Abstract
Key message
The auxin signaling and root morphogenesis are harmoniously controlled by two counteracted teams including (1) auxin/indole-3-acetic acid (AUX/IAA)-histone deacetylase (HDA) and (2) auxin response factor (ARF)-histone acetyltransferase (HAT).
Abstract
The involvement of histone acetylation in the regulation of transcription was firstly reported a few decades ago. In planta, auxin is the first hormone group that was discovered and it is also the most studied phytohormone. Current studies have elucidated the functions of histone acetylation in the modulation of auxin signaling as well as in the regulation of root morphogenesis under both normal and stress conditions. Based on the recent outcomes, this review is to provide a hierarchical view about the functions of histone acetylation in auxin signaling and root morphogenesis. In this report, we suggest that the auxin signaling must be controlled harmoniously by two counteracted teams including (1) auxin/indole-3-acetic acid (AUX/IAA)-histone deacetylase (HDA) and (2) auxin response factor (ARF)-histone acetyltransferase (HAT). Moreover, the balance in auxin signaling is very critical to contribute to normal root morphogenesis.
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References
Allfrey VG, Faulkner R, Mirsky AE (1964) Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA 51(5):786–794. https://doi.org/10.1073/pnas.51.5.786
Alver BH, Kim KH, Lu P, Wang X, Manchester HE, Wang W, Haswell JR, Park PJ, Roberts CW (2017) The SWI/SNF chromatin remodelling complex is required for maintenance of lineage specific enhancers. Nat Commun 8:14648. https://doi.org/10.1038/ncomms14648
Anzola JM, Sieberer T, Ortbauer M, Butt H, Korbei B, Weinhofer I, Mullner AE, Luschnig C (2010) Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin. Proc Natl Acad Sci USA 107(22):10308–10313. https://doi.org/10.1073/pnas.0913918107
Armstrong JA, Papoulas O, Daubresse G, Sperling AS, Lis JT, Scott MP, Tamkun JW (2002) The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J 21(19):5245–5254. https://doi.org/10.1093/emboj/cdf517
Braszewska-Zalewska AJ, Wolny EA, Smialek L, Hasterok R (2013) Tissue-specific epigenetic modifications in root apical meristem cells of Hordeum vulgare. PLoS ONE 8(7):e69204. https://doi.org/10.1371/journal.pone.0069204
Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158(1):423–438. https://doi.org/10.1104/pp.111.186999
Chandler JW (2016) Auxin response factors. Plant Cell Environ 39(5):1014–1028. https://doi.org/10.1111/pce.12662
Chen DH, Huang Y, Jiang C, Si JP (2018) Chromatin-based regulation of plant root development. Front Plant Sci 9:1509. https://doi.org/10.3389/fpls.2018.01509
Chung PJ, Kim YS, Jeong JS, Park SH, Nahm BH, Kim JK (2009) The histone deacetylase OsHDAC1 epigenetically regulates the OsNAC6 gene that controls seedling root growth in rice. Plant J 59(5):764–776. https://doi.org/10.1111/j.1365-313X.2009.03908.x
Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78:273–304. https://doi.org/10.1146/annurev.biochem.77.062706.153223
Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445
Do BH, Phuong VTB, Tran GB, Nguyen NH (2019) Emerging functions of chromatin modifications in auxin biosynthesis in response to environmental alterations. Plant Growth Regul 87:165–174. https://doi.org/10.1007/s10725-018-0453-x
Dong X, Weng Z (2013) The correlation between histone modifications and gene expression. Epigenomics 5(2):113–116. https://doi.org/10.2217/epi.13.13
Du Z, Li H, Wei Q, Zhao X, Wang C, Zhu Q, Yi X, Xu W, Liu XS, Jin W, Su Z (2013) Genome-wide analysis of histone modifications: H3K4me2, H3K4me3, H3K9ac, and H3K27ac in Oryza sativa L. Japonica Mol Plant 6(5):1463–1472. https://doi.org/10.1093/mp/sst018
Efroni I, Han SK, Kim HJ, Wu MF, Steiner E, Birnbaum KD, Hong JC, Eshed Y, Wagner D (2013) Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev Cell 24(4):438–445. https://doi.org/10.1016/j.devcel.2013.01.019
Enders TA, Strader LC (2015) Auxin activity: past, present, and future. Am J Bot 102(2):180–196. https://doi.org/10.3732/ajb.1400285
Fina JP, Casati P (2015) HAG3, a histone acetyltransferase, affects UV-B responses by negatively regulating the expression of DNA repair enzymes and sunscreen content in Arabidopsis thaliana. Plant Cell Physiol 56(7):1388–1400. https://doi.org/10.1093/pcp/pcv054
Guilfoyle TJ (2015) The PB1 domain in auxin response factor and Aux/IAA proteins: a versatile protein interaction module in the auxin response. Plant Cell 27(1):33–43. https://doi.org/10.1105/tpc.114.132753
Jang IC, Pahk YM, Song SI, Kwon HJ, Nahm BH, Kim JK (2003) Structure and expression of the rice class-I type histone deacetylase genes OsHDAC1-3: OsHDAC1 overexpression in transgenic plants leads to increased growth rate and altered architecture. Plant J 33(3):531–541
Jegu T, Veluchamy A, Ramirez-Prado JS, Rizzi-Paillet C, Perez M, Lhomme A, Latrasse D, Coleno E, Vicaire S, Legras S, Jost B, Rougee M, Barneche F, Bergounioux C, Crespi M, Mahfouz MM, Hirt H, Raynaud C, Benhamed M (2017) The Arabidopsis SWI/SNF protein BAF60 mediates seedling growth control by modulating DNA accessibility. Genome Biol 18(1):114. https://doi.org/10.1186/s13059-017-1246-7
Kagale S, Rozwadowski K (2011) EAR motif-mediated transcriptional repression in plants: an underlying mechanism for epigenetic regulation of gene expression. Epigenetics 6(2):141–146. https://doi.org/10.4161/epi.6.2.13627
Kagale S, Links MG, Rozwadowski K (2010) Genome-wide analysis of ethylene-responsive element binding factor-associated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis. Plant Physiol 152(3):1109–1134. https://doi.org/10.1104/pp.109.151704
Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451
Kim JM, To TK, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M (2008) Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49(10):1580–1588. https://doi.org/10.1093/pcp/pcn133
Kim JM, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114. https://doi.org/10.3389/fpls.2015.00114
Kingston RE, Narlikar GJ (1999) ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev 13:2339–2352
Kornet N, Scheres B (2009) Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis. Plant Cell 21(4):1070–1079. https://doi.org/10.1105/tpc.108.065300
Krogan NT, Long JA (2009) Why so repressed? Turning off transcription during plant growth and development. Curr Opin Plant Biol 12(5):628–636. https://doi.org/10.1016/j.pbi.2009.07.011
Kuhn A, Harborough SR, McLaughlin HM, Kepinski S, Østergaard L (2019) Direct ETTIN-auxin interaction controls chromatin state in gynoecium development. bioRxiv. https://doi.org/10.1101/863134
Lai WKM, Pugh BF (2017) Understanding nucleosome dynamics and their links to gene expression and DNA replication. Nat Rev Mol Cell Biol 18(9):548–562. https://doi.org/10.1038/nrm.2017.47
Lau S, Jurgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20(7):1738–1746. https://doi.org/10.1105/tpc.108.060418
Lawrence M, Daujat S, Schneider R (2016) Lateral thinking: how histone modifications regulate gene expression. Trends Genet 32(1):42–56. https://doi.org/10.1016/j.tig.2015.10.007
Leyser O (2018) Auxin signaling. Plant Physiol 176(1):465–479. https://doi.org/10.1104/pp.17.00765
Li C, Xu J, Li J, Li Q, Yang H (2014a) Involvement of Arabidopsis histone acetyltransferase HAC family genes in the ethylene signaling pathway. Plant Cell Physiol 55(2):426–435. https://doi.org/10.1093/pcp/pct180
Li H, Yan S, Zhao L, Tan J, Zhang Q, Gao F, Wang P, Hou H, Li L (2014b) Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol 14:105. https://doi.org/10.1186/1471-2229-14-105
Li SB, Xie ZZ, Hu CG, Zhang JZ (2016) A review of auxin response factors (ARFs) in plants. Front Plant Sci 7:47. https://doi.org/10.3389/fpls.2016.00047
Li H, Torres-Garcia J, Latrasse D, Benhamed M, Schilderink S, Zhou W, Kulikova O, Hirt H, Bisseling T (2017) Plant-specific histone deacetylases HDT1/2 regulate GIBBERELLIN 2-OXIDASE2 expression to control Arabidopsis root meristem cell number. Plant Cell 29(9):2183–2196
Li C, Liu D, Lin Z, Guan B, Liu D, Yang L, Deng X, Mei F, Zhou Z (2019) Histone acetylation modification affects cell wall degradation and aerenchyma formation in wheat seminal roots under waterlogging. Plant Growth Regul 87:149–163. https://doi.org/10.1007/s10725-018-0460-y
Liu C, Li LC, Chen WQ, Chen X, Xu ZH, Bai SN (2013) HDA18 affects cell fate in Arabidopsis root epidermis via histone acetylation at four kinase genes. Plant Cell 25(1):257–269. https://doi.org/10.1105/tpc.112.107045
Liu K, Yuan C, Li H, Lin W, Yang Y, Shen C, Zheng X (2015) Genome-wide identification and characterization of auxin response factor (ARF) family genes related to flower and fruit development in papaya (Carica papaya L.). BMC Genom 16:901. https://doi.org/10.1186/s12864-015-2182-0
Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312(5779):1520–1523. https://doi.org/10.1126/science.1123841
Luo M, Wang YY, Liu X, Yang S, Lu Q, Cui Y, Wu K (2012) HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. J Exp Bot 63(8):3297–3306. https://doi.org/10.1093/jxb/ers059
Manzano C, Ramirez-Parra E, Casimiro I, Otero S, Desvoyes B, De Rybel B, Beeckman T, Casero P, Gutierrez C, Pozo JCD (2012) Auxin and epigenetic regulation of SKP2B, an F-box that represses lateral root formation. Plant Physiol 160(2):749–762. https://doi.org/10.1104/pp.112.198341
Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80. https://doi.org/10.1146/annurev.cellbio.23.090506.123214
Morales V, Richard-Foy H (2000) Role of histone N-terminal tails and their acetylation in nucleosome dynamics. Mol Cell Biol 20(19):7230–7237. https://doi.org/10.1128/mcb.20.19.7230-7237.2000
Nanao MH, Vinos-Poyo T, Brunoud G, Thevenon E, Mazzoleni M, Mast D, Laine S, Wang S, Hagen G, Li H, Guilfoyle TJ, Parcy F, Vernoux T, Dumas R (2014) Structural basis for oligomerization of auxin transcriptional regulators. Nat Commun 5:3617. https://doi.org/10.1038/ncomms4617
Nguyen NH, Cheong JJ (2018) The AtMYB44 promoter is accessible to signals that induce different chromatin modifications for gene transcription. Plant Physiol Biochem 130:1–19. https://doi.org/10.1016/j.plaphy.2018.06.030
Nguyen HN, Kim JH, Jeong CY, Hong SW, Lee H (2013) Inhibition of histone deacetylation alters Arabidopsis root growth in response to auxin via PIN1 degradation. Plant Cell Rep 32(10):1625–1636. https://doi.org/10.1007/s00299-013-1474-6
Nguyen NH, Nguyen CTT, Jung C, Cheong JJ (2019) AtMYB44 suppresses transcription of the late embryogenesis abundant protein gene AtLEA4-5. Biochem Biophys Res Commun 511(4):931–934. https://doi.org/10.1016/j.bbrc.2019.03.006
Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13(8):1959–1968. https://doi.org/10.1105/tpc.010127
Peer WA, Blakeslee JJ, Yang HB, Murphy AS (2011) Seven things we think we know about auxin transport. Mol Plant 4(3):487–504. https://doi.org/10.1093/mp/ssr034
Richmond TJ, Finch JT, Rushton B, Rhodes D, Klug A (1984) The structure of the nucleosome core particle at 7Å resolution. Nature 311:532–537
Saiga S, Moller B, Watanabe-Taneda A, Abe M, Weijers D, Komeda Y (2012) Control of embryonic meristem initiation in Arabidopsis by PHD-finger protein complexes. Development 139(8):1391–1398. https://doi.org/10.1242/dev.074492
Seto E, Yoshida M (2014) Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol 6(4):a018713. https://doi.org/10.1101/cshperspect.a018713
Sieberer T, Hauser MT, Seifert GJ, Luschnig C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13(10):837–842. https://doi.org/10.1016/s0960-9822(03)00327-0
Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319(5868):1384–1386. https://doi.org/10.1126/science.1151461
Tanaka M, Kikuchi A, Kamada H (2008) The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol 146(1):149–161. https://doi.org/10.1104/pp.107.111674
Tiwari SB, Hagen G, Guilfoyle TJ (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16(2):533–543. https://doi.org/10.1105/tpc.017384
Tramontano WA, Scanlon C (1996) Cell cycle inhibition by sodium butyrate in legume root meristems. Phytochemistry 41:85–88
van der Woude LC, Perrella G, Snoek BL, van Hoogdalem M, Novak O, van Verk MC, van Kooten HN, Zorn LE, Tonckens R, Dongus JA, Praat M, Stouten EA, Proveniers MCG, Vellutini E, Patitaki E, Shapulatov U, Kohlen W, Balasubramanian S, Ljung K, van der Krol AR, Smeekens S, Kaiserli E, van Zanten M (2019) Histone deacetylase 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion. Proc Natl Acad Sci USA 116(50):25343–25354. https://doi.org/10.1073/pnas.1911694116
Vandenbussche F, Petrasek J, Zadnikova P, Hoyerova K, Pesek B, Raz V, Swarup R, Bennett M, Zazimalova E, Benkova E, Van Der Straeten D (2010) The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development 137(4):597–606. https://doi.org/10.1242/dev.040790
Vlachonasios KE, Thomashow MF, Triezenberg SJ (2003) Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell 15(3):626–638
Weiste C, Droge-Laser W (2014) The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery. Nat Commun 5:3883. https://doi.org/10.1038/ncomms4883
Woodward AW, Bartel B (2005) A receptor for auxin. Plant Cell 17(9):2425–2429. https://doi.org/10.1105/tpc.105.036236
Wright RC, Nemhauser JL (2015) New tangles in the auxin signaling web. F1000Prime Rep 7:19. https://doi.org/10.12703/P7-19
Wu K, Zhang L, Zhou C, Yu CW, Chaikam V (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59(2):225–234. https://doi.org/10.1093/jxb/erm300
Wu MF, Yamaguchi N, Xiao J, Bargmann B, Estelle M, Sang Y, Wagner D (2015) Auxin-regulated chromatin switch directs acquisition of flower primordium founder fate. Elife 4:e09269. https://doi.org/10.7554/eLife.09269
Xu CR, Liu C, Wang YL, Li LC, Chen WQ, Xu ZH, Bai SN (2005) Histone acetylation affects expression of cellular patterning genes in the Arabidopsis root epidermis. Proc Natl Acad Sci USA 102(40):14469–14474. https://doi.org/10.1073/pnas.0503143102
Yamamuro C, Zhu JK, Yang Z (2016) Epigenetic modifications and plant hormone action. Mol Plant 9(1):57–70. https://doi.org/10.1016/j.molp.2015.10.008
Yan S, Zhang Q, Li Y, Huang Y, Zhao L, Tan J, He S, Li L (2014) Comparison of chromatin epigenetic modification patterns among root meristem, elongation and maturation zones in maize (Zea mays L.). Cytogenet Genome Res 143(1–3):179–188. https://doi.org/10.1159/000361003
Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16(11):1123–1127. https://doi.org/10.1016/j.cub.2006.04.029
Yuan L, Chen X, Chen H, Wu K, Huang S (2019) Histone deacetylases HDA6 and HDA9 coordinately regulate valve cell elongation through affecting auxin signaling in Arabidopsis. Biochem Biophys Res Commun 508(3):695–700. https://doi.org/10.1016/j.bbrc.2018.11.082
Zhu Y, Dong A, Meyer D, Pichon O, Renou JP, Cao K, Shen WH (2006) Arabidopsis NRP1 and NRP2 encode histone chaperones and are required for maintaining postembryonic root growth. Plant Cell 18(11):2879–2892. https://doi.org/10.1105/tpc.106.046490
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We would like to thank Chelsea Anita Kelland (University of California at Davis, USA) for her careful and critical reading of our manuscript.
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CTN and NHN wrote the manuscript. NHN supervised the writing of the manuscript. GBT searched the literature and revised the manuscript. All authors gave final approval for publication and agree to be held accountable for the work performed therein.
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Nguyen, C.T., Tran, GB. & Nguyen, N.H. Homeostasis of histone acetylation is critical for auxin signaling and root morphogenesis. Plant Mol Biol 103, 1–7 (2020). https://doi.org/10.1007/s11103-020-00985-1
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DOI: https://doi.org/10.1007/s11103-020-00985-1