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Volume 49 Issue 1
Jan.  2022
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Article Contents

Nucleolar histone deacetylases HDT1, HDT2, and HDT3 regulate plant reproductive development

doi: 10.1016/j.jgg.2021.10.002
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This work was supported by funding from the National Natural Science Foundation of China (31991203 and 31870295).

  • Received Date: 2021-06-15
  • Accepted Date: 2021-10-14
  • Rev Recd Date: 2021-10-14
  • Publish Date: 2021-10-23
  • Nucleolus is a membrane-less organelle where ribosomes are assembled, and ribosomal RNAs (rRNAs) transcribed and processed. The assembled ribosomes composed of ribosomal proteins and rRNAs synthesize proteins for cell survival. In plants, the loss of nucleolar ribosomal proteins often causes gametophytically or embryonically lethality. The amount of rRNAs are under stringent regulation according to demand and partially switched off by epigenetic modifications. However, the molecular mechanism for the selective activation or silencing is still unclear, and the transcriptional coordination of rRNAs and ribosomal proteins is also unknown. Here, we report the critical role of three Arabidopsis nucleolar proteins HDT1, HDT2, and HDT3 in fertility and transcription of rDNAs and rRNA processing-related genes through histone acetylation. This study highlights the important roles of transcriptional repression of ribosome biogenesis-related genes for plant reproductive development.
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  • Bencivenga, S., Colombo, L., and Masiero, S., 2011. Cross talk between the sporophyte and the megagametophyte during ovule development. Sex. Plant Reprod. 24, 113-121.
    Bourque, S., Jeandroz, S., Grandperret, V., Lehotai, N., Aime, S., Soltis, D.E., Miles, N.W., Melkonian, M., Deyholos, M.K., Leebens-Mack, J.H., et al., 2016. The evolution of HD2 proteins in green plants. Trends Plant Sci. 21, 1008-1016.
    Brambilla, V., Battaglia, R., Colombo, M., Masiero, S., Bencivenga, S., Kater, M.M., and Colombo, L., 2007. Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell 19, 2544-2556.
    Broadhvest, J., Baker, S.C., and Gasser, C.S., 2000. SHORT INTEGUMENTS 2 pro motes growth during Arabidopsis reproductive development. Genetics 155, 899-907.
    Chandrasekhara, C., Mohannath, G., Blevins, T., Pontvianne, F., and Pikaard, C.S., 2016. Chromosome-specific NOR inactivation explains selective rRNA gene silencing and dosage control in Arabidopsis. Genes Dev. 30, 177-190.
    Chen, Z.J., Comai, L., and Pikaard, C.S., 1998. Gene dosage and stochastic effects de termine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. Proc. Nat. Acad. Sci. U S A 95, 14891.
    Chen, X., Lu, L., Qian, S., Scalf, M., Smith, L. M., & Zhong, X., 2018. Canonical and noncanonical actions of Arabidopsis histone deacetylases in ribosomal RNA processing. Plant Cell 30, 134-152.
    Chantha, S.C., Gray-Mitsumune, M., Houde, J., and Matton, D.P., 2010. The MIDASIN and NOTCHLESS genes are essential for female gametophyte development in Arabidopsis thaliana. Physiol. Mol. Biol. Plants 16, 3-18.
    Chevalier, D., Batoux, M., Fulton, L., Pfister, K., Yadav, R.K., Schellenberg, M., and Schneitz, K., 2005. STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc Nat Acad Sci U S A 102, 9074-9079.
    Chevalier, E., Loubert-Hudon, A., Zimmerman, E.L., and Matton, D.P., 2011. Cell-cell communication and signaling pathways within the ovule:from its inception to fertilization. New Phytol. 192, 13-28.
    Colville, A., Alhattab, R., Hu, M., Labbe, H., Xing, T., and Miki, B., 2011. Role of HD2 genes in seed germination and early seedling growth in Arabidopsis. Plant Cell Rep. 30, 1969-1979.
    Durut, N., Abou-Ellail, M., Pontvianne, F., Das, S., Kojima, H., Ukai, S., de Bures, A., Comella, P., Nidelet, S., Rialle, S., et al., 2014. A duplicated NUCLEOLIN gene with antagonistic activity is required for chromatin organization of silent 45S rDNA in Arabidopsis. Plant Cell 26, 1330-1344.
    Feng, C., Cai, X.W., Su, Y.N., Li, L., Chen, S., He, X.J., 2021. Arabidopsis RPD3-like histone deacetylases form multiple complexes involved in stress response. J. Genet. Genomics doi.org/10.1016/j.jgg.2021.04.004.
    Ferretti M.B., and Karbstein K., 2019. Does functional specialization of ribosomes really exist? RNA 25, 521-538.
    Fu Y., Li M., Zhang S., et al., 2020. Analyses of functional conservation and divergence reveal requirement of bHLH010/089/091 for pollen development at elevated temperature in Arabidopsis. J Genet Genomics 47, 477-492.
    Han, Z., Yu, H., Zhao, Z., Hunter, D., Luo, X., Duan, J., and Tian, L., 2016. AtHD2D gene plays a role in plant growth, development, and response to abiotic stresses in Arabidopsis thaliana. Front. Plant Sci. 7, 310.
    Hao, L., Wei, X., Zhu, J., Shi, J., Liu, J., Gu, H., Tsuge, T., and Qu, L.J., 2017. SNAIL1 is essential for female gametogenesis in Arabidopsis thaliana. J. Integr. Plant Biol. 59, 629-641.
    Hill, T.A., Broadhvest, J., Kuzoff, R.K., and Gasser, C.S., 2006. Arabidopsis SHORT INTEGUMENTS 2 is a mitochondrial DAR GTPase. Genetics 174, 707-718.
    Huang, C.K., Huang, L.F., Huang, J.J., Wu, S.J., Yeh, C.H., and Lu, C.A., 2010. A DEAD-box protein, AtRH36, is essential for female gametophyte development and is involved in rRNA biogenesis in Arabidopsis. Plant Cell Physiol. 51, 694-706.
    Huang, X., Run, M., Sun, M.X., 2019. OsGCD1, a novel player in rice intine construction. J. Genet. Genomics 46, 359-362.
    Imai, A., Komura, M., Kawano, E., Kuwashiro, Y., and Takahashi, T., 2008. A semi-dominant mutation in the ribosomal protein L10 gene suppresses the dwarf phenotype of the acl5 mutant in Arabidopsis thaliana. Plant J. 56, 881-890.
    Jia, P.F., Xue, Y., Li, H.J., and Yang, W.C., 2018. Golgi-localized LOT regulates trans-Golgi network biogenesis and pollen tube growth. Proc. Nat. Acad. Sci. U S A 115, 12307-12312
    Klepikova, A.V., Kasianov, A.S., Gerasimov, E.S., Logacheva, M.D., and Penin, A.A., 2016. A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. Plant J. 88, 1058-1070.
    Kutashev, K.O., Franek, M., Diamanti, K., Komorowski, J., Olsinova, M., and Dvorackova, M., 2021. Nucleolar rDNA folds into condensed foci with a specific combination of epigenetic marks. Plant J. 105, 1534-1548.
    Lawrence, R.J., Earley, K., Pontes, O., Silva, M., Chen, Z.J., Neves, N., Viegas, W., and Pikaard, C.S., 2004. A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol. Cell 13, 599-609.
    Lewis, M.S., and Pikaard, C.S., 2001. Restricted chromosomal silencing in nucleolar dominance. Proc. Nat. Acad. Sci. U S A 98, 14536-14540.
    Li, H.J., and Yang, W.C., 2020. Central cell in flowering plants:specification, signaling, and evolution. Frontiers Plant Sci. 11, 590307.
    Li, H., Torres-Garcia, J., Latrasse, D., Benhamed, M., Schilderink, S., Zhou, W., KulI kova, O., Hirt, H., and Bisseling, T., 2017. Plant-specific histone deacetylases HDT1/2 regulate GIBBERELLIN 2-OXIDASE2 expression to control Arabidopsis root meristem cell number. Plant Cell 29, 2183.
    Li, H., and Yang, W., 2016. RLKs orchestrate the signaling in plant male-female interaction. Sci. China Life Sci. 59, 867-877.
    Li, H.J., Liu, N.Y., Shi, D.Q., Liu, J., and Yang, W.C., 2010. YAO is a nucleolar WD40-repeat protein critical for embryogenesis and gametogenesis in Arabidopsis. BMC Plant Biol. 10, 169.
    Li, H.J., Meng, J.G., and Yang, W.C., 2018. Multilayered signaling pathways for pollen tube growth and guidance. Plant Reprod. 31, 31-41.
    Li, H.J., Zhu, S.S., Zhang, M.X., Wang, T., Liang, L., Xue, Y., Shi, D.Q., Liu, J., and Yang, W.C., 2015. Arabidopsis CBP1 is a novel regulator of transcription initiation in central cell-mediated pollen tube guidance. Plant Cell 27, 2880-2893.
    Li, N., Yuan, L., Liu, N., Shi, D., Li, X., Tang, Z., Liu, J., Sundaresan, V., and Yang, W.C., 2009. SLOW WALKER2, a NOC1/MAK21 homologue, is essential for coordinated cell cycle progression during female gametophyte development in Arabidopsis. Plant Physiol. 151, 1486-1497.
    Lieber, D., Lora, J., Schrempp, S., Lenhard, M., and Laux, T., 2011. Arabidopsis WIH1 and WIH2 genes act in the transition from somatic to reproductive cell fate. Curr. Biol. 21, 1009-1017.
    Liu, M., Shi, D.Q., Yuan, L., Liu, J., and Yang, W.C., 2010. SLOW WALKER3, encoding a putative DEAD-box RNA helicase, is essential for female gametogenesis in Arabidopsis. J. Integr. Plant Biol. 52, 817-828.
    Luo, M., Wang, Y.Y., Liu, X., Yang, S., Lu, Q., Cui, Y., and Wu, K., 2012. HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. J. Exp. Bot. 63, 3297-3306.
    Lusser, A., Brosch, G., Loidl, A., Haas, H., and Loidl, P., 1997. Identification of maize histone deacetylase HD2 as an acidic nucleolar phosphoprotein. Science 277, 88-91.
    Matsumura, Y., Ohbayashi, I., Takahashi, H., Kojima, S., Ishibashi, N., Keta, S., Nakagawa, A., Hayashi, R., Saez-Vasquez, J., Echeverria, M., et al., 2016. A genetic link between epigenetic repressor AS1-AS2 and a putative small subunit processome in leaf polarity establishment of Arabidopsis. Biol. Open 5, 942 -954.
    McAbee, J.M., Hill, T.A., Skinner, D.J., Izhaki, A., Hauser, B.A., Meister, R.J., Venugopala Reddy, G., Meyerowitz, E.M., Bowman, J.L., and Gasser, C.S., 2006. ABERRANT TESTA SHAPE encodes a KANADI family member, linking polarity determination to separation and growth of Arabidopsis ovule integuments. Plant J. 46, 522-531.
    McConnell, J.R., and Barton, M.K., 1998. Leaf polarity and meristem formation in Arabidopsis. Development 125, 2935-2942.
    Missbach, S., Weis, B.L., Martin, R., Simm, S., Bohnsack, M.T., and Schleiff, E., 2013. 40S ribosome biogenesis co-factors are essential for gametophyte and embryo development. PLoS One 8, e54084.
    Olmedo-Monfil, V., Duran-Figueroa, N., Arteaga-Vazquez, M., Demesa-Arevalo, E., Autran, D., Grimanelli, D., Slotkin, R.K., Martienssen, R.A., and Vielle-Calzada, J.P., 2010. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464, 628-632.
    Pandey, R., Muller, A., Napoli, C.A., Selinger, D.A., Pikaard, C.S., Richards, E.J., Bender, J., Mount, D.W., and Jorgensen, R.A., 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.
    Park, J., Lim, C.J., Shen, M., Park, H.J., Cha, J.Y., Iniesto, E., Rubio, V., Mengiste, T., Zhu, J.K., Bressan, R.A., et al., 2018. Epigenetic switch from repressive to permissive chromatin in response to cold stress. Proc. Nat. Acad. Sci. U S A 115, E5400-E5409.
    Pillitteri, L.J., Bemis, S.M., Shpak, E.D., and Torii, K.U., 2007. Haploinsufficiency after successive loss of signaling reveals a role for ERECTA-family genes in Arabidopsis ovule development. Development 134, 3099-3109.
    Pontvianne, F., Abou-Ellail, M., Douet, J., Comella, P., Matia, I., Chandrasekhara, C., Debures, A., Blevins, T., Cooke, R., Medina, F.J., et al., 2010. Nucleolin is required for DNA methylation state and the expression of rRNA gene variants in Arabidopsis thaliana. PLoS Genet. 6, e1001225.
    Portereiko, M.F., Sandaklie-Nikolova, L., Lloyd, A., Dever, C.A., Otsuga, D., and Drews, G.N., 2006. NUCLEAR FUSION DEFECTIVE1 encodes the Arabidopsis RPL21M protein and is required for karyogamy during female gametophyte development and fertilization. Plant Physiol. 141, 957-965.
    Ray, A., Robinson-Beers, K., Ray, S., Baker, S.C., Lang, J.D., Preuss, D., Milligan, S.B., and Gasser, C.S., 1994. Arabidopsis floral homeotic gene BELL (BEL1) controls ovule development through negative regulation of AGAMOUS gene (AG). Proc. Nat. Acad. Sci. U S A 91, 5761-5765.
    Robinson-Beers, K., Pruitt, R.E., and Gasser, C.S., 1992. Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4, 1237-1249.
    Saez-Vasquez, J., and Delseny, M., 2019. Ribosome biogenesis in plants:from functional 45S ribosomal DNA organization to ribosome assembly factors. Plant Cell 31, 1945-1967.
    Schmidt, A., Wuest, S.E., Vijverberg, K., Baroux, C., Kleen, D., and Grossniklaus, U., 2011. Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol. 9, e1001155.
    Shi, D.Q., and Yang, W.C., 2011. Ovule development in Arabidopsis:progress and challenge. Curr. Opin. Plant Biol. 14, 74-80.
    Shi, D.Q., Liu, J., Xiang, Y.H., Ye, D., Sundaresan, V., and Yang, W.C., 2005. SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17, 2340-2354.
    Wang H., Liu Y., Bruffett K., Lee J., Hause G., Walker J.C., Zhang S., 2008. Haplo-insufficiency of MPK3 in MPK6 mutant background uncovers a novel function of these two MAPKs in Arabidopsis ovule development. Plant Cell 20, 602-613.
    Wang, J.G., Feng, C., Liu, H.H., Ge, F.R., Li, S., Li, H.J., and Zhang, Y., 2016. HAPLESS13-mediated trafficking of STRUBBELIG is critical for ovule development in Arabidopsis. PLoS Genet. 12, e1006269.
    Weijers, D., Franke-van Dijk, M., Vencken, R.J., Quint, A., Hooykaas, P., and Offringa, R., 2001. An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128, 4289-4299.
    Weis, B.L., Kovacevic, J., Missbach, S., and Schleiff, E., 2015. Plant-specific features of ribosome biogenesis. Trends Plant Sci. 20, 729-740.
    Xiong, F., Duan, C.Y., Liu, H.H., Wu, J.H., Zhang, Z.H., Li, S., and Zhang, Y., 2020. Arabidopsis KETCH1 is critical for the nuclear accumulation of ribosomal proteins and gametogenesis. Plant Cell 32, 1270-1284.
    Yang, W.C., Shi, D.Q., and Chen, Y.H., 2010. Female gametophyte development in flowering plants. Annu. Rev. Plant Biol. 61, 89-108.
    Zhang, M.X., Zhu, S.S., Xu, Y.C., Guo, Y.L., Yang, W.C., and Li, H.J., 2020. Transcriptional repression specifies the central cell for double fertilization. Proc. Nat. Acad. Sci. U S A 117, 6231-6236.
    Zhang, Y., Yin, B., Zhang, J., Cheng, Z., Liu, Y., Wang, B., Guo, X., Liu, X., Liu, D., Li, H., et al., 2019. Histone deacetylase HDT1 is involved in stem vascular development in Arabidopsis. Int. J. Mol. Sci. 20, 3452.
    Zhao, T., Zhan, Z., Jiang, D., 2019. Histone modifications and their regulatory roles in plant development and environmental memory. J. Genet. Genomics 46, 467-476.
    Zsogon, A., Szakonyi, D., Shi, X., and Byrne, M.E., 2014. Ribosomal protein RPL27a promotes female gametophyte development in a dose-dependent manner. Plant Physiol. 165, 1133-1143.
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