Abstract
Key message
Our results showed the histone deacetylase inhibitors (HDIs) control root development in Arabidopsis via regulation of PIN1 degradation.
Abstract
Epigenetic regulation plays a crucial role in the expression of many genes in response to exogenous or endogenous signals in plants as well as other organisms. One of epigenetic mechanisms is modifications of histone, such as acetylation and deacetylation, are catalyzed by histone acetyltransferase (HAT) and histone deacetylase (HDAC), respectively. The Arabidopsis HDACs, HDA6, and HDA19, were reported to function in physiological processes, including embryo development, abiotic stress response, and flowering. In this study, we demonstrated that histone deacetylase inhibitors (HDIs) inhibit primary root elongation and lateral root emergence. In response to HDIs treatment, the PIN1 protein was almost abolished in the root tip. However, the PIN1 gene did not show decreased expression in the presence of HDIs, whereas IAA genes exhibited increases in transcript levels. In contrast, we observed a stable level of gene expression of stress markers (KIN1 and COR15A) and a cell division marker (CYCB1). Taken together, these results suggest that epigenetic regulation may control auxin-mediated root development through the 26S proteasome-mediated degradation of PIN1 protein.
Similar content being viewed by others
Abbreviations
- CHS:
-
Chalcone synthase
- CYCB1:
-
Cyclin B1
- DAB:
-
Diaminobenzidine
- GUS:
-
β-Glucuronidase
- HAT:
-
Histone acetyltransferase
- HDAC:
-
Histone deacetylase
- HDIs:
-
Histone deacetylase inhibitors
- LR:
-
Lateral root
- MS:
-
Murashige and Skoog
- NaB:
-
Sodium butyrate
- NPA:
-
Naphthylphthalamic acid
- ROS:
-
Reactive oxygen species
- TSA:
-
Trichostatin A
References
Anzola JM, Sieberer T, Ortbauer M, Butt H, Korbei B, Weinhofer I, Müllner 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 107:10308–10313
Aufsatz W, Mette MF, Van Der Winden J, Matzke M, Matzke AJ (2002) HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J 21:6832–6841
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602
Chen LT, Wu K (2010) Role of histone deacetylases HDA6 and HDA19 in ABA and abiotic stress response. Plant Signal Behav 5:1318–1320
Chiatante D, Di Iorio A, Maiuro L, Scippa SG (1999) Effect of water stress on root meristems in woody and herbaceous plants during the first stage of development. Plant Soil 217:159–172
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 59:764–776
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:35–43
Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69:437–449
Geldner N, Richter S, Vieten A, Marquardt S, Torres-Ruiz RA, Mayer U, Jürgens G (2004) Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131:389–400
Jaillais Y, Gaude T (2007) Sorting out the sorting functions of endosomes in Arabidopsis. Plant Signal Behav 2:556–558
Jefferson RA, Kavanagh TA, Bevan MV (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Joseph DC (2009) Phenotypic analysis of Arabidopsis mutants: diaminobenzidine stain for hydrogen peroxide. In: Weigel D, Glazebrook J (eds) Arabidopsis: a laboratory manual. CSHL Press, Cold Spring Harbor
Lee H, Yan G, Masaru O, Liming X, Becky S, Jian-Kang Z (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21:2692–2702
Li KL, Bai X, Li Y, Cai H, Ji W, Tang LL, Wen YD, Zhu YM (2009) GsGASA1 mediated root growth inhibition in response to chronic cold stress is marked by the accumulation of DELLAs. J Plant Physiol 168:2153–2160
Louis M, Rosato RR, Brault L, Osbild S, Battaglia E, Yang XH, Grant S, Bagrel D (2004) The histone deacetylase inhibitor sodium butyrate induces breast cancer cell apoptosis through diverse cytotoxic actions including glutathione depletion and oxidative stress. Int J Oncol 25:1701–1711
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 63:3297–3306
Manzano C, Ramirez-Parra E, Casimiro I, Otero S, Desvoyes B, De Rybel B, Beeckman T, Casero P, Gutierrez C, C Del Pozo J (2012) Auxin and epigenetic regulation of SKP2B, an F-box that represses lateral root formation. Plant Physiol 160:749–762
Marhavý P, Bielach A, Abas L, Abuzeineh A, Duclercq J, Tanaka H, Pařezová M, Petrášek J, Friml J, Kleine-Vehn J, Benková E (2011) Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev Cell 21:796–804
Murfett J, Wang X, Hagen G, Guilfoyle TJ (2001) Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13:1047–1061
Oh JE, Kim YH, Kim JH, Kwon Y, Lee H (2011a) Enhanced level of anthocyanin leads to increased salt tolerance in Arabidopsis PAP1-D plants upon sucrose treatment. J Korean Soc Appl Biol Chem 54:79–88
Oh JE, Kwon Y, Kim JH, Noh H, Hong SW, Lee H (2011b) A dual role for MYB60 in stomatal regulation and root growth of Arabidopsis thaliana under drought stress. Plant Mol Biol 77:91–103
Pandey R, Muller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ, Bender J, Mount DW, Jorgensen RA (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
Peer WA, Blakeslee JJ, Yang H, Murphy AS (2011) Seven things we think we know about auxin transport. Molecular Plant 4:487–504
Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14:399–408
Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590
Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence RJ, Pikaard CS, Murfett J, Furner I, Vaucheret H, Scheid OM (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16:1021–1034
Robert HS, Offringa R (2008) Regulation of auxin transport polarity by AGC kinases. Curr Opin Plant Biol 11:495–502
Sassi M, Lu Y, Zhang Y, Wang J, Dhonukshe P, Blilou I, Dai M, Li J, Gong X, Jaillais Y, Yu X, Traas J, Ruberti I, Wang H, Scheres B, Vernoux T, Xu J (2012) COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1- and PIN2-dependent auxin transport in Arabidopsis. Development 139:3402–3412
Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386
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 146:149–161
Tian L, Chen ZJ (2001) Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc Natl Acad Sci USA 98:200–205
Tian L, Wang J, Fong MP, Chen M, Cao H, Gelvin SB, Chen ZJ (2003) Genetic control of developmental changes induced by disruption of Arabidopsis histone deacetylase 1 (AtHD1) expression. Genetics 165:399–409
Tramontano WA, Scanlon C (1996) Cell cycle inhibition by sodium butyrate in legume root meristems. Phytochem 41:85–88
Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166:1637–1645
Wu K, Malik K, Tian L, Brown D, Miki B (2000) Functional analysis of a RPD3 histone deacetylase homolog in Arabidopsis thaliana. Plant Mol Biol 44:167–176
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 59:225–234
Xiong L, Wang RG, Mao G, Koczan JM (2006) Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic acid. Plant Physiol 142:1065–1074
Zazímalová E, Murphy AS, Yang H, Hoyerová K, Hosek P (2010) Auxin transporters-why so many? Cold Spring Harb Perspect Biol 2:a001552
Acknowledgments
We would like to thank to Dr. Kequiang Wu (National Taiwan University) for donating hda19 seeds. This work was supported by a grant from the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (to Hojoung Lee, 2012; Grant #2012-112068-3) and by a grant from the National Research Foundation (to Suk-Whan Hong; Grant #2012R1A1A4A01006448).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Y.-I. Park.
Electronic supplementary material
Below is the link to the electronic supplementary material.
299_2013_1474_MOESM2_ESM.png
Fig. S1 The hda19 knock-out mutant indicated retarded lateral root development. a The Arabidopsis wild-type and hda19 seedlings were grown on 1/2× MS medium for 15 days. b The relative index of lateral root number per primary root length (mm) was determined. The experiment was repeated three times (n = 10). One-way ANOVA (Duncan’s test; p < 0.05) was performed to determine significant differences in this index between Col-0 and hda19 mutant. The letters were marked above the column to reflect significant differences. Vertical bars show the standard error (n = 30) (PNG 292 kb)
299_2013_1474_MOESM3_ESM.png
Fig. S2 The response of hda19 knock-out mutant to exogenous auxin. Five-day-old Arabidopsis wild-type and hda19 seedlings were transferred to 1/2× MS medium supplemented with the indicated concentration of IAA for 10 days. The abnormal root structures were observed in hda19 growing on medium containing 5 μM of IAA. The red arrows indicate emergence of the swollen area in hda19 root on IAA medium. In addition, 5-day-old Arabidopsis wild-type seedlings were also transferred to 1/2× MS medium supplemented with indicated concentrations of NaB or TSA in combination with IAA for 10 days. The red arrows indicate emergence of swollen areas in root. The experiment was repeated three times (n = 10) (PNG 836 kb)
299_2013_1474_MOESM4_ESM.png
Fig. S3 PIN1 localization in the lateral root emergence area. Five-day-old Arabidopsis wild-type seedlings harboring the PIN1:GFP construct were transferred to 1/2× MS medium supplemented with indicated concentration of IAA alone or in combination with NPA for 4 days. The PIN1:GFP signal was visualized using a confocal laser scanning microscope. The experiment was repeated three times (n = 10). Bar = 50 μm (PNG 121 kb)
Rights and permissions
About this article
Cite this article
Nguyen, H.N., Kim, J.H., Jeong, C.Y. et al. Inhibition of histone deacetylation alters Arabidopsis root growth in response to auxin via PIN1 degradation. Plant Cell Rep 32, 1625–1636 (2013). https://doi.org/10.1007/s00299-013-1474-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-013-1474-6