An Arabidopsis AT-hook motif nuclear protein mediates somatic embryogenesis and coinciding genome duplication.

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Abstrakt

Tytuł:: An Arabidopsis AT-hook motif nuclear protein mediates somatic embryogenesis and coinciding genome duplication.
Autorzy:: Karami O; Plant Developmental Genetics, Institute of Biology Leiden, Leiden University, Leiden, Netherlands. .
Rahimi A; Plant Developmental Genetics, Institute of Biology Leiden, Leiden University, Leiden, Netherlands.
Mak P; Plant Developmental Genetics, Institute of Biology Leiden, Leiden University, Leiden, Netherlands.; Sanquin Plasma Products B.V., Amsterdam, Netherlands.
Horstman A; Bioscience, Wageningen University and Research, Wageningen, Netherlands.; Laboratory of Molecular Biology, Wageningen University and Research, Wageningen, Netherlands.
Boutilier K; Bioscience, Wageningen University and Research, Wageningen, Netherlands.
Compier M; Plant Developmental Genetics, Institute of Biology Leiden, Leiden University, Leiden, Netherlands.; Rijk Zwaan Netherlands B.V., De Lier, The Netherlands.
van der Zaal B; Plant Developmental Genetics, Institute of Biology Leiden, Leiden University, Leiden, Netherlands.
Offringa R; Plant Developmental Genetics, Institute of Biology Leiden, Leiden University, Leiden, Netherlands. .
Źródło:: Nature communications [Nat Commun] 2021 May 04; Vol. 12 (1), pp. 2508. Date of Electronic Publication: 2021 May 04.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Original Publication: [London] : Nature Pub. Group
MeSH Terms:: AT-Hook Motifs*
Plant Somatic Embryogenesis Techniques*
Arabidopsis/*embryology
Arabidopsis/*genetics
Arabidopsis Proteins/*metabolism
Chromatin Assembly and Disassembly/*genetics
Gene Expression Regulation, Plant/*genetics
Arabidopsis Proteins/genetics ; Chromosome Segregation/genetics ; Gene Duplication ; Gene Expression Regulation, Plant/drug effects ; Heat-Shock Response/genetics ; Histone Deacetylase Inhibitors/pharmacology ; Hydroxamic Acids/pharmacology ; Polyploidy ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Up-Regulation
References:: Yarbrough, J. A. Anatomical and developmental studies of the foliar embryos of Bryophyllum calycinum. Am. J. Bot. 19, 443–453 (1932). (PMID: 10.1002/j.1537-2197.1932.tb09663.x)
Taylor, R. L. The foliar embryos of Malaxis paludosa. Can. J. Bot. 45, 1553–1556 (1967). (PMID: 10.1139/b67-159)
Ozias-Akins, P. & van Dijk, P. J. Mendelian genetics of apomixis in plants. Annu. Rev. Genet. 41, 509–537 (2007). (PMID: 1807633110.1146/annurev.genet.40.110405.090511)
Hand, M. L. & Koltunow, A. M. G. The genetic control of apomixis: asexual seed formation. Genetics 197, 441–450 (2014). (PMID: 24939990406390510.1534/genetics.114.163105)
Birnbaum, K. D. & Sánchez Alvarado, A. Slicing across kingdoms: regeneration in plants and animals. Cell 132, 697–710 (2008). (PMID: 18295584269230810.1016/j.cell.2008.01.040)
Smertenko, A. & Bozhkov, P. V. Somatic embryogenesis: life and death processes during apical-basal patterning. J. Exp. Bot. 65, 1343–1360 (2014). (PMID: 2462295310.1093/jxb/eru005)
Bhojwani, S. S. Plant Tissue Culture: Applications and Limitations (Elsevier B.V., 2012).
Gaj, M. D. Direct somatic embryogenesis as a rapid and efficient system for in vitro regeneration of Arabidopsis thaliana. Plant Cell Tissue Organ Cult. 64, 39–46 (2001). (PMID: 10.1023/A:1010679614721)
Jiménez, V. M. Involvement of plant hormones and plant growth regulators on in vitro somatic embryogenesis. Plant Growth Regul. 47, 91–110 (2005). (PMID: 10.1007/s10725-005-3478-x)
Horstman, A., Bemer, M. & Boutilier, K. A transcriptional view on somatic embryogenesis. Regeneration 4, 201–206 (2017). (PMID: 29299323574378410.1002/reg2.91)
Lotan, T. et al. Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93, 1195–1205 (1998). (PMID: 965715210.1016/S0092-8674(00)81463-4)
Stone, S. L. et al. LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc. Natl Acad. Sci. 98, 11806–11811 (2001). (PMID: 1157301410.1073/pnas.20141349858812)
Boutilier, K. et al. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14, 1737–1749 (2002). (PMID: 1217201915146210.1105/tpc.001941)
Zuo, J., Niu, Q.-W., Frugis, G. & Chua, N.-H. The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J. 30, 349–359 (2002). (PMID: 1200068210.1046/j.1365-313X.2002.01289.x)
Aravind, L. & Landsman, D. AT-hook motifs identified in a wide variety of DNA-binding proteins. Nucleic Acids Res. 26, 4413–4421 (1998). (PMID: 974224314787110.1093/nar/26.19.4413)
Reeves, R. Nuclear functions of the HMG proteins. Biochim. Biophys. Acta 1799, 3–14 (2010). (PMID: 1974860510.1016/j.bbagrm.2009.09.001)
Sgarra, R. et al. HMGA molecular network: from transcriptional regulation to chromatin remodeling. Biochim. Biophys. Acta 1799, 37–47 (2010). (PMID: 1973285510.1016/j.bbagrm.2009.08.009)
Fujimoto, S. et al. Identification of a novel plant MAR DNA binding protein localized on chromosomal surfaces. Plant Mol. Biol. 56, 225–239 (2004). (PMID: 1560474010.1007/s11103-004-3249-5)
Zhao, J., Favero, D. S., Peng, H. & Neff, M. M. Arabidopsis thaliana AHL family modulates hypocotyl growth redundantly by interacting with each other via the PPC/DUF296 domain. Proc. Natl Acad. Sci. 110, E4688–E4697 (2013). (PMID: 2421860510.1073/pnas.12192771103845178)
Street, I. H., Shah, P. K., Smith, A. M., Avery, N. & Neff, M. M. The AT-hook-containing proteins SOB3/AHL29 and ESC/AHL27 are negative modulators of hypocotyl growth in Arabidopsis. Plant J. 54, 1–14 (2008). (PMID: 1808831110.1111/j.1365-313X.2007.03393.x)
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. 71, 39–50 (2009). (PMID: 1951725210.1007/s11103-009-9507-9)
Ng, K.-H., Yu, H. & Ito, T. AGAMOUS controls GIANT KILLER, a multifunctional chromatin modifier in reproductive organ patterning and differentiation. PLoS Biol. 7, e1000251 (2009). (PMID: 19956801277434110.1371/journal.pbio.1000251)
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 25, 187–201 (2013). (PMID: 23335615358453310.1105/tpc.112.102210)
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. 143, 1152–1162 (2007). (PMID: 17277098182092610.1104/pp.106.093542)
Karami, O. et al. A suppressor of axillary meristem maturation promotes longevity in flowering plants. Nat. Plants 6, 368–376 (2020). (PMID: 3228455110.1038/s41477-020-0637-z)
van der Zaal, E. J. & Hooykaas, P. J. J. Control of plant growth and developmental processes. WO2004/066985, https://patentscope.wipo.int/search/en/detail.jsf?docId=WO2004069865 (2004).
Lim, P. O. 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. 52, 1140–1153 (2007). (PMID: 1797103910.1111/j.1365-313X.2007.03317.x)
Himes, S. R. et al. The role of high-mobility group I(Y) proteins in expression of IL-2 and T cell proliferation. J. Immunol. 164, 3157–3168 (2000). (PMID: 1070670610.4049/jimmunol.164.6.3157)
Khanday, I., Skinner, D., Yang, B., Mercier, R. & Sundaresan, V. A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature 565, 91–95 (2019). (PMID: 3054215710.1038/s41586-018-0785-8)
Horstman, A. et al. AIL and HDG proteins act antagonistically to control cell proliferation. Development 142, 454–464 (2015). (PMID: 25564655)
Catez, F. et al. Network of dynamic interactions between histone H1 and high-mobility-group proteins in chromatin. Mol. Cell. Biol. https://doi.org/10.1128/MCB.24.10.4321 . (2004).
Kishi, Y., Fujii, Y., Hirabayashi, Y. & Gotoh, Y. HMGA regulates the global chromatin state and neurogenic potential in neocortical precursor cells. Nat. Neurosci. 15, 1127–1133 (2012). (PMID: 2279769510.1038/nn.3165)
Jagannathan, M., Cummings, R. & Yamashita, Y. M. A conserved function for pericentromeric satellite DNA. Elife 7, 1–19 (2018). (PMID: 10.7554/eLife.34122)
Meister, P., Mango, S. E. & Gasser, S. M. Locking the genome: nuclear organization and cell fate. Curr. Opin. Genet. Dev. 21, 167174 (2011). (PMID: 10.1016/j.gde.2011.01.023)
Bourbousse, C. et al. Light signaling controls nuclear architecture reorganization during seedling establishment. Proc. Natl Acad. Sci. 112, E2836–E2844 (2015). (PMID: 2596433210.1073/pnas.15035121124450433)
She, W. et al. Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development 140, 4008–4019 (2013). (PMID: 2400494710.1242/dev.095034)
Jasencakova, Z. et al. Histone modifications in Arabidopsis—high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J. 33, 471–480 (2003). (PMID: 1258130510.1046/j.1365-313X.2003.01638.x)
Yelagandula, R. et al. The histone variant H2A.W defines heterochromatin and promotes chromatin condensation in arabidopsis. Cell 158, 98–109 (2014). (PMID: 24995981467182910.1016/j.cell.2014.06.006)
Finn, T. E. et al. Transgene expression and transgene-induced silencing in diploid and autotetraploid Arabidopsis. Genetics 187, 409–423 (2011). (PMID: 21078688303048610.1534/genetics.110.124370)
Tsukaya, H. Does ploidy level directly control cell size? Counterevidence from Arabidopsis genetics. PLoS ONE 8, e83729 (2013). (PMID: 24349549386152010.1371/journal.pone.0083729)
Fang, Y. & Spector, D. L. Centromere positioning and dynamics in living arabidopsis plants. Genetics 16, 5710–5718 (2005).
De Storme, N. et al. Glucan synthase-like8 and sterol methyltransferase2 are required for ploidy consistency of the sexual reproduction system in Arabidopsis. Plant Cell 25, 387–403 (2013). (PMID: 23404886360876710.1105/tpc.112.106278)
Edgar, B. A. & Orr-Weaver, T. L. Endoreplication cell cycles: more for less. Cell 105, 297–306 (2001). (PMID: 1134858910.1016/S0092-8674(01)00334-8)
Lermontova, I. et al. Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18, 2443–2451 (2006). (PMID: 17028205162660610.1105/tpc.106.043174)
Lee, H. O., Davidson, J. M. & Duronio, R. J. Endoreplication : polyploidy with purpose. Genes Dev. https://doi.org/10.1101/gad.1829209.results . (2009).
Maison, C. & Almouzni, G. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 5, 296–304 (2004). (PMID: 1507155410.1038/nrm1355)
Kondo, Y. et al. Downregulation of histone H3 lysine 9 methyltransferase G9a induces centrosome disruption and chromosome instability in cancer cells. PLoS ONE 3, e2037 (2008). (PMID: 18446223232357410.1371/journal.pone.0002037)
Carone, D. M. & Lawrence, J. B. Heterochromatin instability in cancer: from the Barr body to satellites and the nuclear periphery. Semin. Cancer Biol. 23, 99–108 (2013). (PMID: 2272206710.1016/j.semcancer.2012.06.008)
Hahn, M. et al. Suv4-20h2 mediates chromatin compaction and is important for cohesin recruitment to heterochromatin. Genes Dev. 27, 859–872 (2013). (PMID: 23599346365022410.1101/gad.210377.112)
Shi, Q. & King, R. W. Chromosome nondisjunction yields tetraploid rather than aneuploid cells in human cell lines. Nature 437, 1038–1042 (2005). (PMID: 1622224810.1038/nature03958)
Yang, F. et al. Trichostatin A and 5-azacytidine both cause an increase in global histone H4 acetylation and a decrease in global DNA and H3K9 methylation during mitosis in maize. BMC Plant Biol. 10, 178 (2010). (PMID: 20718950309530810.1186/1471-2229-10-178)
Tanaka, M., Kikuchi, A. & Kamada, H. The arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol. 146, 149–161 (2008). (PMID: 18024558223055110.1104/pp.107.111674)
Li, H. et al. The histone deacetylase inhibitor trichostatin a promotes totipotency in the male gametophyte. Plant Cell 26, 195–209 (2014). (PMID: 24464291396356810.1105/tpc.113.116491)
Pecinka, A. et al. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22, 3118–3129 (2010). (PMID: 20876829296555510.1105/tpc.110.078493)
Fusco, A. & Fedele, M. Roles of HMGA proteins in cancer. Nat. Rev. Cancer 7, 899–910 (2007). (PMID: 1800439710.1038/nrc2271)
Gaspar-Maia, A., Alajem, A., Meshorer, E. & Ramalho-Santos, M. Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 12, 36–47 (2011). (PMID: 21179060389157210.1038/nrm3036)
Pillot, M. et al. Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Plant Cell 22, 307–320 (2010). (PMID: 20139161284541910.1105/tpc.109.071647)
Breuer, C., Braidwood, L. & Sugimoto, K. Endocycling in the path of plant development. Curr. Opin. Plant Biol. 17C, 78–85 (2014). (PMID: 10.1016/j.pbi.2013.11.007)
Yanagida, M. Basic mechanism of eukaryotic chromosome segregation. Philos. Trans. R. Soc. Lond. B 360, 609–621 (2005). (PMID: 10.1098/rstb.2004.1615)
Winkelmann, T., Sangwan, R. S. & Schwenkel, H.-G. Flow cytometric analyses in embryogenic and non-embryogenic callus lines of Cyclamen persicum Mill.: relation between ploidy level and competence for somatic embryogenesis. Plant Cell Rep. 17, 400–404 (1998). (PMID: 3073657910.1007/s002990050414)
Borchert, T., Fuchs, J., Winkelmann, T. & Hohe, A. Variable DNA content of Cyclamen persicum regenerated via somatic embryogenesis: rethinking the concept of long-term callus and suspension cultures. Plant Cell Tissue Organ Cult. 90, 255–263 (2007). (PMID: 10.1007/s11240-007-9264-x)
Orbović, V. et al. Analysis of genetic variability in various tissue culture-derived lemon plant populations using RAPD and flow cytometry. Euphytica 161, 329–335 (2007). (PMID: 10.1007/s10681-007-9559-3)
Prado, M. J. et al. Detection of somaclonal variants in somatic embryogenesis-regenerated plants of Vitis vinifera by flow cytometry and microsatellite markers. Plant Cell Tissue Organ Cult. 103, 49–59 (2010). (PMID: 10.1007/s11240-010-9753-1)
Weingartner, M. et al. Expression of a nondegradable cyclin B1 affects plant development and leads to endomitosis by inhibiting the formation of a phragmoplast. Plant Cell 16, 643–657 (2004).
Iwata, E. et al. 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 23, 4382–4393 (2011). (PMID: 22167058326987210.1105/tpc.111.092049)
Soriano, M., Li, H. & Boutilier, K. Microspore embryogenesis: establishment of embryo identity and pattern in culture. Plant Reprod. 26, 181–196 (2013). (PMID: 23852380374732110.1007/s00497-013-0226-7)
Breuninger, H., Rikirsch, E., Hermann, M., Ueda, M. & Laux, T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell 14, 867–876 (2008). (PMID: 1853911510.1016/j.devcel.2008.03.008)
R, S. et al. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057–1065 (2005). (PMID: 10.1038/ncb1316)
Masson, J. & Paszkowski, J. The culture response of Arabidopsis thaliana protoplasts is determined by the growth conditions of donor plants. Plant J. 2, 829–833 (1992). (PMID: 10.1111/j.1365-313X.1992.tb00153.x)
Gleave, A. P. A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20, 1203–1207 (1992). (PMID: 146385710.1007/BF00028910)
Becker, D., Kemper, E., Schell, J. & Masterson, R. New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol. Biol. 20, 1195–1197 (1992). (PMID: 146385510.1007/BF00028908)
Karimi, M., Depicker, A. & Hilson, P. Recombinational cloning with plant gateway vectors. Plant Physiol. 145, 1144–1154 (2007). (PMID: 18056864215172810.1104/pp.107.106989)
Immink, R. G. H. et al. Characterization of SOC1’s central role in flowering by the identification of its upstream and downstream regulators. Plant Physiol. 160, 433–449 (2012). (PMID: 22791302344021710.1104/pp.112.202614)
Schwab, R., Ossowski, S., Riester, M., Warthmann, N. & Weigel, D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18, 1121–1133 (2006). (PMID: 16531494145687510.1105/tpc.105.039834)
Passarinho, P. et al. BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Mol. Biol. 68, 225–237 (2008). (PMID: 1866358610.1007/s11103-008-9364-y)
Den Dulk-Ras, A. & Hooykaas, J. P. Electroporation of Agrobacterium tumefaciens. Plant Cell Electroporation Electrofusion Protoc. 55, 63–72 (1995). (PMID: 10.1385/0-89603-328-7:63)
Clough, S. J. & Bent, F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998). (PMID: 1006907910.1046/j.1365-313x.1998.00343.x)
Gamborg, O. L., Miller, R. & Ojima, K. Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50, 151–158 (1968). (PMID: 565085710.1016/0014-4827(68)90403-5)
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408 (2001). (PMID: 1184660910.1006/meth.2001.1262)
Czechowski, T., Stitt, M., Altmann, T. & Udvardi, M. K. Genome-wide identification and testing of superior reference genes for transcript normalization. Plant Physiol. 139, 5–17 (2005). (PMID: 16166256120335310.1104/pp.105.063743)
Anandalakshmi, R. et al. A viral suppressor of gene silencing in plants. Proc. Natl Acad. Sci. 95, 13079–13084 (1998). (PMID: 978904410.1073/pnas.95.22.1307923715)
Baroux, C., Pecinka, A., Fuchs, J., Schubert, I. & Grossniklaus, U. The triploid endosperm genome of Arabidopsis adopts a peculiar, parental-dosage-dependent chromatin organization. Plant Cell 19, 1782–1794 (2007). (PMID: 17557811195573010.1105/tpc.106.046235)
She, W., Grimanelli, D. & Baroux, C. An efficient method for quantitative, single-cell analysis of chromatin modification and nuclear architecture in whole-mount ovules in arabidopsis. J. Vis. Exp. (2014) https://doi.org/10.3791/51530 . (2014).
Substance Nomenclature:: 0 (Arabidopsis Proteins)
0 (BABY BOOM protein, Arabidopsis)
0 (Histone Deacetylase Inhibitors)
0 (Hydroxamic Acids)
0 (Transcription Factors)
3X2S926L3Z (trichostatin A)
Entry Date(s):: Date Created: 20210505 Date Completed: 20210524 Latest Revision: 20230131
Update Code:: 20240104
PubMed Central ID:: PMC8096963
DOI:: 10.1038/s41467-021-22815-8
PMID:: 33947865
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Plant somatic cells can be reprogrammed into totipotent embryonic cells that are able to form differentiated embryos in a process called somatic embryogenesis (SE), by hormone treatment or through overexpression of certain transcription factor genes, such as BABY BOOM (BBM). Here we show that overexpression of the AT-HOOK MOTIF CONTAINING NUCLEAR LOCALIZED 15 (AHL15) gene induces formation of somatic embryos on Arabidopsis thaliana seedlings in the absence of hormone treatment. During zygotic embryogenesis, AHL15 expression starts early in embryo development, and AH15 and other AHL genes are required for proper embryo patterning and development beyond the globular stage. Moreover, AHL15 and several of its homologs are upregulated and required for SE induction upon hormone treatment, and they are required for efficient BBM-induced SE as downstream targets of BBM. A significant number of plants derived from AHL15 overexpression-induced somatic embryos are polyploid. Polyploidisation occurs by endomitosis specifically during the initiation of SE, and is caused by strong heterochromatin decondensation induced by AHL15 overexpression.

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