The MADS domain transcription factor AGAMOUS (AG) regulates floral meristem termination by preventing maintenance of the histone modification lysine 27 of histone H3 (H3K27me3) along the KNUCKLES (KNU) coding sequence. At 2 d after AG binding, cell division has diluted the repressive mark H3K27me3, allowing activation of KNU transcription prior to floral meristem termination. However, how many other downstream genes are temporally regulated by this intrinsic epigenetic timer and what their functions are remain unknown. Here, we identify direct AG targets regulated through cell cycle-coupled H3K27me3 dilution in Arabidopsis thaliana. Expression of the targets KNU, AT HOOK MOTIF NUCLEAR LOCALIZED PROTEIN18 (AHL18), and PLATZ10 occurred later in plants with longer H3K27me3-marked regions. We established a mathematical model to predict timing of gene expression and manipulated temporal gene expression using the H3K27me3-marked del region from the KNU coding sequence. Increasing the number of del copies delayed and reduced KNU expression in a polycomb repressive complex 2- and cell cycle-dependent manner. Furthermore, AHL18 was specifically expressed in stamens and caused developmental defects when misexpressed. Finally, AHL18 bound to genes important for stamen growth. Our results suggest that AG controls the timing of expression of various target genes via cell cycle-coupled dilution of H3K27me3 for proper floral meristem termination and stamen development.

Department of Biological Chemistry College of Bioscience and Biotechnology Chubu University Kasugai 487 8501 Japan

Department of Biology Faculty of Science Kyushu University Nishi ku 819 0395 Japan

Department of Experimental Plant Biology Faculty of Science Charles University Prague 12844 Czech Republic

Division of Biological Science Graduate School of Science and Technology Nara Institute of Science and Technology Ikoma 630 0192 Japan

Temasek Life Sciences Laboratory National University of Singapore Singapore 117604 Singapore

Zobrazit více v PubMed

Alabert C, Barth TK, Reverón-Gómez N, Sidoli S, Schmidt A, Jensen ON, Imhof A, Groth A. Two distinct modes for propagation of histone PTMs across the cell cycle. Genes Dev. 2015:29(6):585–590. 10.1101/gad.256354.114 PubMed DOI PMC

Aoyanagi T, Ikeya S, Kobayashi A, Kozaki A. Gene regulation via the combination of transcription factors in the INDETERMINATE DOMAIN and GRAS families. Genes (Basel) 2020:11(6):613. 10.3390/genes11060613 PubMed DOI PMC

Bemer M, Grossniklaus U. Dynamic regulation of polycomb group activity during plant development. Curr Opin Plant Biol. 2012:15(5):523–529. 10.1016/j.pbi.2012.09.006 PubMed DOI

Bogliotti YS, Ross PJ. Mechanisms of histone H3 lysine 27 trimethylation remodeling during early mammalian development. Epigenetics 2012:7(9):976–981. 10.4161/epi.21615 PubMed DOI PMC

Bollier N, Sicard A, Leblond J, Latrasse D, Gonzalez N, Gévaudant F, Benhamed M, Raynaud C, Lenhard M, Chevalier C, et al. . At-MINI ZINC FINGER2 and SI-INHIBITOR OF MERISTEM ACTIVITY, a conserved missing link in the regulation of floral meristem termination in Arabidopsis and tomato. Plant Cell 2018:30(1):83–100. 10.1105/tpc.17.00653 PubMed DOI PMC

Bosco CD, Lezhneva L, Biehl A, Leister D, Strotmann H, Wanner G, Meurer J. Inactivation of the chloroplast ATP synthase γ subunit results in high non-photochemical fluorescence quenching and altered nuclear gene expression in Arabidopsis thaliana. J Biol Chem. 2004:279(2):1060–1069. 10.1074/jbc.M308435200 PubMed DOI

Chen L, Wang F, Wang X, Liu Y-G. Robust one-tube Ω-PCR strategy accelerates precise sequence modification of plasmids for functional genomics. Plant Cell Physiol. 2013:54(4):634–642. 10.1093/pcp/pct009 PubMed DOI PMC

Cheng Y, Cao L, Wang S, Li Y, Shi X, Liu H, Li L, Zhang Z, Fowke LC, Wang H, et al. . Downregulation of multiple CDK inhibitor ICK/KRP genes upregulates the E2F pathway and increases cell proliferation, and organ and seed sizes in Arabidopsis. Plant J. 2013:75(4):642–655. 10.1111/tpj.12228 PubMed DOI

Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J. Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet. 2009:5(3):e1000440. 10.1371/journal.pgen.1000440 PubMed DOI PMC

Churchman ML, Brown ML, Kato N, Kirik V, Hülskamp M, Inzé D, De Veylder L, Walker JD, Zheng Z, Oppenheimer DG, et al. . SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell 2006:18(11):3145–3157. 10.1105/tpc.106.044834 PubMed DOI PMC

Di Mambro R, De Ruvo M, Pacifici E, Salvi E, Sozzani R, Benfey PN, Busch W, Novak O, Ljung K, Di Paola L, et al. . Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root. Proc Natl Acad Sci USA. 2017:114(36):E7641–E7649. 10.1073/pnas.1705833114 PubMed DOI PMC

Doyle MR, Amasino RM. A single amino acid change in the enhancer of zeste ortholog CURLY LEAF results in vernalization-independent, rapid flowering in Arabidopsis. Plant Physiol. 2009:151(3):1688–1697. 10.1104/pp.109.145581 PubMed DOI PMC

Eccleston A, Cesari F, Skipper M. Transcription and epigenetics. Nature 2013:502(7472):461. 10.1038/502461a PubMed DOI

Frigerio M, Alabadí D, Pérez-Gómez J, García-Cárcel L, Phillips AL, Hedden P, Blázquez MA. Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol. 2006:142(2):553–563. 10.1104/pp.106.084871 PubMed DOI PMC

Gong W, Shen YP, Ma LG, Pan Y, Du YL, Wang DH, Yang JY, Hu LD, Liu XF, Dong CX, et al. . Genome-Wide ORFeome cloning and analysis of Arabidopsis transcription factor genes. Plant Physiol. 2004:135(2):773–782. 10.1104/pp.104.042176 PubMed DOI PMC

González-Morales SI, Chávez-Montes RA, Hayano-Kanashiro C, Alejo-Jacuinde G, Rico-Cambron TY, de Folter S, Herrera-Estrella L. Regulatory network analysis reveals novel regulators of seed desiccation tolerance in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2016:113(35):E5232–E5241. 10.1073/pnas.1610985113 PubMed DOI PMC

Gross T, Becker A. Transcription factor action orchestrates the complex expression pattern of CRABS CLAW in Arabidopsis. Genes (Basel) 2021:12(11):1663. 10.3390/genes12111663 PubMed DOI PMC

Hanada K, Sawada Y, Kuromori T, Klausnitzer R, Saito K, Toyoda T, Shinozaki K, Li W-H, Hirai MY. Functional compensation of primary and secondary metabolites by duplicate genes in Arabidopsis thaliana. Mol Biol Evol. 2011:28(1):377–382. 10.1093/molbev/msq204 PubMed DOI PMC

Harashima H, Sekine M. Cyclin-dependent protein kinases in the control of cell cycle in plants. In: Protein kinases and stress signaling in plants. New York: John Wiley & Sons, Ltd; 2020. p. 347–368.

Huang R, Huang T, Irish VF. Do epigenetic timers control petal development? Front Plant Sci. 2021:12:709360. 10.3389/fpls.2021.709360 PubMed DOI PMC

Ikeuchi M, Iwase A, Sugimoto K. Control of plant cell differentiation by histone modification and DNA methylation. Curr Opin Plant Biol. 2015:28:60–67. 10.1016/j.pbi.2015.09.004 PubMed DOI

Ito T, Ng K-H, Lim T-S, Yu H, Meyerowitz EM. The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell 2007:19(11):3516–3529. 10.1105/tpc.107.055467 PubMed DOI PMC

Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann JL, Meyerowitz EM. The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 2004:430(6997):356–360. 10.1038/nature02733 PubMed DOI

Iwata E, Ikeda S, Matsunaga S, Kurata M, Yoshioka Y, Criqui M-C, Genschik P, Ito M. GIGAS CELL1, a novel negative regulator of the anaphase-promoting complex/cyclosome, is required for proper mitotic progression and cell fate determination in Arabidopsis. Plant Cell 2011:23(12):4382–4393. 10.1105/tpc.111.092049 PubMed DOI PMC

Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol. 2005:15(17):1560–1565. 10.1016/j.cub.2005.07.023 PubMed DOI

Katz A, Oliva M, Mosquna A, Hakim O, Ohad N. FIE And CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J. 2004:37(5):707–719. 10.1111/j.1365-313X.2003.01996.x PubMed DOI

Kim D-H, Sung S. Polycomb-mediated gene silencing in Arabidopsis thaliana. Mol Cells. 2014:37(12):841–850. 10.14348/molcells.2014.0249 PubMed DOI PMC

Kumar N, Larkin JC. Why do plants need so many cyclin-dependent kinase inhibitors? Plant Signal Behav. 2017:12(2):e1282021. 10.1080/15592324.2017.1282021 PubMed DOI PMC

Kumar M, Le DT, Hwang S, Seo PJ, Kim HU. Role of the INDETERMINATE DOMAIN genes in plants. Int J Mol Sci. 2019:20(9):2286. 10.3390/ijms20092286 PubMed DOI PMC

Kuusk S, Sohlberg JJ, Long JA, Fridborg I, Sundberg E. STY1 and STY2 promote the formation of apical tissues during Arabidopsis gynoecium development. Development 2002:129(20):4707–4717. 10.1242/dev.129.20.4707 PubMed DOI

Kwaśniewska K, Breathnach C, Fitzsimons C, Goslin K, Thomson B, Beegan J, Finocchio A, Prunet N, Ó’Maoiléidigh DS, Wellmer F. Expression of KNUCKLES in the stem cell domain is required for its function in the control of floral meristem activity in Arabidopsis. Front Plant Sci. 2021:12:704351. 10.3389/fpls.2021.704351 PubMed DOI PMC

Lai WKM, Pugh BF. Understanding nucleosome dynamics and their links to gene expression and DNA replication. Nat Rev Mol Cell Biol. 2017:18(9):548–562. 10.1038/nrm.2017.47 PubMed DOI PMC

Lebedev V. Stability of transgene inheritance in progeny of field-grown pear trees over a 7-year period. Plants 2022:11(2):151. 10.3390/plants11020151 PubMed DOI PMC

Lee K, Seo PJ. Coordination of matrix attachment and ATP-dependent chromatin remodeling regulate auxin biosynthesis and Arabidopsis hypocotyl elongation. PLoS One 2017:12(7):e0181804. 10.1371/journal.pone.0181804 PubMed DOI PMC

Lenhard M, Bohnert A, Jürgens G, Laux T. Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 2001:105(6):805–814. 10.1016/S0092-8674(01)00390-7 PubMed DOI

Li Q, Wang J, Ye J, Zheng X, Xiang X, Li C, Fu M, Wang Q, Zhang Z, Wu Y. The maize imprinted gene Floury3 encodes a PLATZ protein required for tRNA and 5S rRNA transcription through interaction with RNA polymerase III. Plant Cell 2017:29(10):2661–2675. 10.1105/tpc.17.00576 PubMed DOI PMC

Li X-C, Zhu J, Yang J, Zhang G-R, Xing W-F, Zhang S, Yang Z-N. Glycerol-3-phosphate acyltransferase 6 (GPAT6) is important for tapetum development in Arabidopsis and plays multiple roles in plant fertility. Mol Plant. 2012:5(1):131–142. 10.1093/mp/ssr057 PubMed DOI

Lim PO, Kim Y, Breeze E, Koo JC, Woo HR, Ryu JS, Park DH, Beynon J, Tabrett A, Buchanan-Wollaston V, et al. . Overexpression of a chromatin architecture-controlling AT-hook protein extends leaf longevity and increases the post-harvest storage life of plants. Plant J. 2007:52(6):1140–1153. 10.1111/j.1365-313X.2007.03317.x PubMed DOI

Liu J, Deng S, Wang H, Ye J, Wu H-W, Sun H-X, Chua N-H. CURLY LEAF regulates gene sets coordinating seed size and lipid biosynthesis. Plant Physiol. 2016:171(1):424–436. 10.1104/pp.15.01335 PubMed DOI PMC

Liu X, Kim YJ, Müller R, Yumul RE, Liu C, Pan Y, Cao X, Goodrich J, Chen X. AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of polycomb group proteins. Plant Cell 2011:23(10):3654–3670. 10.1105/tpc.111.091538 PubMed DOI PMC

Liu S, Yang R, Liu M, Zhang S, Yan K, Yang G, Huang J, Zheng C, Wu C. PLATZ2 Negatively regulates salt tolerance in Arabidopsis seedlings by directly suppressing the expression of the CBL4/SOS3 and CBL10/SCaBP8 genes. J Exp Bot. 2020:71(18):5589–5602. 10.1093/jxb/eraa259 PubMed DOI

Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D. A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 2001:105(6):793–803. 10.1016/S0092-8674(01)00384-1 PubMed DOI

Ma C, Haslbeck M, Babujee L, Jahn O, Reumann S. Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant Physiol. 2006:141(1):47–60. 10.1104/pp.105.073841 PubMed DOI PMC

Matsushita A, Furumoto T, Ishida S, Takahashi Y. AGF1, an AT-Hook protein, is necessary for the negative feedback of AtGA3ox1 encoding GA 3-oxidase. Plant Physiol. 2007:143(3):1152–1162. 10.1104/pp.106.093542 PubMed DOI PMC

Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 1998:95(6):805–815. 10.1016/S0092-8674(00)81703-1 PubMed DOI

Michael TP, Mockler TC, Breton G, McEntee C, Byer A, Trout JD, Hazen SP, Shen R, Priest HD, Sullivan CM, et al. . Network discovery pipeline elucidates conserved time-of-day–specific cis-regulatory modules. PLoS Genet. 2008:4(2):e14. 10.1371/journal.pgen.0040014 PubMed DOI PMC

Mozgova I, Hennig L. The polycomb group protein regulatory network. Annu Rev Plant Biol. 2015:66(1):269–296. 10.1146/annurev-arplant-043014-115627 PubMed DOI

Mozgova I, Köhler C, Hennig L. Keeping the gate closed: functions of the polycomb repressive complex PRC2 in development. Plant J. 2015:83(1):121–132. 10.1111/tpj.12828 PubMed DOI

Nagano Y, Furuhashi H, Inaba T, Sasaki Y. A novel class of plant-specific zinc-dependent DNA-binding protein that binds to A/T-rich DNA sequences. Nucleic Acids Res. 2001:29(20):4097–4105. 10.1093/nar/29.20.4097 PubMed DOI PMC

Ng K-H, Yu H, Ito T. AGAMOUS controls GIANT KILLER, a multifunctional chromatin modifier in reproductive organ patterning and differentiation. PLoS Biol. 2009:7(11):e1000251. 10.1371/journal.pbio.1000251 PubMed DOI PMC

Ó’Maoiléidigh DS, Wuest SE, Rae L, Raganelli A, Ryan PT, Kwaśniewska K, Das P, Lohan AJ, Loftus B, Graciet E, et al. . Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS. Plant Cell 2013:25(7):2482–2503. 10.1105/tpc.113.113209 PubMed DOI PMC

Pajoro A, Madrigal P, Muiño JM, Matus J, Jin J, Mecchia MA, Debernardi JM, Palatnik JF, Balazadeh S, Arif M, et al. . Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development. Genome Biol. 2014:15(3):R41. 10.1186/gb-2014-15-3-r41 PubMed DOI PMC

Parcy F, Nilsson O, Busch MA, Lee I, Weigel D. A genetic framework for floral patterning. Nature 1998:395(6702):561–566. 10.1038/26903 PubMed DOI

Payne T, Johnson SD, Koltunow AM. KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium. Development 2004:131(15):3737–3749. 10.1242/dev.01216 PubMed DOI

Pelayo MA, Yamaguchi N, Ito T. One factor, many systems: the floral homeotic protein AGAMOUS and its epigenetic regulatory mechanisms. Curr Opin Plant Biol. 2021:61:102009. 10.1016/j.pbi.2021.102009 PubMed DOI

Planchais S, Glab N, Inzé D, Bergounioux C. Chemical inhibitors: a tool for plant cell cycle studies. FEBS Lett. 2000:476(1–2):78–83. 10.1016/S0014-5793(00)01675-6 PubMed DOI

Probst AV, Dunleavy E, Almouzni G. Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol. 2009:10(3):192–206. 10.1038/nrm2640 PubMed DOI

Prunet N, Morel P, Thierry AM, Eshed Y, Bowman JL, Negrutiu I, Trehin C. REBELOTE, SQUINT, and ULTRAPETALA1 function redundantly in the temporal regulation of floral meristem termination in Arabidopsis thaliana. Plant Cell. 2008:20(4):901–919. 10.1105/tpc.107.053306 PubMed DOI PMC

Ramachandran S, Henikoff S. Replicating nucleosomes. Sci Adv. 2015:1(7):e1500587. 10.1126/sciadv.1500587 PubMed DOI PMC

Reddy GV, Heisler MG, Ehrhardt DW, Meyerowitz EM. Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 2004:131(17):4225–4237. 10.1242/dev.01261 PubMed DOI

Riechmann JL, Heard J, Martin G, Reuber L, Jiang C-Z, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, et al. . Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 2000:290(5499):2105–2110. 10.1126/science.290.5499.2105 PubMed DOI

Ross PJ, Ragina NP, Rodriguez RM, Iager AE, Siripattarapravat K, Lopez-Corrales N, Cibelli JB. Polycomb gene expression and histone H3 lysine 27 trimethylation changes during bovine preimplantation development. Reproduction 2008:136(6):777–785. 10.1530/REP-08-0045 PubMed DOI

Ryan PT, Ó’Maoiléidigh DS, Drost HG, Kwaśniewska K, Gabel A, Grosse I, Graciet E, Quint M, Wellmer F. Patterns of gene expression during Arabidopsis flower development from the time of initiation to maturation. BMC Genom. 2015:16:488. 10.1186/s12864-015-1699-6 PubMed DOI PMC

Sablowski R. Flowering and determinacy in Arabidopsis. J Exp Bot. 2007:58(5):899–907. 10.1093/jxb/erm002 PubMed DOI

Shang E, Ito T, Sun B. Control of floral stem cell activity in Arabidopsis. Plant Signal Behav. 2019:14(11):1659706. 10.1080/15592324.2019.1659706 PubMed DOI PMC

Shang E, Wang X, Li T, Guo F, Ito T, Sun B. Robust control of floral meristem determinacy by position-specific multifunctions of KNUCKLES. Proc Natl Acad Sci USA. 2021:118(36):e2102826118. 10.1073/pnas.2102826118 PubMed DOI PMC

Širl M, Šnajdrová T, Gutiérrez-Alanís D, Dubrovsky JG, Vielle-Calzada JP, Kulich I, Soukup A. At-Hook motif nuclear localised protein 18 as a novel modulator of root system architecture. Int J Mol Sci. 2020:21(5):1886. 10.3390/ijms21051886 PubMed DOI PMC

Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in Arabidopsis. Plant Cell. 1990:2(8):755–767. 10.1105/tpc.2.8.755 PubMed DOI PMC

Sohlberg JJ, Myrenås M, Kuusk S, Lagercrantz U, Kowalczyk M, Sandberg G, Sundberg E. STY1 regulates auxin homeostasis and affects apical–basal patterning of the Arabidopsis gynoecium. Plant J. 2006:47(1):112–123. 10.1111/j.1365-313X.2006.02775.x PubMed DOI

Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, Xie D. The jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect jasmonate-regulated stamen development in Arabidopsis. Plant Cell 2011:23(3):1000–1013. 10.1105/tpc.111.083089 PubMed DOI PMC

Street IH, Shah PK, Smith AM, Avery N, Neff MM. The AT-hook-containing proteins SOB3/AHL29 and ESC/AHL27 are negative modulators of hypocotyl growth in Arabidopsis. Plant J. 2008:54(1):1–14. 10.1111/j.1365-313X.2007.03393.x PubMed DOI

Sun B, Ito T. Regulation of floral stem cell termination in Arabidopsis. Front Plant Sci. 2015:6:17. 10.3389/fpls.2015.00017 PubMed DOI PMC

Sun B, Looi L-S, Guo S, He Z, Gan E-S, Huang J, Xu Y, Wee W-Y, Ito T. Timing mechanism dependent on cell division is invoked by polycomb eviction in plant stem cells. Science 2014:343(6170):1248559. 10.1126/science.1248559 PubMed DOI

Sun B, Xu Y, Ng K-H, Ito T. A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev. 2009:23(15):1791–1804. 10.1101/gad.1800409 PubMed DOI PMC

Sun B, Zhou Y, Cai J, Shang E, Yamaguchi N, Xiao J, Looi L-S, Wee W-Y, Gao X, Wagner D, et al. . Integration of transcriptional repression and polycomb-mediated silencing of WUSCHEL in floral meristems. Plant Cell 2019:31(7):1488–1505. 10.1105/tpc.18.00450 PubMed DOI PMC

Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013:14(2):178–192. 10.1093/bib/bbs017 PubMed DOI PMC

Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 2017:45(W1):W122–W129. 10.1093/nar/gkx382 PubMed DOI PMC

Veylder LD, Beeckman T, Beemster GTS, Krols L, Terras F, Landrieu I, Schueren EVD, Maes S, Naudts M, Inzé D. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 2001:13(7):1653–1668. 10.1105/TPC.010087 PubMed DOI PMC

Wang A, Hou Q, Si L, Huang X, Luo J, Lu D, Zhu J, Shangguan Y, Miao J, Xie Y, et al. . The PLATZ transcription factor GL6 affects grain length and number in rice1[OPEN]. Plant Physiol. 2019:180(4):2077–2090. 10.1104/pp.18.01574 PubMed DOI PMC

Wang J, Ji C, Li Q, Zhou Y, Wu Y. Genome-wide analysis of the plant-specific PLATZ proteins in maize and identification of their general role in interaction with RNA polymerase III complex. BMC Plant Biol. 2018:18(1):221. 10.1186/s12870-018-1443-x PubMed DOI PMC

Weigel D, Glazebrook J. Arabidopsis: a laboratory manual. CSHL Press; 2002.

Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM. Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet. 2006:2(7):e117. 10.1371/journal.pgen.0020117 PubMed DOI PMC

Wigge PA. Ambient temperature signalling in plants. Curr Opin Plant Biol. 2013:16(5):661–666. 10.1016/j.pbi.2013.08.004 PubMed DOI

Wong MM, Bhaskara GB, Wen T-N, Lin W-D, Nguyen TT, Chong GL, Verslues PE. Phosphoproteomics of Arabidopsis highly ABA-induced1 identifies AT-Hook–Like10 phosphorylation required for stress growth regulation. Proc Natl Acad Sci USA. 2019:116(6):2354–2363. 10.1073/pnas.1819971116 PubMed DOI PMC

Xiao C, Chen F, Yu X, Lin C, Fu Y-F. Over-expression of an AT-hook gene, AHL22, delays flowering and inhibits the elongation of the hypocotyl in Arabidopsis thaliana. Plant Mol Biol. 2009:71(1–2):39–50. 10.1007/s11103-009-9507-9 PubMed DOI

Xiao J, Jin R, Yu X, Shen M, Wagner JD, Pai A, Song C, Zhuang M, Klasfeld S, He C, et al. . Cis and trans determinants of epigenetic silencing by polycomb repressive complex 2 in Arabidopsis. Nat Genet. 2017:49(10):1546–1552. 10.1038/ng.3937 PubMed DOI

Xu Y, Yamaguchi N, Gan E-S, Ito T. When to stop: an update on molecular mechanisms of floral meristem termination. J Exp Bot. 2019:70(6):1711–1718. 10.1093/jxb/erz048 PubMed DOI

Yadeta KA, Hanemian M, Smit P, Hiemstra JA, Pereira A, Marco Y, Thomma BPHJ. The Arabidopsis thaliana DNA-binding protein AHL19 mediates Verticillium wilt resistance. MPMI. 2011:24(12):1582–1591. 10.1094/MPMI-04-11-0090 PubMed DOI

Yamaguchi N. The epigenetic mechanisms regulating floral hub genes and their potential for manipulation. J Exp Bot. 2022:73(5):1277–1287. 10.1093/jxb/erab490 PubMed DOI

Yamaguchi N, Huang J, Tatsumi Y, Abe M, Sugano SS, Kojima M, Takebayashi Y, Kiba T, Yokoyama R, Nishitani K, et al. . Chromatin-mediated feed-forward auxin biosynthesis in floral meristem determinacy. Nat Commun. 2018:9(1):5290. 10.1038/s41467-018-07763-0 PubMed DOI PMC

Yamaguchi N, Huang J, Xu Y, Tanoi K, Ito T. Fine-tuning of auxin homeostasis governs the transition from floral stem cell maintenance to gynoecium formation. Nat Commun. 2017:8(1):1125. 10.1038/s41467-017-01252-6 PubMed DOI PMC

Yamaguchi N, Matsubara S, Yoshimizu K, Seki M, Hamada K, Kamitani M, Kurita Y, Nomura Y, Nagashima K, Inagaki S, et al. . H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis. Nat Commun. 2021:12(1):616. 10.1038/s41467-021-23766-w PubMed DOI PMC

Yamaguchi N, Winter CM, Wu M-F, Kwon CS, William DA, Wagner D. PROTOCOLS: chromatin immunoprecipitation from Arabidopsis tissues. Arabidopsis Book 2014:12:e0170. 10.1199/tab.0170 PubMed DOI PMC

Yan W, Chen D, Schumacher J, Durantini D, Engelhorn J, Chen M, Carles CC, Kaufmann K. Dynamic control of enhancer activity drives stage-specific gene expression during flower morphogenesis. Nat Commun. 2019:10(1):1705. 10.1038/s41467-019-09513-2 PubMed DOI PMC

Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 1990:346(6279):35–39. 10.1038/346035a0 PubMed DOI

Yoon K-J, Vissers C, Ming G, Song H. Epigenetics and epitranscriptomics in temporal patterning of cortical neural progenitor competence. J Cell Biol. 2018:217(6):1901–1914. 10.1083/jcb.201802117 PubMed DOI PMC

Yun J, Kim Y-S, Jung J-H, Seo PJ, Park C-M. The AT-hook motif-containing protein AHL22 regulates flowering initiation by modifying FLOWERING LOCUS T chromatin in Arabidopsis. J Biol Chem. 2012:287(19):15307–15316. 10.1074/jbc.M111.318477 PubMed DOI PMC

Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 2007:5(5):e129. 10.1371/journal.pbio.0050129 PubMed DOI PMC

Zhang W-M, Fang D, Cheng X-Z, Cao J, Tan X-L. Insights into the molecular evolution of AT-hook motif nuclear localization genes in Brassica napus. Front Plant Sci. 2021a:12:714305. 10.3389/fpls.2021.714305 PubMed DOI PMC

Zhang X, He Y, Li L, Liu H, Hong G. Involvement of the R2R3-MYB transcription factor MYB21 and its homologs in regulating flavonol accumulation in Arabidopsis stamen. J Exp Bot. 2021b:72(12):4319–4332. 10.1093/jxb/erab156 PubMed DOI PMC

Zhang S, Yang R, Huo Y, Liu S, Yang G, Huang J, Zheng C, Wu C. Expression of cotton PLATZ1 in transgenic Arabidopsis reduces sensitivity to osmotic and salt stress for germination and seedling establishment associated with modification of the abscisic acid, gibberellin, and ethylene signalling pathways. BMC Plant Biol. 2018:18(1):218. 10.1186/s12870-018-1416-0 PubMed DOI PMC

Zhao J, Favero DS, Peng H, Neff MM. Arabidopsis thaliana AHL family modulates hypocotyl growth redundantly by interacting with each other via the PPC/DUF296 domain. Proc Natl Acad Sci USA. 2013:110(48):E4688–E4697. 10.1073/pnas.1219277110 PubMed DOI PMC

Zhou Y, Wang H, Gilmer S, Whitwill S, Fowke LC. Effects of co-expressing the plant CDK inhibitor ICK1 and D-type cyclin genes on plant growth, cell size and ploidy in Arabidopsis thaliana. Planta 2003:216(4):604–613. 10.1007/s00425-002-0935-x PubMed DOI

Zhou J, Wang X, Lee J-Y, Lee J-Y. Cell-to-cell movement of two interacting AT-hook factors in Arabidopsis root vascular tissue patterning. Plant Cell 2013:25(1):187–201. 10.1105/tpc.112.102210 PubMed DOI PMC

Zik M, Irish VF. Flower development: initiation, differentiation, and diversification. Annu Rev Cell Dev Biol. 2003:19(1):119–140. 10.1146/annurev.cellbio.19.111301.134635 PubMed DOI