PLANT STRESS; RNA METHYLATION; RNA MODIFICATION; RNA SEQUENCE; STOP CODON; TRANSPOSON; ANALOGS AND DERIVATIVES; ARABIDOPSIS; CHEMISTRY; FLOWER; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; METHYLATION; PLANT LEAF; PLANT ROOT; SEQUENCE ANALYSIS;

ADENOSINE; ARABIDOPSIS; DNA TRANSPOSABLE ELEMENTS; FLOWERS; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; METHYLATION; PLANT LEAVES; PLANT ROOTS; RNA, PLANT; SEQUENCE ANALYSIS, RNA;

EID: 84949762420     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0839-2     Document Type: Article

References (139)

1. Matera AG, Terns RM, Terns MP. Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat Rev Mol Cell Biol. 2007;8:209-20.
2. 6-methyl-adenosine modification in messenger and long non-coding RNA. Trends Biochem Sci. 2013;4:204-9.
3. Grosjean H. Fine-tuning of RNA functions by modification and editing. Berlin: Springer-Verlag; 2005.
4. 6-methyladenosine-dependent regulation of messenger RNA stability. Nature. 2013;7481:117-20.
5. 6A methylated mRNAs are enriched on translating ribosomes during meiosis, and under rapamycin treatment. PLoS One. 2015;10(7):e0132090.
6. 6A-seq. Nature. 2012;7397:201-6.
7. Zhong S, Hongying L, Bodi Z, Button JD, Vespa L, Herzog M, et al. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. Plant Cell. 2008;20:1278-88.
8. Meyer KD, Saletore Y, Zumbo P, Elemento O, Mason CE, Jaffrey SR. Comprehensive analysis of mRNA methylation reveals enrichment in 3' UTRs and near stop codons. Cell. 2012;7:1635-46.
9. Keene JD, Komisarow JM, Friedersdorf MB. RIP-Chip: the isolation and identification of mRNAs, microRNAs and protein components of ribonucleoprotein complexes from cell extracts. Nat Protoc. 2006;1:302-7.
10. 6A-seq based on immunocapturing and massively parallel sequencing. Nat Protoc. 2013;1:176-89.
11. Fustin JM, Doi M, Yamaguchi Y, Hida H, Nishimura S, Yoshida M, et al. RNA-methylation-dependent RNA processing controls the speed of the circadian clock. Cell. 2013;155:793-806.
12. Li YL, Wang XL, Li CP, Hu SN, Yu J, Song SH. Transcriptome-wide N6-methyladenosine profiling of rice callus and leaf reveals the presence of tissue-specific competitors involved in selective mRNA modification. RNA Biol. 2014;11(9):1180-8.
13. Luo GZ, MacQueen A, Zheng G, Duan H, Dore LC, Lu Z, et al. Unique features of the m6A methylome in Arabidopsis thaliana. Nat Commun. 2014;5:5630.
14. Csepany T, Lin A, Baldick Jr CJ, Beemon K. Sequence specificity of mRNA N6-adenosine methyltransferase. J Biol Chem. 1990;265:20117-22.
15. Schledzewski K, Brinkmann H, Mendel RR. Phylogenetic analysis of components of the eukaryotic vesicle transport system reveals a common origin of adaptor protein complexes 1, 2, and 3 and the F subcomplex of the coatomer COPI. J Mol Evol. 1999;6:770-8.
16. Footitt S, Slocombe SP, Larner V, Kurup S, Wu Y, Larson T, et al. Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J. 2002;12:2912-22.
17. Bedhomme M, Hoffmann M, McCarthy EA, Gambonnet B, Moran RG, Rébeillé F, et al. Folate metabolism in plants: an Arabidopsis homolog of the mammalian mitochondrial folate transporter mediates folate import into chloroplasts. J Biol Chem. 2005;41:34823-31.
18. Heyndrickx KS, Vandepoele K. Systematic identification of functional plant modules through the integration of complementary data sources. Plant Physiol. 2012;159:884-901.
19. Jammes F, Song C, Shin D, Munemasa S, Takeda K, Gu D, et al. MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc Natl Acad Sci U S A. 2009;48:20520-5.
20. Aranda-Sicilia MN, Cagnac O, Chanroj S, Sze H, Rodríguez-Rosales MP, Venema K. Arabidopsis KEA2, a homolog of bacterial KefC, encodes a K(+)/H(+) antiporter with a chloroplast transit peptide. Biochim Biophys Acta. 2012;9:2362-71.
21. Tsugeki R, Ditengou FA, Sumi Y, Teale W, Palme K, Okada K. NO VEIN mediates auxin-dependent specification and patterning in the Arabidopsis embryo, shoot, and root. Plant Cell. 2009;10:3133-51.
22. Charrier B, Champion A, Henry Y, Kreis M. Expression profiling of the whole Arabidopsis shaggy-like kinase multigene family by real-time reverse transcriptase-polymerase chain reaction. Plant Physiol. 2002;2:577-90.
23. Lellis AD, Kasschau KD, Whitham SA, Carrington JC. Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol. 2002;12:1046-51.
24. Kawamura Y, Uemura M. Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J. 2003;2:141-54.
25. Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, et al. The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics. 2006;7:2180-98.
26. Teotia S, Lamb RS. The paralogous genes RADICAL-INDUCED CELL DEATH1 and SIMILAR TO RCD ONE1 have partially redundant functions during Arabidopsis development. Plant J. 2008;1:29-41.
27. Chen LT, Luo M, Wang YY, Wu K. Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot. 2010;12:3345-53.
28. Kindgren P, Kremnev D, Blanco NE, de Dios Barajas López J, Fernández AP, Tellgren-Roth C, et al. The plastid redox insensitive 2 mutant of Arabidopsis is impaired in PEP activity and high light-dependent plastid redox signalling to the nucleus. Plant J. 2012;2:279-91.
29. Yang S, Zeng X, Li T, Liu M, Zhang S, Gao S, et al. AtACDO1, an ABC1-like kinase gene, is involved in chlorophyll degradation and the response to photooxidative stress in Arabidopsis. J Exp Bot. 2012;63(10):3959-73.
30. Zhang X, Wang C, Zhang Y, Sun Y, Mou Z. The Arabidopsis mediator complex subunit positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell. 2012;10:4294-309.
31. Pu L, Liu MS, Kim SY, Chen LF, Fletcher JC, Sung ZR. EMBRYONIC FLOWER1 and ULTRAPETALA1 act antagonistically on Arabidopsis development and stress response. Plant Physiol. 2013;2:812-30.
32. Shrestha B, Guragain B, Sridhar VV. Involvement of co-repressor LUH and the adapter proteins SLK1 and SLK2 in the regulation of abiotic stress response genes in Arabidopsis. BMC Plant Biol. 2014;14:54.
33. Lee SJ, Lee MH, Kim JI, Kim SY. Arabidopsis putative MAP kinase kinase kinases Raf10 and Raf11 are positive regulators of seed dormancy and ABA response. Plant Cell Physiol. 2015;1:84-97.
34. Zolman BK, Silva ID, Bartel B. The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid beta-oxidation. Plant Physiol. 2001;3:1266-78.
35. Nito K, Kamigaki A, Kondo M, Hayashi M, Nishimura M. Functional classification of Arabidopsis peroxisome biogenesis factors proposed from analyses of knockdown mutants. Plant Cell Physiol. 2007;6:763-74.
36. Attallah CV, Welchen E, Martin AP, Spinelli SV, Bonnard G, Palatnik JF, et al. Plants contain two SCO proteins that are differentially involved in cytochrome c oxidase function and copper and redox homeostasis. J Exp Bot. 2011;12:4281-94.
37. Hare PD, Moller SG, Huang LF, Chua NH. LAF3, a novel factor required for normal phytochrome A signaling. Plant Physiol. 2003;4:1592-604.
38. Parker G, Schofield R, Sundberg B, Turner S. Isolation of COV1, a gene involved in the regulation of vascular patterning in the stem of Arabidopsis. Development. 2003;10:2139-48.
39. van Leeuwen W, Okrész L, Bögre L, Munnik T. Learning the lipid language of plant signalling. Trends Plant Sci. 2004;8:378-84.
40. Caryl AP, Armstrong SJ, Jones GH, Franklin FC. A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma. 2000;109(1-2):62-71.
41. Kanno T, Bucher E, Daxinger L, Huettel B, Böhmdorfer G, Gregor W, et al. A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet. 2008;40(5):670-5.
42. Campi M, D'Andrea L, Emiliani J, Casati P. Participation of chromatin-remodeling proteins in the repair of ultraviolet-B-damaged DNA. Plant Physiol. 2012;158(2):981-95.
43. Liu Y, Deng Y, Li G, Zhao J. Replication factor C1 (RFC1) is required for double-strand break repair during meiotic homologous recombination in Arabidopsis. Plant J. 2013;73:154-65.
44. Hanada K, Zhang X, Borevitz JO, Li WH, Shiu SH. A large number of novel coding small open reading frames in the intergenic regions of the Arabidopsis thaliana genome are transcribed and/or under purifying selection. Genome Res. 2007;5:632-40.
45. Habu Y, Mathieu O, Tariq M, Probst AV, Smathajitt C, Zhu T, et al. Epigenetic regulation of transcription in intermediate heterochromatin. EMBO Rep. 2006;12:1279-84.
46. Yaish MW, Peng M, Rothstein SJ. AtMBD9 modulates Arabidopsis development through the dual epigenetic pathways of DNA methylation and histone acetylation. Plant J. 2009;1:123-35.
47. Joukov V, Groen AC, Prokhorova T, Gerson R, White E, Rodriguez A, et al. The BRCA1/BARD1 heterodimer modulates ran-dependent mitotic spindle assembly. Cell. 2006;3:539-52.
48. Liu Y, Wang F, Zhang H, He H, Ma L, Deng XW. Functional characterization of the Arabidopsis ubiquitin-specific protease gene family reveals specific role and redundancy of individual members in development. Plant J. 2008;5:844-56.
49. Silady RA, Ehrhardt DW, Jackson K, Faulkner C, Oparka K, Somerville CR. The GRV2/RME-8 protein of Arabidopsis functions in the late endocytic pathway and is required for vacuolar membrane flow. Plant J. 2008;1:29-41.
50. Li G, Siddiqui H, Teng Y, Lin R, Wan XY, Li J, et al. Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis. Nat Cell Biol. 2011;5:616-22.
51. Lei L, Li S, Du J, Bashline L, Gu Y. Cellulose synthase INTERACTIVE3 regulates cellulose biosynthesis in both a microtubule-dependent and microtubule-independent manner in Arabidopsis. Plant Cell. 2013;12:4912-23.
52. Fujimori K, Ohta D. Isolation and characterization of a histidine biosynthetic gene in Arabidopsis encoding a polypeptide with two separate domains for phosphoribosyl-ATP pyrophosphohydrolase and phosphoribosyl-AMP cyclohydrolase. Plant Physiol. 1998;1:275-83.
53. Han SK, Song JD, Noh YS, Noh B. Role of plant CBP/p300-like genes in the regulation of flowering time. Plant J. 2007;1:103-14.
54. Li MW, AuYeung WK, Lam HM. The GCN2 homologue in Arabidopsis thaliana interacts with uncharged tRNA and uses Arabidopsis eIF2aα molecules as direct substrates. Plant Biol (Stuttg). 2013;1:13-8.
55. Lu DP, Christopher DA. Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana. Mol Genet Genomics. 2008;3:199-210.
56. Brooks MA, Dziembowski A, Quevillon-Cheruel S. Structure of the yeast Pml1 splicing factor and its integration into the RES complex. Nucleic Acids Res. 2009;37:129-43.
57. Chung T, Wang D, Kim CS, Yadegari R, Larkins BA. Plant SMU-1 and SMU-2 homologues regulate pre-mRNA splicing and multiple aspects of development. Plant Physiol. 2009;3:1498-512.
58. Hamada T, Igarashi H, Taguchi R, Fujiwara M, Fukao Y, Shimmen T, et al. The putative RNA-processing protein, THO2, is a microtubule-associated protein in tobacco. Plant Cell Physiol. 2009;4:801-11.
59. Kang CH, Feng Y, Vikram M, Jeong IS, Lee JR, Bahk JD, et al. Arabidopsis thaliana PRP40s are RNA polymerase II C-terminal domain-associating proteins. Arch Biochem Biophys. 2009;1:30-8.
60. Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH. Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell. 2004;1:241-56.
61. Lee CP, Eubel H, O'Toole N, Millar AH. Heterogeneity of the mitochondrial proteome for photosynthetic and non-photosynthetic Arabidopsis metabolism. Mol Cell Proteomics. 2008;7:1297-316.
62. Zybailov B, Rutschow H, Friso GL, Rudella A, Emanuelsson O, Sun Q, et al. Sorting Signals, N-Terminal Modifications and Abundance of the Chloroplast Proteome. PLoS One. 2008;3(4), e1994.
63. Nikolovski N, Rubtsov D, Segura MP, Miles GP, Stevens TJ, Dunkley TP, et al. Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics. Plant Physiol. 2012;2:1037-51.
64. Rosgaard L, Zygadlo A, Scheller HV, Mant A, Jensen PE. Insertion of the plant photosystem I subunit G into the thylakoid membrane. FEBS J. 2005;15:4002-10.
65. de Bianchi S, Dall'Osto L, Tognon G, Morosinotto T, Bassi R. Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell. 2008;20(4):1012-28.
66. Sawchuk MG, Donner TJ, Head P, Scarpella E. Unique and overlapping expression patterns among members of photosynthesis-associated nuclear gene families in Arabidopsis. Plant Physiol. 2008;4:1908-24.
67. Woo HR, Kim JH, Nam HG, Lim PO. The delayed leaf senescence mutants of Arabidopsis, ore1, ore3, and ore9 are tolerant to oxidative stress. Plant Cell Physiol. 2004;7:923-32.
68. Mikkelsen MD, Thomashow MF. A role for circadian evening elements in cold-regulated gene expression in Arabidopsis. Plant J. 2009;2:328-39.
69. Zygadlo A, Jensen PE, Leister D, Scheller HV. Photosystem I lacking the PSI-G subunit has a higher affinity for plastocyanin and is sensitive to photodamage. Biochim Biophys Acta. 2005;2:154-63.
70. Ferro M, Brugière S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, et al. AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics. 2010;6:1063-84.
71. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, et al. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 2003;11:2623-33.
72. Gillissen B, Bürkle L, André B, Kühn C, Rentsch D, Brandl B, et al. A new family of high-affinity transporters for adenine, cytosine, and purine derivatives in Arabidopsis. Plant Cell. 2000;2:291-300.
73. Diener AC, Gaxiola RA, Fink GR. Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell. 2001;7:1625-38.
74. Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, et al. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 2001;4:1646-67.
75. Pertry I, Václavíková K, Depuydt S, Galuszka P, Spíchal L, Temmerman W, et al. Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc Natl Acad Sci U S A. 2009;3:929-34.
76. Bae MS, Cho EJ, Choi EY, Park OK. Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J. 2003;5:652-63.
77. Sels J, Mathys J, De Coninck BM, Cammue BP, De Bolle MF. Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol Biochem. 2008;11:941-50.
78. Wormit A, Butt SM, Chairam I, McKenna JF, Nunes-Nesi A, Kjaer L, et al. Osmosensitive changes of carbohydrate metabolism in response to cellulose biosynthesis inhibition. Plant Physiol. 2012;1:105-17.
79. Yang Y, Xu R, Ma CJ, Vlot AC, Klessig DF, Pichersky E. Inactive methyl indole-3-acetic acid ester can be hydrolyzed and activated by several esterases belonging to the AtMES esterase family of Arabidopsis. Plant Physiol. 2008;3:1034-45.
80. Tanaka H, Ishikawa M, Kitamura S, Takahashi Y, Soyano T, Machida C, et al. The AtNACK1/HINKEL and STUD/TETRASPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes Cells. 2004;12:1199-211.
81. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, et al. A gene expression map of Arabidopsis thaliana development. Nat Genet. 2005;5:501-6.
82. Borg M, Brownfield L, Khatab H, Sidorova A, Lingaya M, Twell D. The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell. 2011;2:534-49.
83. ReDuplák D, Dupl'áková N, Honys D. Wide-scale screening of T-DNA lines for transcription factor genes affecting male gametophyte development in Arabidopsis. Sex Plant Reprod. 2012;1:39-60.
84. Lee JH, Yoon HJ, Terzaghi W, Martinez C, Dai M, Li J, et al. DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell. 2010;6:1716-32.
85. Froehlich JE, Wilkerson CG, Ray WK, McAndrew RS, Osteryoung KW, Gage DA, et al. Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J Proteome Res. 2003;4:413-25.
86. Carroll AJ, Heazlewood JL, Ito J, Millar AH. Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol Cell Proteomics. 2008;2:347-69.
87. Mähönen AP, Higuchi M, Törmäkangas K, Miyawaki K, Pischke MS, Sussman MR, et al. Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr Biol. 2006;11:1116-22.
88. Suzuki T, Miwa K, Ishikawa K, Yamada H, Aiba H, Mizuno T. The Arabidopsis sensor His-kinase, AHk4, can respond to cytokinins. Plant Cell Physiol. 2001;2:107-13.
89. Gruis DF, Selinger DA, Curran JM, Jung R. Redundant proteolytic mechanisms process seed storage proteins in the absence of seed-type members of the vacuolar processing enzyme family of cysteine proteases. Plant Cell. 2002;11:2863-82.
90. Yang H, Matsubayashi Y, Nakamura K, Sakagami Y. Diversity of Arabidopsis genes encoding precursors for phytosulfokine, a peptide growth factor. Plant Physiol. 2001;3:842-51.
91. Etchells JP, Provost CM, Turner SR. Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling. PLoS Genet. 2012;11, e1002997.
92. Gidda SK, Miersch O, Levitin A, Schmidt J, Wasternack C, Varin L. Biochemical and molecular characterization of a hydroxyjasmonate sulfotransferase from Arabidopsis thaliana. J Biol Chem. 2003;20:17895-900.
93. Libault M, Wan J, Czechowski T, Udvardi M, Stacey G. Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol Plant Microbe Interact. 2007;8:900-11.
94. Huibers RP, de Jong M, Dekter RW, Van den Ackerveken G. Disease-specific expression of host genes during downy mildew infection of Arabidopsis. Mol Plant Microbe Interact. 2009;9:1104-15.
95. Ahlfors R, Brosché M, Kollist H, Kangasjärvi J. Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J. 2009;1:1-12.
96. Liu J, Elmore JM, Lin ZJ, Coaker G. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe. 2011;2:137-46.
97. Ogawa T, Ueda Y, Yoshimura K, Shigeoka S. Comprehensive analysis of cytosolic Nudix hydrolases in Arabidopsis thaliana. J Biol Chem. 2005;26:25277-83.
98. Brown DM, Zhang Z, Stephens E, Dupree P, Turner SR. Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis. Plant J. 2009;4:732-46.
99. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, et al. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature. 2007;7154:661-5.
100. Ghelis T, Bolbach G, Clodic G, Habricot Y, Miginiac E, Sotta B, et al. Protein tyrosine kinases and protein tyrosine phosphatases are involved in abscisic acid-dependent processes in Arabidopsis seeds and suspension cells. Plant Physiol. 2008;3:1668-80.
101. Salzman RA, Fujita T, Zhu-Salzman K, Hasegawa PM, Bressan RA. An improved RNA isolation method for plant tissues containing high levels of phenolic compounds or carbohydrates. Plant Mol Biol Rep. 1999;17:11-7.
102. Azevedo H, Lino-Neto T, Tavares RM. An improved method for high quality RNA isolation from needles of adult maritime pine trees. Plant Mol Biol Rep. 2003;21:333-8.
103. Bodi Z, Zhong S, Mehra S, Song J, Graham N, Li H, et al. Adenosine methylation in Arabidopsis mRNA is associated with the 3' End and reduced levels cause developmental defects. Front Plant Sci. 2012;3:48. eCollection 2012.
104. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular biology of the cell. 4th ed. New York, NY: Garland Science; 2002.
105. Dahlberg JE, Lund E. Does protein synthesis occur in the nucleus? Curr Opin Cell Biol. 2004;16:335-8.
106. Go YM, Jones DP. Redox compartmentalization in eukaryotic cells. Biochim Biophys Acta. 2008;1780(11):1273-90.
107. Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J. Molecular Cell Biology. 4th ed. New York, NY: W. H. Freeman; 2000.
108. Ochs RS. Biochemistry. Burlington, MA: Jones & Bartlett Learning; 2012.
109. Walter P, Blobel G. Translocation of proteins across the endoplasmic reticulum. II. Signal recognition protein (SRP) mediates the selective binding to microsomal membranes of in-vitro-assembled polysomes synthesizing secretory protein. J Cell Biol. 1981;91:551-6.
110. Walter P, Blobel G. Translocation of proteins across the endoplasmic reticulum III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J Cell Biol. 1981;91:557-61.
111. Stephens SB, Nicchitta CV. Divergent regulation of protein synthesis in the cytosol and endoplasmic reticulum compartments of mammalian cells. Mol Biol Cell. 2008;2:623-32.
112. 6A) in RNA: an old modification with a novel epigenetic function. Genomics Proteomics Bioinformatics. 2013;1:8-17.
113. Mohammad HP, Baylin SB. Linking cell signaling and the epigenetic machinery. Nat Biotechnol. 2010;10:1033-8.
114. Perry RP, Kelley DE, Friderici K, Rottman F. The methylated constituents of L cell messenger RNA: evidence for an unusual cluster at the 5' terminus. Cell. 1975;4:387-94.
115. 6-methyladenosine and gene expression control. Nat Rev Mol Cell Biol. 2014;5:313-26.
116. 6A RNA methylation. Nat Rev Genet. 2014;5:293-306.
117. Stoltzfus CM, Dane RW. Accumulation of spliced avian retrovirus mRNA is inhibited in S-adenosylmethionine-depleted chicken embryo fibroblasts. J Virol. 1982;42:918-31.
118. Camper SA, Albers RJ, Coward JK, Rottman FM. Effect of undermethylation on mRNA cytoplasmic appearance and half-life. Mol Cell Biol. 1984;4:538-43.
119. Tuck MT, Wiehl PE, Pan T. Inhibition of 6-methyladenine formation decreases the translation efficiency of dihydrofolate reductase transcripts. Int J Biochem Cell Biol. 1999;31:837-51.
120. DeLeon SBT, Davidson EH. Gene regulation: Gene control network in development. Annu Rev Biophys Biomol Struct. 2007;36:191-212.
121. Rapaport F, Khanin R, Liang Y, Pirun M, Krek A, Zumbo P, et al. Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data. Genome Biol. 2013;9:R95.
122. Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol. 2008;3:1201-11.
123. McMahon MJ, Kofranek AM, Rubatzky VE. Plant Science. Upper Saddle River, NJ: Pearson Education, Inc.; 2011.
124. Bengough AG, Bransby MF, Hans J, McKenna SJ, Roberts TJ, Valentine TA. Root responses to soil physical conditions; growth dynamics from field to cell. J Exp Bot. 2006;2:437-47.
125. Feschotte C. Transposable elements and the evolution of regulatory networks. Nat Rev Genet. 2008;9:397-405.
126. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: complexity, diversity, and dynamics. Science. 2009;5956:1112-5.
127. Bucher E, Reinders J, Mirouze M. Epigenetic control of transposon transcription and mobility in Arabidopsis. Curr Opin Plant Biol. 2012;5:503-10.
128. Belancio VP, Hedges DJ, Deininger P. Mammalian non-LTR retrotransposons: for better or worse, in sickness and in health. Genome Res. 2008;18:343-58.
129. Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8:272-85.
130. van de Lagemaat LN, Landry JR, Mager DL, Medstrand P. Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet. 2003;19:530-6.
131. Marino-Ramirez L, Lewis KC, Landsman D, Jordan IK. Transposable elements donate lineagespecific regulatory sequences to host genomes. Cytogenet Genome Res. 2005;110:333-41.
132. Kang SG, Liu WH, Lu P, Jin HY, Lim HW, Shepherd J, et al. MicroRNAs of the miR-17 92 family are critical regulators of T(FH) differentiation. Nat Immunol. 2013;8:849-57.
133. Gambiono G, Perrone I, Gribaudo I. A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem Anal. 2008;19:520-5.
134. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;4:R36.
135. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;16:2078-9.
136. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;7:923-30.
137. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative Genomics Viewer. Nat Biotechnol. 2011;1:24-6.
138. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;5:511-5.
139. Berardini TZ, Mundodi S, Reiser R, Huala E, Garcia-Hernandez M, Zhang P, et al. Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol. 2004;2:1-11.