HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
BB/M023079/1
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
31767749
PubMed Central
PMC6911240
DOI
10.1073/pnas.1911694116
PII: 1911694116
Knihovny.cz E-resources
- Keywords
- Arabidopsis, H2A.Z, HDA9, shade avoidance, thermomorphogenesis,
- MeSH
- Arabidopsis enzymology genetics physiology MeSH
- Histone Deacetylases genetics metabolism MeSH
- Histones genetics metabolism MeSH
- Indoleacetic Acids metabolism MeSH
- Mixed Function Oxygenases genetics metabolism MeSH
- Arabidopsis Proteins genetics metabolism MeSH
- Gene Expression Regulation, Plant MeSH
- Basic Helix-Loop-Helix Transcription Factors genetics metabolism MeSH
- Protein Binding MeSH
- Hot Temperature MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- H2A.Z protein, Arabidopsis MeSH Browser
- HDA9 protein, Arabidopsis MeSH Browser
- Histone Deacetylases MeSH
- Histones MeSH
- Indoleacetic Acids MeSH
- Mixed Function Oxygenases MeSH
- PIF4 protein, Arabidopsis MeSH Browser
- Arabidopsis Proteins MeSH
- Basic Helix-Loop-Helix Transcription Factors MeSH
- YUCCA8 protein, Arabidopsis MeSH Browser
Many plant species respond to unfavorable high ambient temperatures by adjusting their vegetative body plan to facilitate cooling. This process is known as thermomorphogenesis and is induced by the phytohormone auxin. Here, we demonstrate that the chromatin-modifying enzyme HISTONE DEACETYLASE 9 (HDA9) mediates thermomorphogenesis but does not interfere with hypocotyl elongation during shade avoidance. HDA9 is stabilized in response to high temperature and mediates histone deacetylation at the YUCCA8 locus, a rate-limiting enzyme in auxin biosynthesis, at warm temperatures. We show that HDA9 permits net eviction of the H2A.Z histone variant from nucleosomes associated with YUCCA8, allowing binding and transcriptional activation by PHYTOCHROME INTERACTING FACTOR 4, followed by auxin accumulation and thermomorphogenesis.
Laboratory of Molecular Biology Wageningen University 6708 PB Wageningen The Netherlands
Laboratory of Plant Physiology Wageningen University 6708 PB Wageningen The Netherlands
School of Biological Sciences Monash University VIC 3800 Melbourne Australia
See more in PubMed
Challinor A. J., et al. , A meta-analysis of crop yield under climate change and adaptation. Nat. Clim. Chang. 4, 287–291 (2014).
Zhao C., et al. , Temperature increase reduces global yields of major crops in four independent estimates. Proc. Natl. Acad. Sci. U.S.A. 114, 9326–9331 (2017). PubMed PMC
Crawford A. J., McLachlan D. H., Hetherington A. M., Franklin K. A., High temperature exposure increases plant cooling capacity. Curr. Biol. 22, R396–R397 (2012). PubMed
Quint M., et al. , Molecular and genetic control of plant thermomorphogenesis. Nat. Plants 2, 15190 (2016). PubMed
Casal J. J., Balasubramanian S., Thermomorphogenesis. Annu. Rev. Plant Biol. 70, 321–346 (2019). PubMed
Koini M. A., et al. , High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408–413 (2009). PubMed
Sun J., Qi L., Li Y., Chu J., Li C., PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating arabidopsis hypocotyl growth. PLoS Genet. 8, e1002594 (2012). PubMed PMC
Franklin K. A., et al. , Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc. Natl. Acad. Sci. U.S.A. 108, 20231–20235 (2011). PubMed PMC
Box M. S., et al. , ELF3 controls thermoresponsive growth in Arabidopsis. Curr. Biol. 25, 194–199 (2015). PubMed
Raschke A., et al. , Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes. BMC Plant Biol. 15, 197 (2015). PubMed PMC
Lee H.-J., et al. , FCA mediates thermal adaptation of stem growth by attenuating auxin action in Arabidopsis. Nat. Commun. 5, 5473 (2014). PubMed
Ballaré C. L., Pierik R., The shade-avoidance syndrome: Multiple signals and ecological consequences. Plant Cell Environ. 40, 2530–2543 (2017). PubMed
Legris M., et al. , Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354, 897–900 (2016). PubMed
Jung J.-H., et al. , Phytochromes function as thermosensors in Arabidopsis. Science 354, 886–889 (2016). PubMed
Sidaway-Lee K., Costa M. J., Rand D. A., Finkenstadt B., Penfield S., Direct measurement of transcription rates reveals multiple mechanisms for configuration of the Arabidopsis ambient temperature response. Genome Biol. 15, R45 (2014). PubMed PMC
Kumar S. V., Wigge P. A., H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136–147 (2010). PubMed
Boden S. A., Kavanová M., Finnegan E. J., Wigge P. A., Thermal stress effects on grain yield in Brachypodium distachyon occur via H2A.Z-nucleosomes. Genome Biol. 14, R65 (2013). PubMed PMC
Zha P., Jing Y., Xu G., Lin R., PICKLE chromatin-remodeling factor controls thermosensory hypocotyl growth of Arabidopsis. Plant Cell Environ. 40, 2426–2436 (2017). PubMed
Huai J., et al. , SEUSS and PIF4 coordinately regulate light and temperature signaling pathways to control plant growth. Mol. Plant 11, 928–942 (2018). PubMed
Cortijo S., et al. , Transcriptional regulation of the ambient temperature response by H2A.Z-nucleosomes and HSF1 transcription factors in Arabidopsis. Mol. Plant 10, 1258–1273 (2017). PubMed PMC
Tasset C., et al. , POWERDRESS-mediated histone deacetylation is essential for thermomorphogenesis in Arabidopsis thaliana. PLoS Genet. 14, e1007280 (2018). PubMed PMC
Shen Y., et al. , Arabidopsis histone deacetylase HDA15 directly represses plant response to elevated ambient temperature. Plant J., 10.1111/tpj.14492 (2019). PubMed DOI
Kumar S. V., H2A.Z at the core of transcriptional regulation in plants. Mol. Plant 11, 1112–1114 (2018). PubMed
Mizuguchi G., et al. , ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303, 343–348 (2004). PubMed
Chen X., et al. , POWERDRESS interacts with HISTONE DEACETYLASE 9 to promote aging in Arabidopsis. eLife 5, e17214 (2016). PubMed PMC
Kim Y. J., et al. , POWERDRESS and HDA9 interact and promote histone H3 deacetylation at specific genomic sites in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 113, 14858–14863 (2016). PubMed PMC
Kang M.-J., Jin H.-S., Noh Y.-S., Noh B., Repression of flowering under a noninductive photoperiod by the HDA9-AGL19-FT module in Arabidopsis. New Phytol. 206, 281–294 (2015). PubMed
Capovilla G., Schmid M., Posé D., Control of flowering by ambient temperature. J. Exp. Bot. 66, 59–69 (2015). PubMed
Verhage L., Angenent G. C., Immink R. G. H., Research on floral timing by ambient temperature comes into blossom. Trends Plant Sci. 19, 583–591 (2014). PubMed
Kim W., Latrasse D., Servet C., Zhou D.-X., Arabidopsis histone deacetylase HDA9 regulates flowering time through repression of AGL19. Biochem. Biophys. Res. Commun. 432, 394–398 (2013). PubMed
Lorrain S., Allen T., Duek P. D., Whitelam G. C., Fankhauser C., Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 53, 312–323 (2008). PubMed
Mayer K. S., et al. , HDA9-PWR-HOS15 is a core histone deacetylase complex regulating transcription and development. Plant Physiol. 180, 342–355 (2019). PubMed PMC
Foreman J., et al. , Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J. 65, 441–452 (2011). PubMed
Yamashino T., et al. , A Link between circadian-controlled bHLH factors and the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol. 44, 619–629 (2003). PubMed
Nusinow D. A., et al. , The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475, 398–402 (2011). PubMed PMC
Yoshida M., Horinouchi S., Beppu T., Trichostatin A and trapoxin: Novel chemical probes for the role of histone acetylation in chromatin structure and function. BioEssays 17, 423–430 (1995). PubMed
Perrella G., et al. , ZINC-FINGER interactions mediate transcriptional regulation of hypocotyl growth in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 115, E4503–E4511 (2018). PubMed PMC
Ma D., et al. , Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light. Proc. Natl. Acad. Sci. U.S.A. 113, 224–229 (2016). PubMed PMC
Zhao Y., et al. , A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291, 306–309 (2001). PubMed
Ha J.-H., Lee H.-J., Jung J.-H., Park C.-M., Thermo-induced maintenance of photo-oxidoreductases underlies plant autotrophic development. Dev. Cell 41, 170–179.e4 (2017). PubMed
Hu Z., et al. , Histone acetyltransferase GCN5 is essential for heat stress-responsive gene activation and thermotolerance in Arabidopsis. Plant J. 84, 1178–1191 (2015). PubMed
van Zanten M., et al. , HISTONE DEACETYLASE 9 represses seedling traits in Arabidopsis thaliana dry seeds. Plant J. 80, 475–488 (2014). PubMed
Perrella G., et al. , Histone deacetylase complex1 expression level titrates plant growth and abscisic acid sensitivity in Arabidopsis. Plant Cell 25, 3491–3505 (2013). PubMed PMC
Li J., Lin Q., Wang W., Wade P., Wong J., Specific targeting and constitutive association of histone deacetylase complexes during transcriptional repression. Genes Dev. 16, 687–692 (2002). PubMed PMC
Tian L., et al. , Reversible histone acetylation and deacetylation mediate genome-wide, promoter-dependent and locus-specific changes in gene expression during plant development. Genetics 169, 337–345 (2005). PubMed PMC
Daxinger L., et al. , Unexpected silencing effects from T-DNA tags in Arabidopsis. Trends Plant Sci. 13, 4–6 (2008). PubMed
Zerzaihi O., Chriett S., Vidal H., Pirola L., Insulin-dependent transcriptional control in L6 rat myotubes is associated with modulation of histone acetylation and accumulation of the histone variant H2A.Z in the proximity of the transcriptional start site. Biochem. Cell Biol. 92, 61–67 (2014). PubMed
Ranjan A., et al. , Nucleosome-free region dominates histone acetylation in targeting SWR1 to promoters for H2A.Z replacement. Cell 154, 1232–1245 (2013). PubMed PMC
Bellstaedt J., et al. , A mobile auxin signal connects temperature sensing in cotyledons with growth responses in hypocotyls. Plant Physiol. 180, 757–766 (2019). PubMed PMC
Yuan L., Chen X., Chen H., Wu K., Huang S., Histone deacetylases HDA6 and HDA9 coordinately regulate valve cell elongation through affecting auxin signaling in Arabidopsis. Biochem. Biophys. Res. Commun. 508, 695–700 (2019). PubMed
Stavang J. A., et al. , Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 60, 589–601 (2009). PubMed
Altaf M., et al. , NuA4-dependent acetylation of nucleosomal histones H4 and H2A directly stimulates incorporation of H2A.Z by the SWR1 complex. J. Biol. Chem. 285, 15966–15977 (2010). PubMed PMC
Liu X., et al. , PHYTOCHROME INTERACTING FACTOR3 associates with the histone deacetylase HDA15 in repression of chlorophyll biosynthesis and photosynthesis in etiolated Arabidopsis seedlings. Plant Cell 25, 1258–1273 (2013). PubMed PMC
Suzuki M., et al. , OLIGOCELLULA1/HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES15 promotes cell proliferation with HISTONE DEACETYLASE9 and POWERDRESS during leaf development in Arabidopsis thaliana. Front. Plant Sci. 9, 580 (2018). PubMed PMC
Lee K., Mas P., Seo P. J., The EC-HDA9 complex rhythmically regulates histone acetylation at the TOC1 promoter in Arabidopsis. Commun. Biol. 2, 143 (2019). PubMed PMC
Park H. J., et al. , HOS15 interacts with the histone deacetylase HDA9 and the evening complex to epigenetically regulate the floral activator GIGANTEA. Plant Cell 31, 37–51 (2019). PubMed PMC
Zhu J.-Y., Oh E., Wang T., Wang Z.-Y., TOC1-PIF4 interaction mediates the circadian gating of thermoresponsive growth in Arabidopsis. Nat. Commun. 7, 13692 (2016). PubMed PMC
Yun J., Kim Y.-S., Jung J.-H., Seo P. J., Park C.-M., The AT-hook motif-containing protein AHL22 regulates flowering initiation by modifying FLOWERING LOCUS T chromatin in Arabidopsis. J. Biol. Chem. 287, 15307–15316 (2012). PubMed PMC
Gu X., Wang Y., He Y., Photoperiodic regulation of flowering time through periodic histone deacetylation of the florigen gene FT. PLoS Biol. 11, e1001649 (2013). PubMed PMC
Reed J. W., Nagpal P., Poole D. S., Furuya M., Chory J., Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5, 147–157 (1993). PubMed PMC
Möller B. K., et al. , Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo. Proc. Natl. Acad. Sci. U.S.A. 114, E2533–E2539 (2017). PubMed PMC
Millenaar F. F., et al. , Differential petiole growth in Arabidopsis thaliana: Photocontrol and hormonal regulation. New Phytol. 184, 141–152 (2009). PubMed
Shimada T. L., Shimada T., Hara-Nishimura I., A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 61, 519–528 (2010). PubMed
Peviani A., Lastdrager J., Hanson J., Snel B., The phylogeny of C/S1 bZIP transcription factors reveals a shared algal ancestry and the pre-angiosperm translational regulation of S1 transcripts. Sci. Rep. 6, 30444 (2016). PubMed PMC
Karimi M., Bleys A., Vanderhaeghen R., Hilson P., Building blocks for plant gene assembly. Plant Physiol. 145, 1183–1191 (2007). PubMed PMC
Clough S. J., Bent A. F., Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998). PubMed
Rahmani F., et al. , Sucrose control of translation mediated by an upstream open reading frame-encoded peptide. Plant Physiol. 150, 1356–1367 (2009). PubMed PMC
Ruyter-Spira C., et al. , Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: Another belowground role for strigolactones? Plant Physiol. 155, 721–734 (2011). PubMed PMC
Pencík A., et al. , Ultra-rapid auxin metabolite profiling for high-throughput mutant screening in Arabidopsis. J. Exp. Bot. 69, 2569–2579 (2018). PubMed PMC
Rappsilber J., Ishihama Y., Mann M., Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663–670 (2003). PubMed
Novák O., et al. , Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 72, 523–536 (2012). PubMed
Rittenberg D., Foster G. L., A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty Acids. J. Biol. Chem. 133, 737–744 (1940).
Nijland W., et al. , Monitoring plant condition and phenology using infrared sensitive consumer grade digital cameras. Agric. For. Meteorol. 184, 98–106 (2014).
Oñate-Sánchez L., Vicente-Carbajosa J., DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques. BMC Res. Notes 1, 93 (2008). PubMed PMC
Livak K. J., Schmittgen T. D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Δ Δ C(T)) Method. Methods 25, 402–408 (2001). PubMed
Trapnell C., Pachter L., Salzberg S. L., TopHat: Discovering splice junctions with RNA-seq. Bioinformatics 25, 1105–1111 (2009). PubMed PMC
Anders S., Pyl P. T., Huber W., HTSeq—A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015). PubMed PMC
Anders S., Huber W., Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010). PubMed PMC
Brown B. A., et al. , A UV-B-specific signaling component orchestrates plant UV protection. Proc. Natl. Acad. Sci. U.S.A. 102, 18225–18230 (2005). PubMed PMC
Kaiserli E., et al. , Integration of light and photoperiodic signaling in transcriptional nuclear foci. Dev. Cell 35, 311–321 (2015). PubMed PMC
Bowler C., et al. , Chromatin techniques for plant cells. Plant J. 39, 776–789 (2004). PubMed
Walter M., et al. , Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428–438 (2004). PubMed
Woude L. C. v. d., Snoek L. B., Verk M. C. v., Zanten M. v., High temperature transcriptomes of mutants in HDA9, PIF4 and Col-0 wild type of young Arabidopsis seedlings. Gene Expression Omnibus (GEO). https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE121383. Deposited 17 October 2018.
Epigenetics and plant hormone dynamics: a functional and methodological perspective
MEDIATOR SUBUNIT17 integrates jasmonate and auxin signaling pathways to regulate thermomorphogenesis