An Overview of Transcription Regulatory Elements in Plant
AbstractIn eukaryotes, transcription regulation is a very complex process and crucial for the proper development and functioning of an organism. Various regulatory elements are involved in this complex regulation. Now there has been a recent surge in the identification of new regulatory element to understand the novel mechanism of transcription regulation. In this review, we summarized different types of transcription regulatory element along with their role in gene regulation. These include the promoter, enhancer, silencer, insulator and trans-acting elements. These regulatory elements contain numerous signatures sequences which are associated with their function and may be useful in their identification. Some of these regulatory elements present far apart from the target genes are known as distal regulatory elements. Now it has become clear that the different types of regulatory elements are not just required for the basal transcription but also involved in the temporal and spatial expression of the target gene.
Adrian J, Farrona S, Reimer JJ, Albani MC, Coupland G, Turck F (2010) cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22:1425-1440. doi: 10.1105/tpc.110.074682
Alberts B, Johnson A, Lewis J et al (2002) Molecular Biology of the Cell. 4th edition. New York: Garland Science; DNA-Binding Motifs in Gene Regulatory Proteins. Available from: https://www.ncbi.nlm.nih.gov/books/NBK26806/
Bannister AJ and Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Research 21:381-395. doi: 10.1038/cr.2011.22
Berger N, Dubreucq B, Roudier F, Dubos C, Lepiniec L (2011) Transcriptional regulation of Arabidopsis LEAFY COTYLEDON2 involves RLE, a cis-element that regulates trimethylation of histone H3 at lysine-27. Plant Cell 23:4065-4078. doi: 10.1105/tpc.111.087866
Blackwood EM and Kadonaga JT (1998) Going the distance: a current view of enhancer action. Science 281:60-63. doi: 10.1126/science.281.5373.60
Brown JL and Kassis JA (2013) Architectural and functional diversity of polycomb group response elements in Drosophila. Genetics 195:407-419. doi: 10.1534/genetics .113.153247
Carninci P, Sandelin A, Lenhard B, Katayama S, Shimokawa K, Ponjavic J, Semple CA, Taylor MS, Engström PG, Frith MC, Forrest AR (2006) Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet 38:626-635. doi:10.1038/ng1789
Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:423-438. doi: 10.1104/pp.111.186999
Chaubet N, Flénet M, Clément B, Brignon P, Gigot C (1996) Identification of cis‐elements regulating the expression of an Arabidopsis histone H4 gene. Plant J 10:425-435. doi: 10.1046/j.1365-313X.1996. 10030425.x
Choi D, Kim JH, Kende H (2004) Whole genome analysis of the OsGRF gene family encoding plant-specific putative transcription activators in rice (Oryza sativa L.). Plant Cell Physiol 45:897-904. doi: 10.1093/pcp/pch098
Clark RM, Wagler TN, Quijada P, Doebley J (2006) A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet 38:594-597. doi: 10.1038/ng1784
Debernardi JM, Mecchia MA, Vercruyssen L, Smaczniak C, Kaufmann K, Inze D, Rodriguez RE, Palatnik JF (2014) Post‐transcriptional control of GRF transcription factors by microRNA miR396 and GIF co‐activator affects leaf size and longevity. Plant J 79:413-426. doi: 10.1111/tpj.12567
Freitas RL, Carvalho CM, Fietto LG, Loureiro ME, Almeida AM, Fontes EP (2007) Distinct repressing modules on the distal region of the SBP2 promoter contribute to its vascular tissue-specific expression in different vegetative organs. Plant Mol Biol 65:603-614. doi: 10.1007/s11103-007-9225-0
García AV, Blanvillain-Baufumé S, Huibers RP, Wiermer M, Li G, Gobbato E, Rietz S, Parker JE (2010) Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathol 6:e1000970. doi: 10.1371/journal.ppat.1000970
Gaston K and Jayaraman PS (2003) Transcriptional repression in eukaryotes: repressors and repression mechanisms. Cell Mol Life Sci 60:721-741.
Gaszner M and Felsenfeld G (2006) Insulators: exploiting transcriptional and epigenetic mechanisms. Nat Rev Genet 7:703-713. doi:10.1038/nrg1925
Georges AB, Benayoun BA, Caburet S, Veitia RA (2010) Generic binding sites, generic DNA-binding domains: where does specific promoter recognition come from? FASEB J 24:346-356. doi: 10.1096/fj.09-142117
Gheldof N, Leleu M, Noordermeer D, Rougemont J, Reymond A (2012) Detecting long-range chromatin interactions using the chromosome conformation capture sequencing (4C-seq) method. Gene Regulatory Networks: Methods Mol Biol 786:211-225. doi: 10.1007/978-1-61779-292-2_13.
Gonzalez N, Pauwels L, Baekelandt A, De Milde L, Van Leene J, Besbrugge N, Heyndrickx KS, Pérez AC, Durand AN, De Clercq R, Van De SE (2015) A repressor protein complex regulates leaf growth in Arabidopsis. Plant Cell 27:2273-2287. doi: 10.1105/tpc.15.00006
Govind CK, Yoon S, Qiu H, Govind S, Hinnebusch AG (2005) Simultaneous recruitment of coactivators by Gcn4p stimulates multiple steps of transcription in vivo. Mol Cell Biol 25:5626-5638. doi: 10.1128/MCB.25.13.5626-5638.2005
Haerizadeh F, Singh MB, Bhalla PL (2006) Transcriptional repression distinguishes somatic from germ cell lineages in a plant. Science 313:496-499. doi: 10.1126/science.1125526
Hahn S and Young ET (2011) Transcriptional regulation in Saccharomyces cerevisiae: transcription factor regulation and function, mechanisms of initiation, and roles of activators and coactivators. Genetics 189:705-736. doi: 10.1534/genetics.111.127019
Hampsey M (1998) Molecular genetics of the RNA polymerase II general transcriptional machinery. Microbiol Mol Biol Rev 62:465-503.
Hernandez-Garcia CM and Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217:109-119. doi: 10.1016/j.plantsci.2013.12.007
Hily JM, Singer SD, Yang Y, Liu Z (2009) A transformation booster sequence (TBS) from Petunia hybrida functions as an enhancer-blocking insulator in Arabidopsis thaliana. Plant Cell Rep 28:1095-1104. doi: 10.1007/s00299-009-0700-8
Jepsen K and Rosenfeld MG (2002) Biological roles and mechanistic actions of co-repressor complexes. J Cell Sci 115:689-698.
Kadonaga JT (2004) Regulation of RNA polymerase II transcription by sequence-specific DNA binding factors. Cell 116:247-257. doi.org/10.1016/S0092-8674(03)01078-X
Kaplan CD, Laprade L, Winston F (2003) Transcription elongation factors repress transcription initiation from cryptic sites. Science 30:1096-1099. doi: 10.1126/science.1087374
Kim WC, Ko JH and Han KH (2012) Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. Plant Mol Biol 78:489-501. doi: 10.1007/s11103-012-9880-7
Kiran K, Ansari SA, Srivastava R, Lodhi N, Chaturvedi CP, Sawant SV, Tuli R (2006). The TATA-box sequence in the basal promoter contributes to determining light-dependent gene expression in plants. Plant physiol 142:364-76. doi: 10.1104/pp.106.084319
Kleinjan DA and van Heyningen V (2005) Long-range control of gene expression: emerging mechanisms and disruption in disease. Am J Hum Genet 76:8-32. doi: 10.1086/426833
Lai C, Xiong LX, Qin X (2009) A 43-bp A/T-rich element upstream of the kinesin gene AtKP1 promoter functions as a silencer in Arabidopsis. Plant Cell Rep 28:851-860. doi: 10.1007/s00299-009-0689-z
Lee JE and Golz JF (2012) Diverse roles of Groucho/Tup1 co-repressors in plant growth and development. Plant Signal Beha 7:86-92. doi: 10.4161/psb.7.1.18377
Lodish H, Berk A, Zipursky SL, et al. (2000) Eukaryotic Transcription Activators. Molecular Cell Biology. 4th edition. New York.
Lodish H, Berk A, Zipursky SL, et al. (2000) Molecular Cell Biology. 4th edition. New York: W. H. Freeman; Section 10.3, Eukaryotic Gene Control: Purposes and General Principles. Available from: https://www.ncbi.nlm.nih.gov/books/NBK21635/
Lodhi N, Ranjan A, Singh M, Srivastava R, Singh SP, Chaturvedi CP, Ansari SA, Sawant SV, Tuli R (2008) Interactions between upstream and core promoter sequences determine gene expression and nucleosome positioning in tobacco PR-1a promoter. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1779(10), pp.634-644.
Majumder P and Cai HN (2003) The functional analysis of insulator interactions in the Drosophila embryo. Proc Natl Acad Sci U S A 100:5223-5228. doi: 10.1073/pnas.0830190100
Maksimenko O, Golovnin A, Georgiev P (2008) Enhancer-promoter communication is regulated by insulator pairing in a Drosophila model bigenic locus. Mol Cell Biol 28:5469-5477. doi: 10.1128/MCB.00461-08
Maston GA, Evans SK, Green MR (2006) Transcriptional regulatory elements in the human genome. Annu Rev Genomics Hum Genet 7:29-59. doi: 10.1146/annurev.genom.7.080505.115623
Mikkelsen MD and Thomashow MF (2009) A role for circadian evening elements in cold‐regulated gene expression in Arabidopsis. Plant J 60:328-339. doi: 10.1111/j.1365-313X.2009. 03957.x
Miyoshi K, Shirai C, Mizuta K (2003) Transcription of genes encoding trans‐acting factors required for rRNA maturation/ribosomal subunit assembly is coordinately regulated with ribosomal protein genes and involves Rap1 in Saccharomyces cerevisiae. Nucleic Acids Res 31:1969-1973. doi: https://doi.org/10.1093/nar/gkg278
Molina C and Grotewold E (2005) Genome wide analysis of Arabidopsis core promoters. BMC Genomics, 6:1-12. doi: 10.1186/1471-2164-6-25
Montavon T and Duboule D (2013) Chromatin organization and global regulation of Hox gene clusters. Philos Trans R Soc Lond B Biol Sci 368: p.20120367. doi: 10.1098/rstb.2012.0367
Naar AM, Lemon BD, Tjian R (2001) Transcriptional coactivator complexes. Annu Rev Biochem 70:475-501. doi: 10.1146/annurev.biochem.70.1.475
Nagore LI, Nadeau RJ, Guo Q, Jadhav YLA, Jarrett HW, Haskins WE (2013) Purification and characterization of transcription factors. Mass Spectrom Rev 32:386-398. doi: 10.1002/mas.21369
Narlikar L and Ovcharenko I (2009) Identifying regulatory elements in eukaryotic genomes. Brief Funct Genomic Proteomic 8:215-230. doi: 10.1093/bfgp/elp014
Nolis IK, McKay DJ, Mantouvalou E, Lomvardas S, Merika M, Thanos D (2009) Transcription factors mediate long-range enhancer–promoter interactions. Proc Natl Acad Sci U S A 106:20222-20227. doi: 10.1073/pnas.0902454106
Nunberg AN, Li Z, Bogue MA, Vivekananda J, Reddy AS, Thomas TL (1994) Developmental and hormonal regulation of sunflower helianthinin genes: proximal promoter sequences confer regionalized seed expression. Plant Cell 6:473-486. doi: 10.1105/tpc.6.4.473
Ochiai H, Sakamoto N, Momiyama A, Akasaka K, Yamamoto T (2008) Analysis of cis-regulatory elements controlling spatio-temporal expression of T-brain gene in sea urchin, Hemicentrotus pulcherrimus. Mech Dev 125:2-17. doi: 10.1016/j.mod.2007.10.009
Ogbourne S and Antalis TM (1998) Transcriptional control and the role of silencers in transcriptional regulation in eukaryotes. Biochem J 331:1-14. doi: 10.1042/bj3310001
Puente P, Wei N, Deng XW (1996) Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J. 15:3732–3743.
Raab JR and Kamakaka RT (2010) Insulators and promoters: closer than we think. Nat Rev Genet 11:439-446. doi: 10.1038/nrg2765
Ranjan A, Ansari, SA, Srivastava R, Mantri S, Asif MH Sawant SV, Tuli R (2009) A T9G mutation in the prototype TATA-box TCACTATATATAG determines nucleosome formation and synergy with upstream activator sequences in plant promoters. Plant Physiol 151: 2174-2186. doi: 10.1104/pp.109.148064
Sawant SV, Kiran K, Mehrotra R, Chaturvedi CP, Ansari SA, Singh P, Lodhi N, Tuli R (2005) A variety of synergistic and antagonistic interactions mediated by cis-acting DNA motifs regulate gene expression in plant cells and modulate stability of the transcription complex formed on a basal promoter. J Exp Bot 56:2345-2353. doi: 10.1093/jxb/eri227
Schauer SE, Schlüter PM, Baskar R, Gheyselinck J, Bolaños A, Curtis MD, Grossniklaus U (2009) Intronic regulatory elements determine the divergent expression patterns of AGAMOUS‐LIKE6 subfamily members in Arabidopsis. Plant J 59:987-1000. doi: 10.1111/j.1365-313X.2009. 03928.x
Serfling E, Jasin M, Schaffner W (1985) Enhancers and eukaryotic gene transcription. Trends Genet 1:224-230. doi:10.1016/0168-9525(85)90088-5
She W, Lin W, Zhu Y, Chen Y, Jin W, Yang Y, Han N, Bian H, Zhu M, Wang J (2010) The gypsy insulator of Drosophila melanogaster, together with its binding protein suppressor of Hairy-wing, facilitate high and precise expression of transgenes in Arabidopsis thaliana. Genetics 185:1141-1150. doi: 10.1534/genetics.110.117960
Shikata M, Takemura M, Yokota A, Kohchi T (2003) Arabidopsis ZIM, a plant-specific GATA factor, can function as a transcriptional activator. Biosci Biotechnol Biochem 67:.2495-2497. doi: 10.1271/bbb.67.2495
Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, Galjart N, de Laat W (2006) CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus. Genes Dev 20:2349-2354.
Srivastava R, Rai KM, Pandey B, Singh SP, Sawant SV (2015) Spt-Ada-Gcn5-Acetyltransferase (SAGA) complex in plants: genome wide identification, evolutionary conservation and functional determination. PloS one 10: e0134709. doi: 10.1371/journal.pone.0134709
Srivastava R, Rai, KM, Srivastava M, Kumar V, Pandey B, Singh SP, Bag SK, Singh BD, Tuli R, Sawant SV (2014) Distinct role of core promoter architecture in regulation of light-mediated responses in plant genes. Mol Plant 7:626-641. doi: 10.1093/mp/sst146
Srivastava R, Singh UM, Dubey NK (2016) Histone Modifications by different histone modifiers: insights into histone writers and erasers during chromatin modification. Journal of Biological Sciences and Medicine, 2: 45-54.
Taatjes DJ, Näär AM, Andel F, Nogales E, Tjian R (2002) Structure, function, and activator-induced conformations of the CRSP coactivator. Science 295:1058-1062. doi: 10.1126/science.1065249
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661-665. doi:10.1038/nature05960
Tilly JJ, Allen DW and Jack T (1998) The CArG boxes in the promoter of the Arabidopsis floral organ identity gene APETALA3 mediate diverse regulatory effects. Development 125:1647-1657.
Vernimmen D, De Gobbi M, Sloane‐Stanley JA, Wood WG, Higgs DR (2007) Long‐range chromosomal interactions regulate the timing of the transition between poised and active gene expression. EMBO J 26:2041-2051. doi: 10.1038/sj.emboj.7601654
Walhout AJ (2006) Unraveling transcription regulatory networks by protein–DNA and protein–protein interaction mapping. Genome Res 16:1445-1454. doi: 10.1101/gr.5321506
Wang S, Chang Y, Guo J, Zeng Q, Ellis BE, Chen JG (2011) Arabidopsis ovate family proteins, a novel transcriptional repressor family, control multiple aspects of plant growth and development. PLoS One 6:e23896. doi: 10.1371/journal.pone.0023896
Wittkopp PJ and Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nature Rev Genet 1:59-69. doi:10.1038/nrg3095
Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evo. 20:1377-419. doi: 10.1093/molbev/msg140
Wright KJ, Marr MT, Tjian R (2006) TAF4 nucleates a core subcomplex of TFIID and mediates activated transcription from a TATA-less promoter. Proc Natl Acad Sci U S A 103:12347-12352. doi: 10.1073/pnas.0605499103
Yamamoto YY, Ichida H, Abe T, Suzuki Y, Sugano S, Obokata J (2007) Differentiation of core promoter architecture between plants and mammals revealed by LDSS analysis. Nucleic Acids Res 35:6219-6226. doi: 10.1093/nar/gkm685
Yamamoto YY, Yoshitsugu T, Sakurai T, Seki M, Shinozaki K, Obokata J (2009) Heterogeneity of Arabidopsis core promoters revealed by high‐density TSS analysis. Plant J 60:350-362. doi: 10.1111/j.1365-313X.2009. 03958.x
Yanagisawa S (2001) The transcriptional activation domain of the plant-specific Dof1 factor functions in plant, animal, and yeast cells. Plant Cell Physiol 42:813-822. doi: 10.1093/pcp/pce105
Yang W, Jefferson RA, Huttner E, Moore JM, Gagliano WB, Grossniklaus U (2005) An egg apparatus-specific enhancer of Arabidopsis, identified by enhancer detection. Plant Physiol 139:1421-1432. doi: 10.1104/pp.105.068262
Yilmaz A, Mejia-Guerra MK, Kurz K, Liang X, Welch L, Grotewold E (2011) AGRIS: the Arabidopsis gene regulatory information server, an update. Nucleic Acids Res 39:1118-1122. doi: 10.1093/nar/gkq1120
Zhang Y, Fan W, Kinkema M, Li X, Dong X (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci U S A 96:6523-6528. doi: 10.1073/pnas.96.11.6523
Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol Plant Microbe Interact 13:191-202. doi: 10.1094/MPMI.2000.13.2.191
Copyright (c) 2016 Yadav et al.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).