Abstract
Auxin is one of the most important hormone groups in plants. It has been documented to play various functions in plant growth and development. In this phytohormone group, indole-3-acetic acid (IAA) is widely considered as a main natural auxin. To date, many lines of evidence have revealed that the alterations of ambient environment such as light and temperature conditions can affect the IAA biosynthesis which consequently redirects the growth and development of the plants so that they can adapt to the new environmental conditions. Current studies have shown the large impact of chromatin modifications in the regulation of eukaryotic gene expression. Previous studies have elucidated different epigenetic factors in the regulation of auxin signaling pathway in the plants. This review aimed to provide a precise and systemic overview of the chromatin modifications at the auxin biosynthesis gene loci, namely YUCCA (YUC) genes, and their effects on the expression of these genes. Based on these emerging data, we propose different hypothetical models demonstrating the functions of epigenetic factors as well as chromatin modifications in the regulation of YUC genes which can subsequently determine the auxin accumulation in the plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agger K, Christensen J, Cloos PAC, Helin K (2008) The emerging functions of histone demethylases. Curr Opin Genet Dev 18:159–168. https://doi.org/10.1016/j.gde.2007.12.003
Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of auxin in regulating Arabidopsis flower development. Planta 223:315–328. https://doi.org/10.1007/s00425-005-0088-9
Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395. https://doi.org/10.1038/cr.2011.22
Brahma S et al (2017) INO80 exchanges H2A.Z for H2A by translocating on DNA proximal to histone dimers. Nat Commun. https://doi.org/10.1038/ncomms15616
Brumos J, Alonso JM, Stepanova AN (2014) Genetic aspects of auxin biosynthesis and its regulation. Physiol Plant 151:3–12. https://doi.org/10.1111/ppl.12098
Casper J et al (2018) The UCSC Genome Browser database: 2018 update. Nucleic Acids Res 46:D762–D769. https://doi.org/10.1093/nar/gkx1020
Chen LQ et al (2016) YUCCA-mediated auxin biogenesis is required for cell fate transition occurring during de novo root organogenesis in Arabidopsis. J Exp Bot 67:4273–4284. https://doi.org/10.1093/jxb/erw213
Cheng YF, Dai XH, Zhao YD (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Gene Dev 20:1790–1799. https://doi.org/10.1101/gad.1415106
Cheng SF et al (2018) WOX11 recruits a histone H3K27me3 demethylase to promote gene expression during shoot development in rice. Nucleic Acids Res 46:2356–2369. https://doi.org/10.1093/nar/gky017
Choi K et al (2005) SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis. Plant Cell 17:2647–2660. https://doi.org/10.1105/tpc.105.035485
Choi K, Park C, Lee J, Oh M, Noh B, Lee I (2007) Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development. Development 134:1931–1941. https://doi.org/10.1242/dev.001891
Coleman-Derr D, Zilberman D (2012) Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002988
Collett CE, Harberd NP, Leyser O (2000) Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol 124:553–561. https://doi.org/10.1104/pp.124.2.553
Cui X et al (2016) REF6 recognizes a specific DNA sequence to demethylate H3K27me3 and regulate organ boundary formation in Arabidopsis. Nat Genet 48:694–699. https://doi.org/10.1038/ng.3556
Deal RB, Henikoff S (2011) Histone variants and modifications in plant gene regulation. Curr Opin Plant Biol 14:116–122. https://doi.org/10.1016/j.pbi.2010.11.005
Deal RB, Topp CN, McKinney EC, Meagher RB (2007) Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell 19:74–83. https://doi.org/10.1105/tpc.106.048447
Derkacheva M, Hennig L (2014) Variations on a theme: Polycomb group proteins in plants. J Exp Bot 65:2769–2784. https://doi.org/10.1093/jxb/ert410
Di DW et al (2016) Functional roles of Arabidopsis CKRC2/YUCCA8 gene and the involvement of PIF4 in the regulation of auxin biosynthesis by cytokinin. Sci Rep. https://doi.org/10.1038/srep36866
Dong XJ, Weng ZP (2013) The correlation between histone modifications and gene expression. Epigenomics 5:113–116. https://doi.org/10.2217/Epi.13.13
Enders TA, Strader LC (2015) Auxin activity: past, present, and future. Am J Bot 102:180–196. https://doi.org/10.3732/ajb.1400285
Franklin KA et al (2011) PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA 108:20231–20235. https://doi.org/10.1073/pnas.1110682108
Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69:437–449. https://doi.org/10.1007/s11103-008-9417-2
Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M (1998) High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci USA 95:7197–7202. https://doi.org/10.1073/pnas.95.12.7197
Grzybkowska D, Morończyk J, Wójcikowska B, Gaj MD (2018) Azacitidine (5-AzaC)-treatment and mutations in DNA methylase genes affect embryogenic response and expression of the genes that are involved in somatic embryogenesis in Arabidopsis. Plant Growth Regul 85:243–256. https://doi.org/10.1007/s10725-018-0389-1
Halpern KB, Vana T, Walker MD (2014) Paradoxical role of DNA methylation in activation of FoxA2 gene expression during endoderm development. J Biol Chem 289:23882–23892. https://doi.org/10.1074/jbc.M114.573469
He CS, Chen XF, Huang H, Xu L (2012) Reprogramming of H3K27me3 is critical for acquisition of pluripotency from cultured Arabidopsis tissues. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002911
Hentrich M et al (2013) The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J 74:626–637. https://doi.org/10.1111/tpj.12152
Hernández-Madrigal F, Ortiz-Castro R, Ruiz-Herrera LF, Cervantes C, López-Bucio J, Martínez-Trujillo M (2018) Temporal root responses in Arabidopsis thaliana L. to chromate reveal structural and regulatory mechanisms involving the SOLITARY ROOT/IAA14 repressor for maintenance of identity meristem genes. Plant Growth Regul. https://doi.org/10.1007/s10725-018-0425-1
Hollender C, Liu ZC (2008) Histone deacetylase genes in Arabidopsis development. J Integr Plant Biol 50:875–885. https://doi.org/10.1111/j.1744-7909.2008.00704.x
Hornitschek P et al (2012) PHYTOCHROME INTERACTING FACTORS 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71:699–711. https://doi.org/10.1111/j.1365-313X.2012.05033.x
Hwang G, Zhu JY, Lee YK, Kim S, Nguyen TT, Kim J, Oh E (2017) PIF4 promotes expression of LNG1 and LNG2 to induce thermomorphogenic growth in Arabidopsis. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01320
Ikeda Y, Men SZ, Fischer U, Stepanova AN, Alonso JM, Ljung K, Grebe M (2009) Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat Cell Biol 11:731–738. https://doi.org/10.1038/ncb1879
Jarillo JA, Pineiro M (2015) H2A.Z mediates different aspects of chromatin function and modulates flowering responses in Arabidopsis. Plant J 83:96–109. https://doi.org/10.1111/tpj.12873
Karolchik D et al (2003) The UCSC genome browser database. Nucleic Acids Res 31:51–54. https://doi.org/10.1093/nar/gkg129
Kasahara H (2016) Current aspects of auxin biosynthesis in plants. Biosci Biotechnol Biochem 80:34–42. https://doi.org/10.1080/09168451.2015.1086259
Khan AA, Lee AJ, Roh TY (2015) Polycomb group protein-mediated histone modifications during cell differentiation. Epigenomics 7:75–84. https://doi.org/10.2217/Epi.14.61
Kim JI et al (2007) yucca6, a dominant mutation in Arabidopsis, affects auxin accumulation and auxin-related phenotypes. Plant Physiol 145:722–735. https://doi.org/10.1104/pp.107.104935
Kim JM et al (2008) Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49:1580–1588. 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. https://doi.org/10.3389/fpls.2015.00114
Koo AJK, Howe GA (2009) The wound hormone jasmonate. Phytochemistry 70:1571–1580. https://doi.org/10.1016/j.phytochem.2009.07.018
Kulaeva OI et al (2013) Molecular mechanisms of transcription through a nucleosome by RNA polymerase II. Mol Biol 47:655–667. https://doi.org/10.1134/S0026893313050099
Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147. https://doi.org/10.1016/j.cell.2009.11.006
Kumar SV, Lucyshyn D, Jaeger KE, Alos E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245. https://doi.org/10.1038/nature10928
Kwon CS, Lee D, Choi G, Chung WI (2009) Histone occupancy-dependent and -independent removal of H3K27 trimethylation at cold-responsive genes in Arabidopsis. Plant J 60:112–121. https://doi.org/10.1111/j.1365-313X.2009.03938.x
Kwon Y, Kim JH, Nguyen HN, Jikumaru Y, Kamiya Y, Hong SW, Lee H (2013) A novel Arabidopsis MYB-like transcription factor, MYBH, regulates hypocotyl elongation by enhancing auxin accumulation. J Exp Bot 64:3911–3922. https://doi.org/10.1093/jxb/ert223
Lademann CA, Renkawitz J, Pfander B, Jentsch S (2017) The INO80 complex removes H2A.Z to promote presynaptic filament formation during homologous recombination. Cell Rep 19:1294–1303. https://doi.org/10.1016/j.celrep.2017.04.051
Lai WKM, Pugh BF (2017) Understanding nucleosome dynamics and their links to gene expression and DNA replication. Nat Rev Mol Cell Biol 18:548–562. https://doi.org/10.1038/nrm.2017.47
Lawrence M, Daujat S, Schneider R (2016) Lateral thinking: how histone modifications regulate gene expression. Trends Genet 32:42–56. https://doi.org/10.1016/j.tig.2015.10.007
Lee K, Seo PJ (2017) Coordination of matrix attachment and ATP-dependent chromatin remodeling regulate auxin biosynthesis and Arabidopsis hypocotyl elongation. PLoS ONE. https://doi.org/10.1371/journal.pone.0181804
Leon J, Rojo E, Sanchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52:1–9. https://doi.org/10.1093/jexbot/52.354.1
Li C et al (2016) Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis. Nat Genet 48:687–693. https://doi.org/10.1038/ng.3555
Liu G, Gao S, Tian H, Wu W, Robert HS, Ding Z (2016) Local transcriptional control of YUCCA regulates auxin promoted root-growth inhibition in response to aluminium stress in Arabidopsis. PLoS Genet. https://doi.org/10.1371/journal.pgen.1006360
Lu FL, Li GL, Cui X, Liu CY, Wang XJ, Cao XF (2008) Comparative analysis of JmjC domain-containing proteins reveals the potential histone demethylases in Arabidopsis and rice. J Integr Plant Biol 50:886–896. https://doi.org/10.1111/j.1744-7909.2008.00692.x
Lu FL, Cui X, Zhang SB, Jenuwein T, Cao XF (2011) Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat Genet 43:715–719. https://doi.org/10.1038/ng.854
Ma D, Li X, Guo Y, Chu J, Fang S, Yan C, Noel JP, Liu H (2016) Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light. Proc Natl Acad Sci USA 113:224–229. https://doi.org/10.1073/pnas.1511437113
Manzano C et al (2012) Auxin and epigenetic regulation of SKP2B, an F-Box that represses lateral root formation. Plant Physiol 160:749–762. https://doi.org/10.1104/pp.112.198341
Mashiguchi K et al (2011) The main auxin biosynthesis pathway in Arabidopsis. P Natl Acad Sci USA 108:18512–18517. https://doi.org/10.1073/pnas.1108434108
McGinty RK, Tan S (2015) Nucleosome structure and function. Chem Rev 115:2255–2273. https://doi.org/10.1021/cr500373h
Mellor J (2006) Dynamic nucleosomes and gene transcription. Trends Genet 22:320–329. https://doi.org/10.1016/j.tig.2006.03.008
Muller-Moule P et al (2016) YUCCA auxin biosynthetic genes are required for Arabidopsis shade avoidance. PeerJ. https://doi.org/10.7717/peerj.2574
Nguyen NH, Cheong JJ (2018) H2A.Z-containing nucleosomes are evicted to activate AtMYB44 transcription in response to salt stress. Biochem Biophys Res Commun 499:1039–1043. https://doi.org/10.1016/j.bbrc.2018.04.048
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 32:1625–1636. https://doi.org/10.1007/s00299-013-1474-6
Noh YS, Amasino RM (2003) PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell 15:1671–1682. https://doi.org/10.1105/tpc.012161
Pandey R et al (2002) Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res 30:5036–5055. https://doi.org/10.1093/nar/gkf660
Papamichos-Chronakis M, Watanabe S, Rando OJ, Peterson CL (2011) Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 144:200–213. https://doi.org/10.1016/j.cell.2010.12.021
Peer WA, Blakeslee JJ, Yang HB, Murphy AS (2011) Seven things we think we know about auxin transport. Mol Plant 4:487–504. https://doi.org/10.1093/mp/ssr034
Peng ML et al (2018) Linking PHYTOCHROME-INTERACTING FACTOR to histone modification in plant shade avoidance. Plant Physiol 176:1341–1351. https://doi.org/10.1104/pp.17.01189
Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590. https://doi.org/10.1146/annurev-arplant-042811-105501
Pinon V, Prasad K, Grigg SP, Sanchez-Perez GF, Scheres B (2013) Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc Natl Acad Sci USA 110:1107–1112. https://doi.org/10.1073/pnas.1213497110
Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274. https://doi.org/10.1104/pp.99.4.1271
Saze H, Tsugane K, Kanno T, Nishimura T (2012) DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol 53:766–784. https://doi.org/10.1093/pcp/pcs008
Scarpella E, Barkoulas M, Tsiantis M (2010) Control of leaf and vein development by auxin. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a001511
Siegfried Z, Simon I (2010) DNA methylation and gene expression. WIREs Syst Biol Med 2:362–371. https://doi.org/10.1002/wsbm.64
Smith AP, Jain A, Deal RB, Nagarajan VK, Poling MD, Raghothama KG, Meagher RB (2010) Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol 152:217–225. https://doi.org/10.1104/pp.109.145532
Stavang JA et al (2009) Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J 60:589–601. https://doi.org/10.1111/j.1365-313X.2009.03983.x
Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45. https://doi.org/10.1038/47412
Struhl K, Segal E (2013) Determinants of nucleosome positioning. Nat Struct Mol Biol 20:267–273. https://doi.org/10.1038/nsmb.2506
Sun JQ, Qi LL, Li YN, Chu JF, Li CY (2012) PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002594
Sura W et al (2017) Dual role of the histone variant H2A.Z in transcriptional regulation of stress-response genes. Plant Cell 29:791–807. https://doi.org/10.1105/tpc.16.00573
Tao Y et al (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176. https://doi.org/10.1016/j.cell.2008.01.049
To TK, Kim JM (2014) Epigenetic regulation of gene responsiveness in Arabidopsis. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00548
Tricker PJ, Gibbings JG, Lopez CMR, Hadley P, Wilkinson MJ (2012) Low relative humidity triggers RNA-directed de novo DNA methylation and suppression of genes controlling stomatal development. J Exp Bot 63:3799–3813. https://doi.org/10.1093/jxb/ers076
Velasquez SM, Barbez E, Kleine-Vehn J, Estevez JM (2016) Auxin and cellular elongation. Plant Physiol 170:1206–1215. https://doi.org/10.1104/pp.15.01863
Weber CM, Henikoff S (2014) Histone variants: dynamic punctuation in transcription. Gene Dev 28:672–682. https://doi.org/10.1101/gad.238873.114
Weiste C, Droge-Laser W (2014) The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery. Nat Commun. https://doi.org/10.1038/ncomms4883
Workman JL (2006) Nucleosome displacement in transcription. Gene Dev 20:2009–2017. https://doi.org/10.1101/gad.1435706
Xu R et al (2015) Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNA methylation pathway in Arabidopsis. J Exp Bot 66:5997–6008. https://doi.org/10.1093/jxb/erv312
Yamamoto Y, Kamiya N, Morinaka Y, Matsuoka M, Sazuka T (2007) Auxin biosynthesis by the YUCCA genes in rice. Plant Physiol 143:1362–1371. https://doi.org/10.1104/pp.106.091561
Yamamuro C, Zhu JK, Yang ZB (2016) Epigenetic modifications and plant hormone action. Mol Plant 9:57–70. https://doi.org/10.1016/j.molp.2015.10.008
Yan W et al (2018) Dynamic and spatial restriction of Polycomb activity by plant histone demethylases. Nat Plants 4:681–689. https://doi.org/10.1038/s41477-018-0219-5
Yuan LY, Liu XC, Luo M, Yang SG, Wu KQ (2013) Involvement of histone modifications in plant abiotic stress responses. J Integr Plant Biol 55:892–901. https://doi.org/10.1111/jipb.12060
Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–919. https://doi.org/10.1126/science.1186366
Zhang T, Zhang WL, Jiang JM (2015) Genome-wide nucleosome occupancy and positioning and their impact on gene expression and evolution in plants. Plant Physiol 168:1406–1416. https://doi.org/10.1104/pp.15.00125
Zhao YD (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64. https://doi.org/10.1146/annurev-arplant-042809-112308
Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309. https://doi.org/10.1126/science.291.5502.306
Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S (2008) Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456:125–129. https://doi.org/10.1038/nature07324
Acknowledgements
We would like to thank Dr. Sara D Siegel (The University of Texas Southwestern, Texas, USA) for her careful and critical reading of our manuscript. This work was supported by a Grant from Ho Chi Minh City Open University (to Nguyen Hoai Nguyen, 2018).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Do, B.H., Phuong, V.T.B., Tran, GB. et al. Emerging functions of chromatin modifications in auxin biosynthesis in response to environmental alterations. Plant Growth Regul 87, 165–174 (2019). https://doi.org/10.1007/s10725-018-0453-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-018-0453-x