Battles and hijacks: Noncoding transcription in plants

Trends in Plant Science

Volumn 20, Issue 6, 2015, Pages 362-371

  Ariel, Federico ^a   Romero Barrios, Natali ^a   Jégu, Teddy ^a   Benhamed, Moussa ^a,b   Crespi, Martin ^a  

^a CNRS   (France)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

Dual noncoding transcription; LncNATs; LncRNAs; RdDM

Indexed keywords

EUKARYOTA;

UNTRANSLATED RNA;

DNA METHYLATION; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; PLANT; PLANT GENOME;

DNA METHYLATION; EPIGENESIS, GENETIC; GENOME, PLANT; PLANTS; RNA, UNTRANSLATED; TRANSCRIPTION, GENETIC;

EID: 84930577223     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2015.03.003     Document Type: Review

References (114)

1. Eddy S.R. The C-value paradox, junk DNA and ENCODE. Curr. Biol. 2012, 22:898-899.
2. Birney E., et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447:799-816.
3. Yamada K., et al. Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 2003, 302:842-846.
4. Doolittle W.F. Is junk DNA bunk? A critique of ENCODE. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:5294-5300.
5. Cech T.R., Steitz J. The noncoding RNA revolution-trashing old rules to forge new ones. Cell 2014, 157:77-94.
6. Kim E-D., Sung S. Long noncoding RNA: unveiling hidden layer of gene regulatory networks. Trends Plant Sci. 2012, 17:16-21.
7. Vannini A., Cramer P. Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Mol. Cell 2012, 45:439-446.
8. Haag J.R., Pikaard C.S. Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol. 2011, 12:483-492.
9. Wierzbicki A.T., et al. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 2008, 135:635-648.
10. Rinn J.L., Chang H.Y. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 2012, 81:145-166.
11. Zheng Q., et al. RNA polymerase V targets transcriptional silencing components to promoters of protein-coding genes. Plant J. 2013, 73:179-189.
12. Bonasio R., Shiekhattar R. Regulation of transcription by long noncoding RNAs. Annu. Rev. Genet. 2014, 48:433-455.
13. Hirsch J., et al. Characterization of 43 non-protein-coding mRNA genes in Arabidopsis, including the MIR162a-derived Transcripts. Plant Physiol. 2006, 140:1192-1204.
14. Ben Amor B., et al. Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res. 2009, 19:57-69.
15. Wen J., et al. In silico identification and characterization of mRNA-like noncoding transcripts in Medicago truncatula. In silico Biol. 2007, 7:485-505.
16. Zhang H., et al. Long non-coding genes implicated in response to stripe rust pathogen stress in wheat (Triticum aestivum L.). Mol. Biol. Rep. 2013, 40:6245-6253.
17. Martin L.B.B., et al. Catalyzing plant science research with RNA-seq. Front. Plant Sci. 2013, 4:66.
18. Liu J., et al. Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 2012, 24:4333-4345.
19. Wang H., et al. Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res. 2014, 24:444-453.
20. Shuai P., et al. Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa. J. Exp. Bot. 2014, 65:4975-4983.
21. Chen J., et al. Genome-wide identification of novel long non-coding RNAs in Populus tomentosa tension wood, opposite wood and normal wood xylem by RNA-seq. Planta 2015, 241:125-143.
22. Soderlund C., et al. Sequencing, mapping, and analysis of 27,455 maize full-length cDNAs. PLoS Genet. 2009, 5:e1000740.
23. Boerner S., McGinnis K.M. Computational identification and functional predictions of long noncoding RNA in Zea mays. PLoS ONE 2012, 7:e43047.
24. Zhang W., et al. Identification of maize long non-coding RNAs responsive to drought stress. PLoS ONE 2014, 9:e98958.
25. Ulitsky I., Bartel D.P. lincRNAs: genomics, evolution, and mechanisms. Cell 2013, 154:26-46.
26. Crespi M., et al. enod4O, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J. 1994, 13:5099-5112.
27. Gultyaev A.P., Roussis A. Identification of conserved secondary structures and expansion segments in enod40 RNAs reveals new enod40 homologues in plants. Nucleic Acids Res. 2007, 35:3144-3152.
28. Rohrig H., et al. Soybean ENOD40 encodes two peptides that bind to sucrose synthase. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:1915-1920.
29. Campalans A., et al. Enod40, a short open reading frame - containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula. Plant Cell 2004, 16:1047-1059.
30. Bardou F., et al. Dual RNAs in plants. Biochimie 2011, 93:1950-1954.
31. Bardou F., et al. Long noncoding RNA modulates alternative splicing regulators in Arabidopsis. Dev. Cell 2014, 30:166-176.
32. Pant B.D., et al. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 2008, 53:731-738.
33. Franco-Zorrilla J.M., et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 2007, 39:1033-1037.
34. Wu H-J., et al. Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol. 2013, 161:1875-1884.
35. Kartha R.V., Subramanian S. Competing endogenous RNAs (ceRNAs): New entrants to the intricacies of gene regulation. Front. Genet. 2014, 5:1-9.
36. Ietswaart R., et al. Flowering time control: another window to the connection between antisense RNA and chromatin. Trends Genet. 2012, 28:445-453.
37. Marquardt S., et al. Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol. Cell 2014, 54:156-165.
38. Sun Q., et al. R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 2013, 340:619-621.
39. Wang Z-W., et al. Antisense-mediated FLC transcriptional repression requires the P-TEFb transcription elongation factor. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:7468-7473.
40. Crevillen P., et al. A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. EMBO J. 2013, 32:140-148.
41. Jegu T., et al. The BAF60 subunit of the SWI/SNF chromatin-remodeling complex directly controls the formation of a gene loop at FLOWERING LOCUS C in Arabidopsis. Plant Cell 2014, 26:538-551.
42. Csorba T., et al. Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:16160-16165.
43. Helliwell C., a, et al. Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLoS ONE 2011, 6:e21513.
44. Heo J.B., Sung S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 2011, 331:76-79.
45. Buzas D.M., et al. Transcription-dependence of histone H3 lysine 27 trimethylation at the Arabidopsis polycomb target gene FLC. Plant J. 2011, 65:872-881.
46. Kaneko S., et al. PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nat. Struct. Mol. Biol. 2013, 20:1258-1264.
47. Davidovich C., et al. Promiscuous RNA binding by polycomb repressive complex 2. Nat. Struct. Mol. Biol. 2013, 20:1250-1257.
48. Cifuentes-Rojas C., et al. Regulatory interactions between RNA and polycomb repressive complex 2. Mol. Cell 2014, 55:171-185.
49. Kretz M., Meister G. RNA binding of PRC2: promiscuous or well ordered?. Mol. Cell 2014, 55:157-158.
50. Jabnoune M., et al. A rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness. Plant Cell 2013, 25:4166-4182.
51. Wunderlich M., et al. Heat shock factor HSFB2a involved in gametophyte development of Arabidopsis thaliana and its expression is controlled by a heat-inducible long non-coding antisense RNA. Plant Mol. Biol. 2014, 85:541-550.
52. Zubko E., Meyer P. A natural antisense transcript of the Petunia hybrida Sho gene suggests a role for an antisense mechanism in cytokinin regulation. Plant J. 2007, 52:1131-1139.
53. Wang H., et al. Prediction of trans-antisense transcripts in Arabidopsis thaliana. Genome Biol. 2006, 7:R92.
54. Borsani O., et al. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 2005, 123:1279-1291.
55. Ron M., et al. Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev. 2010, 24:1010-1021.
56. Held M., a, et al. Small-interfering RNAs from natural antisense transcripts derived from a cellulose synthase gene modulate cell wall biosynthesis in barley. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:20534-20539.
57. Law J., Jacobsen S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 2010, 11:204-220.
58. Wierzbicki A.T. The role of long non-coding RNA in transcriptional gene silencing. Curr. Opin. Plant Biol. 2012, 15:517-522.
59. Matzke M.a, et al. RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu. Rev. Plant Biol. 2014, Published online December 10, 2014. 10.1146/annurev-arplant-043014-114633.
60. Moazed D. Small RNAs in transcriptional gene silencing and genome defence. Nature 2009, 457:413-420.
61. Moissiard G., et al. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 2012, 336:1448-1451.
62. Wierzbicki A.T., et al. Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev. 2012, 26:1825-1836.
63. Brabbs T.R., et al. The stochastic silencing phenotype of Arabidopsis morc6 mutants reveals a role in efficient RNA-directed DNA methylation. Plant J. 2013, 75:836-846.
64. Du J., et al. Mechanism of DNA methylation-directed histone methylation by KRYPTONITE. Mol. Cell 2014, 55:495-504.
65. Onodera Y., et al. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 2005, 120:613-622.
66. Herr A.J., et al. RNA polymerase IV directs silencing of endogenous DNA. Science 2005, 308:118-120.
67. Cam H.P., et al. Transcriptional scaffolds for heterochromatin assembly. Cell 2009, 136:610-614.
68. Ausin I., et al. IDN1 and IDN2: two proteins required for de novo DNA methylation in Arabidopsis thaliana. Nat. Struct. Mol. Biol. 2009, 16:1325-1327.
69. Law J., et al. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr. Biol. 2010, 20:951-956.
70. Ausin I., et al. INVOLVED IN DE NOVO 2-containing complex involved in RNA-directed DNA methylation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:8374-8381.
71. Johnson L.M., et al. SRA- and SET-domain-containing proteins link RNA Polymerase V occupancy to DNA methylation. Nature 2014, 507:124-128.
72. Bohmdorfer G., et al. RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA. Plant J. 2014, 79:181-191.
73. Pontes O., et al. RNA polymerase V functions in Arabidopsis interphase heterochromatin organization independently of the 24-nt siRNA-directed DNA methylation pathway. Mol. Plant 2009, 2:700-710.
74. He X-J., et al. NRPD4, a protein related to the RPB4 subunit of RNA Polymerase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation. Genes Dev. 2009, 23:318-330.
75. Law J., et al. SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLoS Genet. 2011, 7:e1002195.
76. Haag J.R., et al. In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell 2012, 48:811-828.
77. Xie Z., et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2004, 2:E104.
78. Kasschau K.D., et al. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol. 2007, 5:e57.
79. He X-J., et al. An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 2009, 137:498-508.
80. Wierzbicki A.T., et al. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat. Genet. 2009, 41:630-634.
81. Zhong X., et al. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 2014, 157:1050-1060.
82. Stroud H., et al. Plants regenerated from tissue culture contain stable epigenome changes in rice. Elife 2013, 2:e00354.
83. Stroud H., et al. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 2013, 152:352-364.
84. Erhard K.F., et al. Maize RNA polymerase IV defines trans-generational epigenetic variation. Plant Cell 2013, 25:808-819.
85. Ding J., et al. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2654-2659.
86. Ding J., et al. RNA-directed DNA methylation is involved in regulating photoperiod-sensitive male sterility in rice. Mol. Plant 2012, 5:1210-1216.
87. Zheng B., et al. Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 2009, 23:2850-2860.
88. Daxinger L., et al. A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J. 2009, 28:48-57.
89. You W., et al. Interplay among RNA polymerases II. IV and V in RNA-directed DNA methylation at a low copy transgene locus in Arabidopsis thaliana. Plant Mol. Biol. 2013, 82:85-96.
90. Gao Z., et al. An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 2010, 465:106-109.
91. Dunoyer P., et al. An endogenous, systemic RNAi pathway in plants. EMBO J. 2010, 29:1699-1712.
92. Sasaki T., et al. Distinct and concurrent pathways of Pol II and Pol IV-dependent siRNA biogenesis at a repetitive trans-silencer locus in Arabidopsis thaliana. Plant J. 2014, 2:127-138.
93. Cantone I., Fisher A.G. Epigenetic programming and reprogramming during development. Nat. Struct. Mol. Biol. 2013, 20:282-289.
94. Cavalli G., Misteli T. Functional implications of genome topology. Nat. Struct. Mol. Biol. 2013, 20:290-299.
95. Ariel F., et al. Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol. Cell 2014, 55:383-396.
96. Huarte M., et al. A large intergenic non-coding RNA induced by p53 mediates global gene repression in the p53 response. Cell 2010, 142:409-419.
97. Tsai M., et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science 2010, 329:689-693.
98. Tripathi V., et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol. Cell 2010, 39:925-938.
99. Cesana M., et al. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011, 147:358-369.
100. Carrieri C., et al. Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 2012, 491:454-457.
101. Ogawa Y., et al. Intersection of the RNA interference and X-inactivation pathways. Science 2008, 320:1336-1341.
102. Piacentini L., et al. Heterochromatin protein 1 (HP1a) positively regulates euchromatic gene expression through RNA transcript association and interaction with hnRNPs in Drosophila. PLoS Genet. 2009, 5:e1000670.
103. Yap K., et al. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 2010, 38:662-674.
104. Rinn J., Guttman M. RNA and dynamic nuclear organization. Science 2014, 345:1240-1241.
105. Zhu Y., et al. A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol. Cell 2013, 49:298-309.
106. Feng S., et al. Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol. Cell 2014, 55:694-707.
107. Grob S., et al. Hi-C analysis in Arabidopsis Identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol. Cell 2014, 55:678-693.
108. Sequeira-Mendes J., et al. The functional topography of the Arabidopsis genome is organized in a reduced number of linear motifs of chromatin states. Plant Cell 2014, 26:2351-2366.
109. Wang C., et al. Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res. 2014, 25:246-256.
110. Mendes M.A., et al. MADS domain transcription factors mediate short-range DNA looping that is essential for target gene expression in Arabidopsis. Plant Cell 2013, 25:2560-2572.
111. Boer D.R., et al. Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 2014, 156:577-589.
112. Hung T., et al. Extensive and coordinated transcription of noncoding RNAs within cell cycle promoters. Nat. Genet. 2011, 43:621-629.
113. Laloum T., et al. CCAAT-box binding transcription factors in plants: Y so many?. Trends Plant Sci. 2013, 18:157-166.
114. Laloum T., et al. Two CCAAT-box-binding transcription factors redundantly regulate early steps of the legume-rhizobia endosymbiosis. Plant J. 2014, 79:757-768.