An Arabidopsis AT-hook motif nuclear protein mediates somatic embryogenesis and coinciding genome duplication.
AT-Hook Motifs
Arabidopsis
/ embryology
Arabidopsis Proteins
/ genetics
Chromatin Assembly and Disassembly
/ genetics
Chromosome Segregation
/ genetics
Gene Duplication
Gene Expression Regulation, Plant
/ drug effects
Heat-Shock Response
/ genetics
Histone Deacetylase Inhibitors
/ pharmacology
Hydroxamic Acids
/ pharmacology
Plant Somatic Embryogenesis Techniques
Polyploidy
Transcription Factors
/ genetics
Up-Regulation
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
04 05 2021
04 05 2021
Historique:
received:
18
12
2019
accepted:
30
03
2021
entrez:
5
5
2021
pubmed:
6
5
2021
medline:
25
5
2021
Statut:
epublish
Résumé
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.
Identifiants
pubmed: 33947865
doi: 10.1038/s41467-021-22815-8
pii: 10.1038/s41467-021-22815-8
pmc: PMC8096963
doi:
Substances chimiques
Arabidopsis Proteins
0
BABY BOOM protein, Arabidopsis
0
Histone Deacetylase Inhibitors
0
Hydroxamic Acids
0
Transcription Factors
0
trichostatin A
3X2S926L3Z
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2508Références
Yarbrough, J. A. Anatomical and developmental studies of the foliar embryos of Bryophyllum calycinum. Am. J. Bot. 19, 443–453 (1932).
doi: 10.1002/j.1537-2197.1932.tb09663.x
Taylor, R. L. The foliar embryos of Malaxis paludosa. Can. J. Bot. 45, 1553–1556 (1967).
doi: 10.1139/b67-159
Ozias-Akins, P. & van Dijk, P. J. Mendelian genetics of apomixis in plants. Annu. Rev. Genet. 41, 509–537 (2007).
pubmed: 18076331
doi: 10.1146/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).
pubmed: 24939990
pmcid: 4063905
doi: 10.1534/genetics.114.163105
Birnbaum, K. D. & Sánchez Alvarado, A. Slicing across kingdoms: regeneration in plants and animals. Cell 132, 697–710 (2008).
pubmed: 18295584
pmcid: 2692308
doi: 10.1016/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).
pubmed: 24622953
doi: 10.1093/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).
doi: 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).
doi: 10.1007/s10725-005-3478-x
Horstman, A., Bemer, M. & Boutilier, K. A transcriptional view on somatic embryogenesis. Regeneration 4, 201–206 (2017).
pubmed: 29299323
pmcid: 5743784
doi: 10.1002/reg2.91
Lotan, T. et al. Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93, 1195–1205 (1998).
pubmed: 9657152
doi: 10.1016/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).
pubmed: 11573014
doi: 10.1073/pnas.201413498
pmcid: 58812
Boutilier, K. et al. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14, 1737–1749 (2002).
pubmed: 12172019
pmcid: 151462
doi: 10.1105/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).
pubmed: 12000682
doi: 10.1046/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).
pubmed: 9742243
pmcid: 147871
doi: 10.1093/nar/26.19.4413
Reeves, R. Nuclear functions of the HMG proteins. Biochim. Biophys. Acta 1799, 3–14 (2010).
pubmed: 19748605
doi: 10.1016/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).
pubmed: 19732855
doi: 10.1016/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).
pubmed: 15604740
doi: 10.1007/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).
pubmed: 24218605
doi: 10.1073/pnas.1219277110
pmcid: 3845178
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).
pubmed: 18088311
doi: 10.1111/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).
pubmed: 19517252
doi: 10.1007/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).
pubmed: 19956801
pmcid: 2774341
doi: 10.1371/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).
pubmed: 23335615
pmcid: 3584533
doi: 10.1105/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).
pubmed: 17277098
pmcid: 1820926
doi: 10.1104/pp.106.093542
Karami, O. et al. A suppressor of axillary meristem maturation promotes longevity in flowering plants. Nat. Plants 6, 368–376 (2020).
pubmed: 32284551
doi: 10.1038/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).
pubmed: 17971039
doi: 10.1111/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).
pubmed: 10706706
doi: 10.4049/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).
pubmed: 30542157
doi: 10.1038/s41586-018-0785-8
Horstman, A. et al. AIL and HDG proteins act antagonistically to control cell proliferation. Development 142, 454–464 (2015).
pubmed: 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).
pubmed: 22797695
doi: 10.1038/nn.3165
Jagannathan, M., Cummings, R. & Yamashita, Y. M. A conserved function for pericentromeric satellite DNA. Elife 7, 1–19 (2018).
doi: 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).
doi: 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).
pubmed: 25964332
doi: 10.1073/pnas.1503512112
pmcid: 4450433
She, W. et al. Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development 140, 4008–4019 (2013).
pubmed: 24004947
doi: 10.1242/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).
pubmed: 12581305
doi: 10.1046/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).
pubmed: 24995981
pmcid: 4671829
doi: 10.1016/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).
pubmed: 21078688
pmcid: 3030486
doi: 10.1534/genetics.110.124370
Tsukaya, H. Does ploidy level directly control cell size? Counterevidence from Arabidopsis genetics. PLoS ONE 8, e83729 (2013).
pubmed: 24349549
pmcid: 3861520
doi: 10.1371/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).
pubmed: 23404886
pmcid: 3608767
doi: 10.1105/tpc.112.106278
Edgar, B. A. & Orr-Weaver, T. L. Endoreplication cell cycles: more for less. Cell 105, 297–306 (2001).
pubmed: 11348589
doi: 10.1016/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).
pubmed: 17028205
pmcid: 1626606
doi: 10.1105/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).
pubmed: 15071554
doi: 10.1038/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).
pubmed: 18446223
pmcid: 2323574
doi: 10.1371/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).
pubmed: 22722067
doi: 10.1016/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).
pubmed: 23599346
pmcid: 3650224
doi: 10.1101/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).
pubmed: 16222248
doi: 10.1038/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).
pubmed: 20718950
pmcid: 3095308
doi: 10.1186/1471-2229-10-178
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).
pubmed: 18024558
pmcid: 2230551
doi: 10.1104/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).
pubmed: 24464291
pmcid: 3963568
doi: 10.1105/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).
pubmed: 20876829
pmcid: 2965555
doi: 10.1105/tpc.110.078493
Fusco, A. & Fedele, M. Roles of HMGA proteins in cancer. Nat. Rev. Cancer 7, 899–910 (2007).
pubmed: 18004397
doi: 10.1038/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).
pubmed: 21179060
pmcid: 3891572
doi: 10.1038/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).
pubmed: 20139161
pmcid: 2845419
doi: 10.1105/tpc.109.071647
Breuer, C., Braidwood, L. & Sugimoto, K. Endocycling in the path of plant development. Curr. Opin. Plant Biol. 17C, 78–85 (2014).
doi: 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).
doi: 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).
pubmed: 30736579
doi: 10.1007/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).
doi: 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).
doi: 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).
doi: 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).
pubmed: 22167058
pmcid: 3269872
doi: 10.1105/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).
pubmed: 23852380
pmcid: 3747321
doi: 10.1007/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).
pubmed: 18539115
doi: 10.1016/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).
doi: 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).
doi: 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).
pubmed: 1463857
doi: 10.1007/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).
pubmed: 1463855
doi: 10.1007/BF00028908
Karimi, M., Depicker, A. & Hilson, P. Recombinational cloning with plant gateway vectors. Plant Physiol. 145, 1144–1154 (2007).
pubmed: 18056864
pmcid: 2151728
doi: 10.1104/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).
pubmed: 22791302
pmcid: 3440217
doi: 10.1104/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).
pubmed: 16531494
pmcid: 1456875
doi: 10.1105/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).
pubmed: 18663586
doi: 10.1007/s11103-008-9364-y
Den Dulk-Ras, A. & Hooykaas, J. P. Electroporation of Agrobacterium tumefaciens. Plant Cell Electroporation Electrofusion Protoc. 55, 63–72 (1995).
doi: 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).
pubmed: 10069079
doi: 10.1046/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).
pubmed: 5650857
doi: 10.1016/0014-4827(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).
pubmed: 11846609
doi: 10.1006/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).
pubmed: 16166256
pmcid: 1203353
doi: 10.1104/pp.105.063743
Anandalakshmi, R. et al. A viral suppressor of gene silencing in plants. Proc. Natl Acad. Sci. 95, 13079–13084 (1998).
pubmed: 9789044
doi: 10.1073/pnas.95.22.13079
pmcid: 23715
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).
pubmed: 17557811
pmcid: 1955730
doi: 10.1105/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).