Research progress of the Elongator complex in plant

Authors

  • Ji XIANGZHUO Gansu Agricultural University, College of Agronomy, Lanzhou 730070; Gansu Agricultural University, Gansu Provincial Key Lab of Arid Land Crop Science, Lanzhou 730070; Gansu Agricultural University, Gansu Key Lab of Crop Improvement & Germplasm Enhancement, Lanzhou 730070 (CN)
  • Zhuang ZELONG Gansu Agricultural University, College of Agronomy, Lanzhou 730070; Gansu Agricultural University, Gansu Provincial Key Lab of Arid Land Crop Science, Lanzhou 730070; Gansu Agricultural University, Gansu Key Lab of Crop Improvement & Germplasm Enhancement, Lanzhou 730070 (CN)
  • Wang YINXIA Gansu Agricultural University, College of Agronomy, Lanzhou 730070; Gansu Agricultural University, Gansu Provincial Key Lab of Arid Land Crop Science, Lanzhou 730070; Gansu Agricultural University, Gansu Key Lab of Crop Improvement & Germplasm Enhancement, Lanzhou 730070 (CN)
  • Zhang YUNFANG Gansu Agricultural University, College of Agronomy, Lanzhou 730070; Gansu Agricultural University, Gansu Provincial Key Lab of Arid Land Crop Science, Lanzhou 730070; Gansu Agricultural University, Gansu Key Lab of Crop Improvement & Germplasm Enhancement, Lanzhou 730070 (CN)
  • Peng YUNLING Gansu Agricultural University, College of Agronomy, Lanzhou 730070; Gansu Agricultural University, Gansu Provincial Key Lab of Arid Land Crop Science, Lanzhou 730070; Gansu Agricultural University, Gansu Key Lab of Crop Improvement & Germplasm Enhancement, Lanzhou 730070 (CN)

DOI:

https://doi.org/10.15835/nbha51113058

Keywords:

DNA methylation, Elongator complex, histone acetylation, RNA polymerase II, tRNA modification

Abstract

The Elongator complex consists of six subunits (ELP1-ELP6), where ELP1-ELP3 forms the core subcomplex and ELP4-ELP6 forms the auxiliary subcomplex. Deletion of any of the six subunits results in an almost identical phenotype, suggesting that all six subunits are essential for cellular function. All six subunits are evolutionarily conserved in terms of sequence and their interactions with other subunits. The most striking features are the structural conservation of the protein complexes and the phenotypic similarity caused by loss-of-function mutations in any protein subunit. Similar to elongation factors in translation, there is a strong interaction between the Elongator complex and RNA polymerase II during transcription. The Elongator complex is also involved in a variety of cellular pathways, including histone modification/acetylation, DNA methylation, tRNA nucleoside modification, etc. Here, we summarized the functions and mechanisms of the Elongator complex in plant growth and development, molecular pathways, and gene regulation. In this way, we aimed to provide a reference for an in-depth study of the Elongator complex.

References

Abbassi NE, Biela A, Glatt S, Lin TY (2020). How elongator acetylates tRNA bases. International Journal of Molecular Sciences 21(21):8209. https://doi.org/10.3390/ijms21218209

Abdel-Fattah W, Jablonowski D, Di Santo R, Thuring KL, Scheidt V, Hammermeister A, Stark MJ (2015). Phosphorylation of Elp1 by Hrr25 is required for elongator-dependent tRNA modification in yeast. PLoS Genetics 11(1):e1004931. https://doi.org/10.1371/journal.pgen.1004931

Bauer F, Matsuyama A, Candiracci J, Dieu M, Scheliga J, Wolf DA, Hermand D (2012). Translational control of cell division by Elongator. Cell Reports 1(5):424-433. https://doi.org/10.1016/j.celrep.2012.04.001

Chen C, Huang B, Eliasson M, Ryden P, Bystrom AS (2011). Elongator complex influences telomeric gene silencing and DNA damage response by its role in wobble uridine tRNA modification. PLoS Genetics 7(9):e1002258. https://doi.org/10.1371/journal.pgen.1002258

Chen Z, Zhang H, Jablonowski D, Zhou X, Ren X, Hong X, Gong Z (2006). Mutations in ABO1/ELO2, a subunit of Holo-Elongator, increase abscisic acid sensitivity and drought tolerance in Arabidopsis thaliana. Molecular and Cellular Biology 26(18):6902-6912. https://doi.org/10.1128/MCB.00433-06

Creppe C, Malinouskaya L, Volvert ML, Gillard M, Close P, Malaise O, Nguyen L (2009). Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 136(3):551-564. https://doi.org/10.1016/j.cell.2008.11.043

Dalwadi U, Yip, CK (2018). Structural insights into the function of Elongator. Cellular and Molecular Life Sciences 75(9):1613-1622. https://doi.org/10.1007/s00018-018-2747-6

Dauden MI, Jaciuk M, Weis F, Lin TY, Kleindienst C, Abbassi N, Glatt S (2019). Molecular basis of tRNA recognition by the Elongator complex. Science Advances 5(7):w2326. https://doi.org/10.1126/sciadv.aaw2326

Dauden MI, Kosinski J, Kolaj-Robin O, Desfosses A, Ori A, Faux C, Muller CW (2017). Architecture of the yeast Elongator complex. EMBO Reports 18(2):264-279. https://doi.org/10.15252/embr.201643353

DeFraia CT, Zhang X, Mou Z (2010). Elongator subunit 2 is an accelerator of immune responses in Arabidopsis thaliana. Plant Journal 64(3):511-523. https://doi.org/10.1111/j.1365-313X.2010.04345.x

Esberg A, Huang B, Johansson MJO, Byström AS (2006). Elevated levels of two tRNA species bypass the requirement for Elongator complex in transcription and exocytosis. Molecular Cell 24(1):39-148. https://doi.org/10.1016/j.molcel.2006.07.031

Falcone A, Nelissen H, Fleury D, Van Lijsebettens M, Bitonti MB (2007). Cytological Investigations of the Arabidopsis thaliana elo1 mutant give new insights into leaf lateral growth and elongator function. Annals of Botany 100(2):261-270. https://doi.org/10.1093/aob/mcm102

Fang X, Cui Y, Li Y, Qi Y (2015a). Transcription and processing of primary microRNAs are coupled by Elongator complex in Arabidopsis. Nature Plants 1:15075. https://doi.org/10.1038/nplants.2015.75

Fellows J, Erdjument-Bromage H, Tempst P, Svejstrup JQ (2000). The Elp2 subunit of elongator and elongating RNA polymerase II holoenzyme is a WD40 repeat protein. Journal of Biological Chemistry 275(17):12896-12899. https://doi.org/10.1074/jbc.275.17.12896

Fernandez-Vazquez J, Vargas-Perez I, Sanso M, Buhne K, Carmona M, Paulo E, Hidalgo E (2013). Modification of tRNA(Lys) UUU by elongator is essential for efficient translation of stress mRNAs. PLoS Genetics 9(7):e1003647. https://doi.org/10.1371/journal.pgen.1003647

Fichtner L, Frohloff F, Bürkner K, Larsen M, Breunig KD, Schaffrath R (2002). Molecular analysis of KTI12/TOT4, a Saccharomyces cerevisiae gene required for Kluyveromyces lactis zymocin action. Molecular Microbiology 43(3):783-791. https://doi.org/10.1046/j.1365-2958.2002.02794.x

Fichtner L, Frohloff F, Jablonowski D, Stark MJ, Schaffrath R (2002). Protein interactions within Saccharomyces cerevisiae Elongator, a complex essential for Kluyveromyces lactis zymocicity. Molecular Microbiology 45(3):817-826. https://doi.org/10.1046/j.1365-2958.2002.03055.x

Fichtner L, Jablonowski D, Schierhorn A, Kitamoto HK, Starkm MJR, Schaffrath R (2003). Elongator's toxin-target (TOT) function is nuclear localization sequence dependent and suppressed by post-translational modification. Molecular Microbiology 49(5):1297-1307. https://doi.org/10.1046/j.1365-2958.2003.03632.x

Fichtner L, Schaffrath R (2002). KTI11 and KTI13, Saccharomyces cerevisiae genes controlling sensitivity to G1 arrest induced by Kluyveromyces lactis zymocin. Molecular Microbiology 44(3):865-875. https://doi.org/10.1046/j.1365-2958.2002.02928.x

Frohloff F (2001). Saccharomyces cerevisiae Elongator mutations confer resistance to the Kluyveromyces lactis zymocin. The EMBO Journal 20(8):1993-2003. https://doi.org/10.1093/emboj/20.8.1993

Huang B (2005). An early step in wobble uridine tRNA modification requires the Elongator complex. RNA 11(4):424-436. https://doi.org/10.1261/rna.7247705

Huang B, Lu J, Bystrom AS (2008). A genome-wide screen identifies genes required for formation of the wobble nucleoside 5-methoxycarbonylmethyl-2-thiouridine in Saccharomyces cerevisiae. RNA 14(10):2183-2194. https://doi.org/10.1261/rna.1184108

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(18):6912. https://doi.org/10.3390/ijms21186912

Jia Y, Tian H, Li H, Yu Q, Wang L, Friml J, Ding Z (2015). The Arabidopsis thaliana elongator complex subunit 2 epigenetically affects root development. Journal of Experimental Botany 66(15):4631-4642. https://doi.org/10.1093/jxb/erv230

Karlsborn T, Tukenmez H, Mahmud AK, Xu F, Xu H, Bystrom AS (2014). Elongator, a conserved complex required for wobble uridine modifications in eukaryotes. RNA Biology 11(12):1519-1528. https://doi.org/10.4161/15476286.2014.992276

Kojima S, Iwasaki M, Takahashi H, Imai T, Matsumura Y, Fleury D, Machida C (2011). Asymmetric leaves2 and Elongator, a histone acetyltransferase complex, mediate the establishment of polarity in leaves of Arabidopsis thaliana. Plant Cell Physiology 52(8):1259-1273. https://doi.org/10.1093/pcp/pcr083

Leitner J, Retzer K, Malenica N, Bartkeviciute R, Lucyshyn D, Jager G, Luschnig C (2015). Meta-regulation of Arabidopsis auxin responses depends on tRNA maturation. Cell Reports 11(4):516-526. https://doi.org/10.1016/j.celrep.2015.03.054

Li Q, Fazly AM, Zhou H, Huang S, Zhang Z, Stillman B (2009). The elongator complex interacts with PCNA and modulates transcriptional silencing and sensitivity to DNA damage agents. PLoS Genetics 5(10):e1000684. https://doi.org/10.1371/journal.pgen.1000684

Lin FJ, Shen L, Jang CW, Falnes PO, ZhangY (2013). Ikbkap/Elp1 deficiency causes male infertility by disrupting meiotic progression. PLoS Genetics 9(5):e1003516. https://doi.org/10.1371/journal.pgen.1003516

Lin Z, Zhao W, Diao W, Xie X, Wang Z, Zhang J, Long J (2012). Crystal Structure of Elongator Subcomplex Elp4–6. Journal of Biological Chemistry 287(25):21501-21508. https://doi.org/10.1074/jbc.M112.341560

Lu J, Huang B, Esberg A, Johansson MJ, Bystrom AS (2005). The Kluyveromyces lactis gamma-toxin targets tRNA anticodons. RNA 11(11):1648-1654. https://doi.org/10.1261/rna.2172105

Matsumoto H, Yasui Y, Ohmori Y, Tanaka W, Ishikawa T, Numa H, Hirano HY (2020). CURLED LATER1 encoding the largest subunit of the Elongator complex has a unique role in leaf development and meristem function in rice. The Plant Journal 104(2):351-364. https://doi.org/10.1111/tpj.14925

Mehlgarten C, Jablonowski D, Breunig KD, Stark MJ, Schaffrath R (2009). Elongator function depends on antagonistic regulation by casein kinase Hrr25 and protein phosphatase Sit4. Molecular Microbiology 73(5):869-881. https://doi.org/10.1111/j.1365-2958.2009.06811.x

Mehlgarten C, Jablonowski D, Wrackmeyer U, Tschitschmann S, Sondermann D, Jäger G, Breunig KD (2010). Elongator function in tRNA wobble uridine modification is conserved between yeast and plants. Molecular Microbiology 76(5):1082-1094. https://doi.org/10.1111/j.1365-2958.2010.07163.x

Mehlgarten C, Schaffrath R (2003). Mutant casein kinase I (Hrr25p/Kti14p) abrogates the G1 cell cycle arrest induced by Kluyveromyces lactis zymocin in budding yeast. Molecular Genetics and Genomics 269(2):188-196. https://doi.org/10.1007/s00438-003-0807-5

Miskiewicz K, Jose LE, Bento-Abreu A, Fislage M, Taes I, Kasprowicz J, Verstreken P (2011). ELP3 controls active zone morphology by acetylating the ELKS family member Bruchpilot. Neuron 72(5):776-788. https://doi.org/10.1016/j.neuron.2011.10.010

Myat AA, Zhou Y, Gao Y, Zhao X, Liang C, Abid MA, Meng Z (2022). Overexpression of GhKTI12 enhances seed yield and biomass production in Nicotiana tabacum. Genes 13(3): 426. https://doi.org/10.3390/genes13030426

Nelissen H, De Groeve S, Fleury D, Neyt P, Bruno L, Bitonti MB, Van Lijsebettens M (2010). Plant Elongator regulates auxin-related genes during RNA polymerase II transcription elongation. Proceedings of the National Academy of Sciences of the United States of America 07(4):1678-1683. https://doi.org/10.1073/pnas.0913559107

Nelissen H, Fleury D, Bruno L, Robles P, De Veylder L, Traas J, Van Lijsebettens M (2005). The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proceedings of the National Academy of Sciences of the United States of America 102(21):7754-7759. https://doi.org/10.1073/pnas.0502600102

Otero G, Fellows J, Li Y, De Bizemont T, Dirac AM, Gustafsson CM, Svejstrup JQ (1999). Elongator, a multisubunit component of a novel RNA polymerase II holoenzyme for transcriptional elongation. Molecular Cell 3(1):109-118. https://doi.org/10.1016/s1097-2765(00)80179-3

Petrakis TG, Søgaard TMM, Erdjument-Bromage H, Tempst P, Svejstrup JQ (2005). Physical and functional interaction between Elongator and the Chromatin-associated Kti12 protein. Journal of Biological Chemistry 280(20):19454-19460. https://doi.org/10.1074/jbc.M413373200

Pokholok DK, Hannett NM, Young RA (2002). Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Molecular Cell 9(4):799-809. https://doi.org/10.1016/s1097-2765(02)00502-6

Selvadurai K, Wang P, Seimetz J, Huang RH (2014). Archaeal Elp3 catalyzes tRNA wobble uridine modification at C5 via a radical mechanism. Nature Chemical Biology 10(10):810-812. https://doi.org/10.1038/nchembio.1610

Skylar A, Matsuwaka S, Wu X (2013). ELONGATA3 is required for shoot meristem cell cycle progression in Arabidopsis thaliana seedlings. Developmental Biology 382(2): 436-445. https://doi.org/10.1016/j.ydbio.2013.08.008

Stirnimann CU, Petsalaki E, Russell RB, Müller CW (2010). WD40 proteins propel cellular networks. Trends in Biochemical Sciences 35(10):565-574. https://doi.org/10.1016/j.tibs.2010.04.003

Versées W, De Groeve S, Van Lijsebettens M (2010). Elongator, a conserved multitasking complex? Molecular Microbiology 76(5):1065-1069. https://doi.org/10.1111/j.1365-2958.2010.07162.x

Wang C, Ding Y, Yao J, Zhang Y, Sun Y, Colee J, Mou Z (2015). Arabidopsis Elongator subunit 2 positively contributes to resistance to the necrotrophic fungal pathogens Botrytis cinerea and Alternaria brassicicola. The Plant Journal 83(6):1019-1033. https://doi.org/10.1111/tpj.12946

Wang K, Rong W, Liu Y, Li H, Zhang Z (2020). Wheat Elongator subunit 4 is required for epigenetic regulation of host immune response to Rhizoctonia cerealis. The Crop Journal 8(4):565-576. https://doi.org/10.1016/j.cj.2019.11.005

Winkler GS, Petrakis TG, Ethelberg S, Tokunaga M, Erdjument-Bromage H, Tempst P, Svejstrup JQ (2001). RNA Polymerase II Elongator Holoenzyme Is Composed of Two Discrete Subcomplexes. Journal of Biological Chemistry 276(35):32743-32749. https://doi.org/10.1074/jbc.M105303200

Woloszynska M, Gagliardi O, Vandenbussche F, De Groeve S, Alonso Baez L, Neyt P, Van Lijsebettens M (2018). The Elongator complex regulates hypocotyl growth in darkness and during photomorphogenesis. Journal of Cell Science 131(2):s203927. https://doi.org/10.1242/jcs.203927

Xu D, Huang W, Li Y, Wang H, Huang H, Cui X (2012). Elongator complex is critical for cell cycle progression and leaf patterning in Arabidopsis. Plant Journal 69(5): 792-808. https://doi.org/10.1111/j.1365-313X.2011.04831.x

Zhou X, Hua D, Chen Z, Zhou Z, Gong Z (2009). Elongator mediates ABA responses, oxidative stress resistance and anthocyanin biosynthesis in Arabidopsis. The Plant Journal 60(1):79-90. https://doi.org/10.1111/j.1365-313X.2009.03931.x

Zhu M, Li Y, Chen G, Ren L, Xie Q, Zhao Z, Hu Z (2015). Silencing SlELP2L, a tomato Elongator complex protein 2-like gene, inhibits leaf growth, accelerates leaf, sepal senescence, and produces dark-green fruit. Scientific Reports 5:7693. https://doi.org/10.1038/srep07693

Published

2023-03-27

How to Cite

XIANGZHUO, J., ZELONG, Z., YINXIA, W., YUNFANG, Z., & YUNLING, P. (2023). Research progress of the Elongator complex in plant. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 51(1), 13058. https://doi.org/10.15835/nbha51113058

Issue

Section

Review Articles
CITATION
DOI: 10.15835/nbha51113058