Transcript elongation by RNA polymerase II in plants: factors, regulation and impact on gene expression.
Arabidopsis
Chromatin
FACT
PAF1C
PELF1
RNA polymerase II
SPT4-SPT5
SPT6
TFIIS
nucleosome
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
26 Jan 2023
26 Jan 2023
Historique:
revised:
12
01
2023
received:
19
12
2022
accepted:
17
01
2023
pubmed:
28
1
2023
medline:
28
1
2023
entrez:
27
1
2023
Statut:
aheadofprint
Résumé
Transcriptional elongation by RNA polymerase II (RNAPII) through chromatin is a dynamic and highly regulated step of eukaryotic gene expression. A combination of transcript elongation factors (TEFs) including modulators of RNAPII activity and histone chaperones facilitate efficient transcription on nucleosomal templates. Biochemical and genetic analyses, primarily performed in Arabidopsis, provided insight into the contribution of TEFs to establish gene expression patterns during plant growth and development. In addition to summarising the role of TEFs in plant gene expression, we emphasise in our review recent advances in the field. Thus, mechanisms are presented how aberrant intragenic transcript initiation is suppressed by repressing transcriptional start sites within coding sequences. We also discuss how transcriptional interference of ongoing transcription with neighbouring genes is prevented. Moreover, it appears that plants make no use of promoter-proximal RNAPII pausing in the way mammals do, but there are nucleosome-defined mechanism(s) that determine the efficiency of mRNA synthesis by RNAPII. Accordingly, a still growing number of processes related to plant growth, development and responses to changing environmental conditions prove to be regulated at the level of transcriptional elongation.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : Gr1159/16-1
Organisme : Deutsche Forschungsgemeinschaft
ID : SFB960/A6
Informations de copyright
© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Antosz, W., Deforges, J., Begcy, K., Bruckmann, A., Poirier, Y., Dresselhaus, T. et al. (2020) Critical role of transcript cleavage in Arabidopsis RNA polymerase II transcriptional elongation. Plant Cell, 32, 1449-1463.
Antosz, W., Pfab, A., Ehrnsberger, H.F., Holzinger, P., Köllen, K., Mortensen, S.A. et al. (2017) The composition of the Arabidopsis RNA polymerase II transcript elongation complex reveals the interplay between elongation and mRNA processing factors. Plant Cell, 29, 854-870.
Bellegarde, F., Maghiaoui, A., Boucherez, J., Krouk, G., Lejay, L., Bach, L. et al. (2019) The chromatin factor HNI9 and ELONGATED HYPOCOTYL5 maintain ROS homeostasis under high nitrogen provision. Plant Physiology, 180, 582-592.
Brkljacic, J. & Grotewold, E. (2017) Combinatorial control of plant gene expression. Biochimica et Biophysica Acta, 1860, 31-40.
Chen, C., Shu, J., Li, C., Thapa, R.K., Nguyen, V., Yu, K. et al. (2019) RNA polymerase II-independent recruitment of SPT6L at transcription start sites in Arabidopsis. Nucleic Acids Research, 47, 6714-6725.
Chen, D. & Lei, E.P. (2019) Function and regulation of chromatin insulators in dynamic genome organization. Current Opinion in Cell Biology, 58, 61-68.
Chen, F.X., Smith, E.R. & Shilatifard, A. (2018) Born to run: control of transcription elongation by RNA polymerase II. Nature Reviews. Molecular Cell Biology, 19, 464-478.
Core, L. & Adelman, K. (2019) Promoter-proximal pausing of RNA polymerase II: a nexus of gene regulation. Genes & Development, 33, 960-982.
Decker, T.-M. (2021) Mechanisms of transcription elongation factor DSIF (Spt4-Spt5). Journal of Molecular Biology, 433, 166657.
Diego-Martin, B., Pérez-Alemany, J., Candela-Ferre, J., Corbalán-Acedo, A., Pereyra, J., Alabadí, D. et al. (2022) The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and transcription start site determination in Arabidopsis. Nucleic Acids Research, 50, 10399-10417.
Dolata, J., Guo, Y., Kolowerzo, A., Smolinski, D., Brzyzek, G., Jarmolowski, A. et al. (2015) NTR1 is required for transcription elongation checkpoints at alternative exons in Arabidopsis. The EMBO Journal, 34, 544-558.
Dollinger, R. & Gilmour, D.S. (2021) Regulation of promoter proximal pausing of RNA polymerase II in metazoans. Journal of Molecular Biology, 433, 166897.
Duina, A.A. (2011) Histone chaperones Spt6 and FACT: similarities and differences in modes of action at transcribed genes. Genetics Research International, 2011, 625210.
Duroux, M., Houben, A., Růzicka, K., Friml, J. & Grasser, K.D. (2004) The chromatin remodelling complex FACT associates with actively transcribed regions of the Arabidopsis genome. The Plant Journal, 40, 660-671.
Dürr, J., Lolas, I.B., Sørensen, B.B., Schubert, V., Houben, A., Melzer, M. et al. (2014) The transcript elongation factor SPT4/SPT5 is involved in auxin-related gene expression in Arabidopsis. Nucleic Acids Research, 42, 4332-4347.
Ehara, H., Kujirai, T., Fujino, Y., Shirouzu, M., Kurumizaka, H. & Sekine, S.-I. (2019) Structural insight into nucleosome transcription by RNA polymerase II with elongation factors. Science, 363, 744-747.
Ehara, H., Kujirai, T., Shirouzu, M., Kurumizaka, H. & Sekine, S.-I. (2022) Structural basis of nucleosome disassembly and reassembly by RNAPII elongation complex with FACT. Science, 377, eabp9466. Available from: https://doi.org/10.1126/science.abp9466
Ehara, H., Yokoyama, T., Shigematsu, H., Yokoyama, S., Shirouzu, M. & Sekine, S.I. (2017) Structure of the complete elongation complex of RNA polymerase II with basal factors. Science, 357, 921-924.
Espinosa-Cores, L., Bouza-Morcillo, L., Barrero-Gil, J., Jiménez-Suárez, V., Lázaro, A., Piqueras, R. et al. (2020) Insights into the function of the NuA4 complex in plants. Frontiers in Plant Science, 11, 125.
Fal, K., Liu, M., Duisembekova, A., Refahi, Y., Haswell, E.S. & Hamant, O. (2017) Phyllotactic regularity requires the Paf1 complex in Arabidopsis. Development, 144, 4428-4436.
Farnung, L., Ochmann, M., Engeholm, M. & Cramer, P. (2021) Structural basis of nucleosome transcription mediated by Chd1 and FACT. Nature Structural & Molecular Biology, 28, 382-387.
Farnung, L., Ochmann, M., Garg, G., Vos, S.M. & Cramer, P. (2022) Structure of a backtracked hexasomal intermediate of nucleosome transcription. Molecular Cell, 82, 3126-3134.e7.
Feng, J. & Shen, W.H. (2014) Dynamic regulation and function of histone monoubiquitination in plants. Frontiers in Plant Science, 5, 83.
Filipovski, M., Soffers, J.H.M., Vos, S.M. & Farnung, L. (2022) Structural basis of nucleosome retention during transcription elongation. Science, 376, 1313-1316.
Fish, R.N. & Kane, C.M. (2002) Promoting elongation with transcript cleavage stimulatory factors. Biochimica et Biophysica Acta, 1577, 287-307.
Formosa, T. & Winston, F. (2020) The role of FACT in managing chromatin: disruption, assembly, or repair? Nucleic Acids Research, 48, 11929-11941.
Francette, A.M., Tripplehorn, S.A. & Arndt, K.M. (2021) The Paf1 complex: a keystone of nuclear regulation operating at the interface of transcription and chromatin. Journal of Molecular Biology, 433, 166979.
Frost, J.M., Kim, M.Y., Park, G.T., Hsieh, P.-H., Nakamura, M., Lin, S.J.H. et al. (2018) FACT complex is required for DNA demethylation at heterochromatin during reproduction in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 115, E4720-E4729.
Gamarra, N. & Narlikar, G.J. (2021) Collaboration through chromatin: motors of transcription and chromatin structure. Journal of Molecular Biology, 433, 166876.
Godoy Herz, M.A. & Kornblihtt, A.R. (2019) Alternative splicing and transcription elongation in plants. Frontiers in Plant Science, 10, 309.
Godoy Herz, M.A., Kubaczka, M.G., Brzyżek, G., Servi, L., Krzyszton, M., Simpson, C. et al. (2019) Light regulates plant alternative splicing through the control of transcriptional elongation. Molecular Cell, 73, 1066-1074.e3.
Grasser, K.D. (2020) The FACT histone chaperone: tuning gene transcription in the chromatin context to modulate plant growth and development. Frontiers in Plant Science, 11, 85.
Grasser, K.D., Rubio, V. & Barneche, F. (2021) Multifaceted activities of the plant SAGA complex. Biochimica et Biophysica Acta, 1864, 194613.
Grasser, M., Kane, C.M., Merkle, T., Melzer, M., Emmersen, J. & Grasser, K.D. (2009) Transcript elongation factor TFIIS is involved in Arabidopsis seed dormancy. Journal of Molecular Biology, 386, 598-611.
Gu, X.L., Wang, H., Huang, H. & Cui, X.F. (2012) SPT6L encoding a putative WG/GW-repeat protein regulates apical-basal polarity of embryo in Arabidopsis. Molecular Plant, 5, 249-259.
Gurova, K., Chang, H.-W., Valieva, M.E., Sandlesh, P. & Studitsky, V.M. (2018) Structure and function of the histone chaperone FACT - resolving FACTual issues. Biochimica et Biophysica Acta, 1861, 892-904.
Hajheidari, M., Koncz, C. & Eick, D. (2013) Emerging roles for RNA polymerase II CTD in Arabidopsis. Trends in Plant Science, 18, 633-643.
Harlen, K.M. & Churchman, L.S. (2017) The code and beyond: transcription regulation by the RNA polymerase II carboxy-terminal domain. Nature Reviews. Molecular Cell Biology, 18, 263-273.
Hartzog, G.A. & Fu, J. (2013) The Spt4-Spt5 complex: a multi-faceted regulator of transcription elongation. Biochimica et Biophysica Acta, 1829, 105-115.
He, X.J., Hsu, Y.F., Zhu, S., Wierzbicki, A.T., Pontes, O., Pikaard, C.S. et al. (2009) An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell, 137, 498-508.
He, Y., Doyle, M.R. & Amasino, R.M. (2004) PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes & Development, 18, 2774-2784.
Hetzel, J., Duttke, S.H., Benner, C. & Chory, J. (2016) Nascent RNA sequencing reveals distinct features in plant transcription. Proceedings of the National Academy of Sciences of the United States of America, 113, 12316-12321.
Ikeda, Y., Kinoshita, Y., Susaki, D., Ikeda, Y., Iwano, M., Takayama, S. et al. (2011) HMG domain containing SSRP1 is required for DNA demethylation and genomic imprinting in Arabidopsis. Developmental Cell, 21, 589-596.
Jaehning, J.A. (2010) The Paf1 complex: platform or player in RNA polymerase II transcription? Biochimica et Biophysica Acta, 1799, 279-388.
Jarillo, J.A. & Piñeiro, M. (2015) H2A.Z mediates different aspects of chromatin function and modulates flowering responses in Arabidopsis. The Plant Journal, 83, 96-109.
Jarosz, M., van Lijsebettens, M. & Woloszynska, M. (2020) Plant elongator-protein complex of diverse activities regulates growth, development, and immune responses. International Journal of Molecular Sciences, 21, 6912.
Jensen, G.S., Fal, K., Hamant, O. & Haswell, E.S. (2017) The RNA polymerase-associated factor 1 complex is required for plant touch responses. Journal of Experimental Botany, 68, 499-511.
Jeronimo, C., Collin, P. & Robert, F. (2016) The RNA polymerase II CTD: the increasing complexity of a low-complexity protein domain. Journal of Molecular Biology, 428, 2607-2622.
Jonkers, I. & Lis, J.T. (2015) Getting up to speed with transcription elongation by RNA polymerase II. Nature Reviews. Molecular Cell Biology, 16, 167-177.
Joo, Y.J., Ficarro, S.B., Chun, Y., Marto, J.A. & Buratowski, S. (2019) In vitro analysis of RNA polymerase II elongation complex dynamics. Genes & Development, 33, 578-589.
Kato, H., Okazaki, K. & Urano, T. (2013) Spt6: two fundamentally distinct functions in the regulation of histone modification. Epigenetics, 8, 1249-1253.
Kettenberger, H., Armache, K.-J. & Cramer, P. (2003) Architecture of the RNA polymerase II-TFIIS complex and implications for mRNA cleavage. Cell, 114, 347-357.
Kindgren, P., Ivanov, M. & Marquardt, S. (2020) Native elongation transcript sequencing reveals temperature dependent dynamics of nascent RNAPII transcription in Arabidopsis. Nucleic Acids Research, 48, 2332-2347.
Kireeva, M.L., Hancock, B., Cremona, G.H., Walter, W., Studitsky, V.M. & Kashlev, M. (2005) Nature of nucleosomal barrier to RNA polymerase II. Molecular Cell, 18, 108.
Köllen, K., Dietz, L., Bies-Etheve, N., Lagrange, T., Grasser, M. & Grasser, K.D. (2015) The zinc-finger protein SPT4 interacts with SPT5L/KTF1 and modulates transcriptional silencing in Arabidopsis. FEBS Letters, 589, 3254-3257.
Kornberg, R.D. & Lorch, Y. (2020) Primary role of the nucleosome. Molecular Cell, 79, 371-375.
Krogan, N.J., Kim, M., Ahn, S.H., Zhong, G., Kobor, M.S., Cagney, G. et al. (2002) RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Molecular Cell Biology, 22, 6979-6992.
Kujirai, T. & Kurumizaka, H. (2020) Transcription through the nucleosome. Current Opinion in Structural Biology, 61, 42-49.
Kwak, H. & Lis, J.T. (2013) Control of transcriptional elongation. Annual Reviews of Genetics, 47, 483-508.
Lai, W.K.M. & Pugh, B.F. (2017) Understanding nucleosome dynamics and their links to gene expression and DNA replication. Nature Reviews. Molecular Cell Biology, 18, 548-562.
Layat, E., Bourcy, M., Cotterell, S., Zdzieszyńska, J., Desset, S., Duc, C. et al. (2021) The histone chaperone HIRA is a positive regulator of seed germination. International Journal of Molecular Sciences, 22, 4031.
Lei, B. & Berger, F. (2020) H2A variants in Arabidopsis: versatile regulators of genome activity. Plant Communications, 1, 100015.
Leng, X., Ivanov, M., Kindgren, P., Malik, I., Thieffry, A., Brodersen, P. et al. (2020) Organismal benefits of transcription speed control at gene boundaries. EMBO Reports, 21, e49315.
Leng, X., Thomas, Q., Rasmussen, S.H. & Marquardt, S. (2020) A G(enomic)P(ositioning)S(ystem) for plant RNAPII transcription. Trends in Plant Science, 25, 744-764.
Li, L., Ye, H., Guo, H. & Yin, Y. (2010) Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proceedings of the National Academy of Sciences of the United States of America, 107, 3918-3923.
Lindstrom, D.L., Squazzo, S.L., Muster, N., Burckin, T.A., Wachter, K.C., Emigh, C.A. et al. (2003) Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5-associated proteins. Molecular Cell Biology, 23, 1368-1378.
Liu, M., Zhu, J. & Dong, Z. (2021) Immediate transcriptional responses of Arabidopsis leaves to heat shock. Journal of Integrative Plant Biology, 63, 468-483.
Liu, Y., Geyer, R., van Zanten, M., Carles, A., Li, Y., Hörold, A. et al. (2011) Identification of the Arabidopsis REDUCED DORMANCY 2 gene uncovers a role for the polymerase associated factor 1 complex in seed dormancy. PLoS One, 6, e22241.
Liu, Y., Zhou, K., Zhang, N., Wei, H., Tan, Y.Z., Zhang, Z. et al. (2020) FACT caught in the act of manipulating the nucleosome. Nature, 577, 426-431.
Lolas, I.B., Himanen, K., Grønlund, J.T., Lynggaard, C., Houben, A., Melzer, M. et al. (2010) The transcript elongation factor FACT affects Arabidopsis vegetative and reproductive development and genetically interacts with HUB1/2. The Plant Journal, 61, 686-697.
Ma, Y., Gil, S., Grasser, K.D. & Mas, P. (2018) Targeted recruitment of the basal transcriptional machinery by LNK clock components controls the circadian rhythms of nascent RNAs in Arabidopsis. Plant Cell, 30, 907-924.
Markusch, H., Michl-Holzinger, P., Obermeyer, S., Thorbecke, C., Bruckmann, A., Babl, S. et al. (2023) ELF1 is a component of the Arabidopsis RNA polymerase II elongation complex and associates with a subset of transcribed genes. The New Phytologist. Available from: https://doi.org/10.1111/NPH.18724
Marquardt, S., Petrillo, E. & Manavella, P.A. (2023) Cotranscriptional RNA processing and modification in plants. Plant Cell. Available from: https://doi.org/10.1093/plcell/koac309
Mayer, A., Lidschreiber, M., Siebert, M., Leike, K., Söding, J. & Cramer, P. (2010) Uniform transitions of the general RNA polymerase II transcription complex. Nature Structural & Molecular Biology, 17, 1272-1278.
Michl-Holzinger, P., Mortensen, S.A. & Grasser, K.D. (2019) The SSRP1 subunit of the histone chaperone FACT is required for seed dormancy in Arabidopsis. Journal of Plant Physiology, 236, 105-108.
Michl-Holzinger, P., Obermeyer, S., Markusch, H., Pfab, A., Ettner, A., Bruckmann, A. et al. (2022) Phosphorylation of the FACT histone chaperone subunit SPT16 affects chromatin at RNA polymerase II transcriptional start sites in Arabidopsis. Nucleic Acids Research, 50, 5014-5028.
Mortensen, S.A. & Grasser, K.D. (2014) The seed dormancy defect of Arabidopsis mutants lacking the transcript elongation factor TFIIS is caused by reduced expression of the DOG1 gene. FEBS Letters, 588, 47-51.
Muniz, L., Nicolas, E. & Trouche, D. (2021) RNA polymerase II speed: a key player in controlling and adapting transcriptome composition. The EMBO Journal, 40, e105740.
Nasim, Z., Susila, H., Jin, S., Youn, G. & Ahn, J.H. (2022) Polymerase II-associated factor 1 complex-regulated FLOWERING LOCUS C-clade genes repress flowering in response to chilling. Frontiers in Plant Science, 13, 817356.
Nielsen, M., Ard, R., Leng, X., Ivanov, M., Kindgren, P., Pelechano, V. et al. (2019) Transcription-driven chromatin repression of intragenic transcription start sites. PLoS Genetics, 15, e1007969.
Nock, A., Ascano, J.M., Barrero, M.J. & Malik, S. (2012) Mediator-regulated transcription through the +1 nucleosome. Molecular Cell, 48, 837-848.
Noe Gonzalez, M., Blears, D. & Svejstrup, J.Q. (2021) Causes and consequences of RNA polymerase II stalling during transcript elongation. Nature Reviews. Molecular Cell Biology, 22, 3-21.
Obermeyer, S., Stöckl, R., Schnekenburger, T., Kapoor, H., Stempfl, T., Schwartz, U. et al. (2023) TFIIS is crucial during early transcript elongation for transcriptional reprogramming in response to heat stress. Journal of Molecular Biology, 435, 167917.
Obermeyer, S., Stöckl, R., Schnekenburger, T., Moehle, C., Schwartz, U. & Grasser, K.D. (2022) Distinct role of subunits of the Arabidopsis RNA polymerase II elongation factor PAF1C in transcriptional reprogramming. Frontiers in Plant Science, 13, 974625.
Oh, S., Zhang, H., Ludwig, P. & van Nocker, S. (2004) A mechanism related to the yeast transcriptional regulator Paf1c is required for expression of the Arabidopsis FLC/MAF MADS box gene family. Plant Cell, 16, 2940-2953.
Osakabe, A., Lorkovic, Z.J., Kobayashi, W., Tachiwana, H., Yelagandula, R., Kurumizaka, H. et al. (2018) Histone H2A variants confer specific properties to nucleosomes and impact on chromatin accessibility. Nucleic Acids Research, 46, 7675-7685.
Osman, S. & Cramer, P. (2020) Structural biology of RNA polymerase II transcription: 20 years on. Annual Review of Cell and Development Biology, 36, 1-34.
Park, S., Oh, S., Ek-Ramos, J. & van Nocker, S. (2010) PLANT HOMOLOGOUS TO PARAFIBROMIN is a component of the PAF1 complex and assists in regulating expression of genes within H3K27ME3-enriched chromatin. Plant Physiology, 153, 821-831.
Perales, M. & Más, P. (2007) A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell, 19, 2111-2123.
Pfab, A., Breindl, M. & Grasser, K.D. (2018) The Arabidopsis histone chaperone FACT is required for stress-induced expression of anthocyanin biosynthetic genes. Plant Molecular Biology, 96, 367-374.
Prather, D., Krogan, N.J., Emili, A., Greenblatt, J.F. & Winston, F. (2005) Identification and characterization of Elf1, a conserved transcription elongation factor in Saccharomyces cerevisiae. Molecular Cell Biology, 25, 10122-10135.
Probst, A.V., Desvoyes, B. & Gutierrez, C. (2020) Similar yet critically different: the distribution, dynamics and function of histone variants. Journal of Experimental Botany, 71, 5191-5204.
Qin, Y., Long, Y. & Zhai, J. (2022) Genome-wide characterization of nascent RNA processing in plants. Current Opinion in Plant Biology, 69, 102294.
Reiter, F., Wienerroither, S. & Stark, A. (2017) Combinatorial function of transcription factors and cofactors. Current Opinion in Genetics & Development, 43, 73-81.
Rossi, M.J., Kuntala, P.K., Lai, W.K.M., Yamada, N., Badjatia, N., Mittal, C. et al. (2021) A high-resolution protein architecture of the budding yeast genome. Nature, 592, 309-314.
Schoborg, T. & Labrador, M. (2014) Expanding the roles of chromatin insulators in nuclear architecture, chromatin organization and genome function. Cellular and Molecular Life Sciences, 71, 4089-4113.
Sdano, M.A., Fulcher, J.M., Palani, S., Chandrasekharan, M.B., Parnell, T.J., Whitby, F.G. et al. (2017) A novel SH2 recognition mechanism recruits Spt6 to the doubly phosphorylated RNA polymerase II linker at sites of transcription. eLife, 6, e28723.
Shu, J., Ding, N., Liu, J., Cui, Y. & Chen, C. (2022) Transcription elongator SPT6L regulates the occupancies of the SWI2/SNF2 chromatin remodelers SYD/BRM and nucleosomes at transcription start sites in Arabidopsis. Nucleic Acids Research, 50, 12754-12767.
Sims, R.J., Belotserkovskaya, R. & Reinberg, D. (2004) Elongation by RNA polymerase II: the short and long of it. Genes & Development, 18, 2437-2468.
Song, A. & Chen, F.X. (2022) The pleiotropic roles of SPT5 in transcription. Transcription, 13, 53-69.
Squazzo, S.L., Costa, P.J., Lindstrom, D.L., Kumer, K.E., Simic, R., Jennings, J.L. et al. (2002) The Paf complex physically and functionally associates with transcription elongation factors in vivo. The EMBO Journal, 21, 1764-1174.
Sullivan, A., Purohit, P.K., Freese, N.H., Pasha, A., Esteban, E., Waese, J. et al. (2019) An ‘eFP-Seq Browser’ for visualizing and exploring RNA sequencing data. The Plant Journal, 100, 641-654.
Szádeczky-Kardoss, I., Szaker, H.M., Verma, R., Darkó, É., Pettkó-Szandtner, A., Silhavy, D. et al. (2022) Elongation factor TFIIS is essential for heat stress adaptation in plants. Nucleic Acids Research, 50, 1927-1950.
Talbert, P.B. & Henikoff, S. (2017) Histone variants on the move: substrates for chromatin dynamics. Nature Reviews. Molecular Cell Biology, 18, 115-126.
Thieffry, A., Vigh, M.L., Bornholdt, J., Ivanov, M., Brodersen, P. & Sandelin, A. (2020) Characterization of Arabidopsis thaliana promoter Bidirectionality and antisense RNAs by inactivation of nuclear RNA decay pathways. Plant Cell, 32, 1845-1867.
Thomas, Q.A., Ard, R., Liu, J., Li, B., Wang, J., Pelechano, V. et al. (2020) Transcript isoform sequencing reveals widespread promoter-proximal transcriptional termination in Arabidopsis. Nature Communications, 11, 2589.
van Lijsebettens, M. & Grasser, K.D. (2014) Transcript elongation factors: shaping transcriptomes after transcript initiation. Trends in Plant Science, 19, 717-726.
Venkatesh, S. & Workman, J.L. (2015) Histone exchange, chromatin structure and the regulation of transcription. Nature Reviews. Molecular Cell Biology, 16, 178-189.
Vos, S.M., Farnung, L., Boehning, M., Wigge, C., Linden, A., Urlaub, H. et al. (2018) Structure of activated transcription complex pol II-DSIF-PAF-SPT6. Nature, 560, 607-612.
Vos, S.M., Farnung, L., Linden, A., Urlaub, H. & Cramer, P. (2020) Structure of complete pol II-DSIF-PAF-SPT6 transcription complex reveals RTF1 allosteric activation. Nature Structural & Molecular Biology, 27, 668-677.
Wang, X., Chen, J., Xie, Z., Liu, S., Nolan, T., Ye, H. et al. (2014) Histone lysine methyltransferase SDG8 is involved in brassinosteroid-regulated gene expression in Arabidopsis thaliana. Molecular Plant, 7, 1303-1315.
Widiez, T., El Kafafi, S., Girin, T., Berr, A., Ruffel, S., Krouk, G. et al. (2011) High nitrogen insensitive 9 (HNI9)-mediated systemic repression of root NO3- uptake is associated with changes in histone methylation. Proceedings of the National Academy of Sciences of the United States of America, 108, 13329-13334.
Wu, Z., Ietswaart, R., Liu, F., Yang, H., Howard, M. & Dean, C. (2016) Quantitative regulation of FLC via coordinated transcriptional initiation and elongation. Proceedings of the National Academy of Sciences of the United States of America, 113, 218-223.
Xiao, J., Lee, U.S. & Wagner, D. (2016) Tug of war: adding and removing histone lysine methylation in Arabidopsis. Current Opinion in Plant Biology, 34, 41-53.
Yu, X., Martin, P.G.P. & Michaels, S.D. (2019) BORDER proteins protect expression of neighboring genes by promoting 3′ pol II pausing in plants. Nature Communications, 10, 4359.
Yu, X., Martin, P.G.P., Zhang, Y., Trinidad, J.C., Xu, F., Huang, J. et al. (2021) The BORDER family of negative transcription elongation factors regulates flowering time in Arabidopsis. Current Biology, 31, 5377-5384.e5.
Yu, X. & Michaels, S.D. (2010) The Arabidopsis Paf1c complex component CDC73 participates in the modification of FLOWERING LOCUS C chromatin. Plant Physiology, 153, 1074-1084.
Zhang, H., Li, X., Song, R., Zhan, Z., Zhao, F., Li, Z. et al. (2022) Cap-binding complex assists RNA polymerase II transcription in plant salt stress response. Plant, Cell & Environment, 45, 2780-2793.
Zhang, H., Ransom, C., Ludwig, P. & van Nocker, S. (2003) Genetic analysis of early flowering mutants in Arabidopsis defines a class of pleiotropic developmental regulator required for expression of the flowering-time switch flowering locus C. Genetics, 164, 347-358.
Zhang, H. & van Nocker, S. (2002) The VERNALIZATION INDEPENDENCE 4 gene encodes a novel regulator of FLOWERING LOCUS C. The Plant Journal, 31, 663-673.
Zhong, Z., Wang, Y., Wang, M., Yang, F., Thomas, Q.A., Xue, Y. et al. (2022) Histone chaperone ASF1 mediates H3.3-H4 deposition in Arabidopsis. Nature Communications, 13, 6970.
Zhu, J., Liu, M., Liu, X. & Dong, Z. (2018) RNA polymerase II activity revealed by GRO-seq and pNET-seq in Arabidopsis. Nature Plants, 4, 1112-1123.