Proteins play a major role in the three-dimensional organization of nuclear genome and its function. While histones arrange DNA into a nucleosome fiber, other proteins contribute to higher-order chromatin structures in interphase nuclei, and mitotic/meiotic chromosomes. Despite the key role of proteins in maintaining genome integrity and transferring hereditary information to daughter cells and progenies, the knowledge about their function remains fragmentary. This is particularly true for the proteins of condensed chromosomes and, in particular, chromosomes of plants. Here, we purified barley mitotic metaphase chromosomes by a flow cytometric sorting and characterized their proteins. Peptides from tryptic protein digests were fractionated either on a cation exchanger or reversed-phase microgradient system before liquid chromatography coupled to tandem mass spectrometry. Chromosomal proteins comprising almost 900 identifications were classified based on a combination of software prediction, available database localization information, sequence homology, and domain representation. A biological context evaluation indicated the presence of several groups of abundant proteins including histones, topoisomerase 2, POLYMERASE 2, condensin subunits, and many proteins with chromatin-related functions. Proteins involved in processes related to DNA replication, transcription, and repair as well as nucleolar proteins were found. We have experimentally validated the presence of FIBRILLARIN 1, one of the nucleolar proteins, on metaphase chromosomes, suggesting that plant chromosomes are coated with proteins during mitosis, similar to those of human and animals. These results improve significantly the knowledge of plant chromosomal proteins and provide a basis for their functional characterization and comparative phylogenetic analyses.

Department of Molecular Biology Faculty of Science Centre of the Region Haná for Biotechnological and Agricultural Research Palacký University Olomouc Olomouc Czechia

Department of Protein Biochemistry and Proteomics Faculty of Science Centre of the Region Haná for Biotechnological and Agricultural Research Palacký University Olomouc Olomouc Czechia

Institute of Experimental Botany of the Czech Academy of Sciences Centre of the Region Haná for Biotechnological and Agricultural Research Olomouc Czechia

Zobrazit více v PubMed

Altschul S. F., Wootton J. C., Gertz E. M., Agarwala R., Morgulis A., Schäffer A. A., et al. . (2005). Protein database searches using compositionally adjusted substitution matrices. FEBS J. 272, 5101–5109. 10.1111/j.1742-4658.2005.04945.x, PMID: PubMed DOI PMC

Antonin W., Neumann H. (2016). Chromosome condensation and decondensation during mitosis. Curr. Opin. Cell Biol. 40, 15–22. 10.1016/j.ceb.2016.01.013, PMID: PubMed DOI

Baker K., Dhillon T., Colas I., Cook N., Milne I., Milne L., et al. . (2015). Chromatin state analysis of the barley epigenome reveals a higher-order structure defined by H3K27me1 and H3K27me3 abundance. Plant J. 84, 111–124. 10.1111/tpj.12963, PMID: PubMed DOI PMC

Bigeard J., Rayapuram N., Bonhomme L., Hirt H., Pflieger D. (2014). Proteomic and phosphoproteomic analyses of chromatin-associated proteins from Arabidopsis thaliana. Proteomics 14, 2141–2155. 10.1002/pmic.201400072, PMID: PubMed DOI

Blavet N., Uřinovská J., Jeřábková H., Chamrád I., Vrána J., Lenobel R., et al. . (2017). UNcleProt (universal nuclear protein database of barley): The first nuclear protein database that distinguishes proteins from different phases of the cell cycle. Nucleus 8, 70–80. 10.1080/19491034.2016.1255391, PMID: PubMed DOI PMC

Blythe S. A., Wieschaus E. F. (2016). Establishment and maintenance of heritable chromatin structure during early drosophila embryogenesis. eLife 5:e20148. 10.7554/eLife.20148, PMID: PubMed DOI PMC

Booth D. G., Beckett A. J., Molina O., Samejima I., Masumoto H., Kouprina N., et al. . (2016). 3D-CLEM reveals that a major portion of mitotic chromosomes is not chromatin. Mol. Cell 64, 790–802. 10.1016/j.molcel.2016.10.009, PMID: PubMed DOI PMC

Booth D. G., Takagi M., Sanchez-Pulido L., Petfalski E., Vargiu G., Samejima K., et al. . (2014). Ki-67 is a PP1-interacting protein that organises the mitotic chromosome periphery. eLife 3:e01641. 10.7554/eLife.01641, PMID: PubMed DOI PMC

Brameier M., Krings A., MacCallum R. M. (2007). NucPred—predicting nuclear localization of proteins. Bioinformatics 23, 1159–1160. 10.1093/bioinformatics/btm066, PMID: PubMed DOI

Chamrád I., Simerský R., Bérešová L., Strnad M., Šebela M., Lenobel R. (2014). Proteomic identification of a candidate sequence of wheat cytokinin-binding protein 1. J. Plant Growth Regul. 33, 896–902. 10.1007/s00344-014-9419-z DOI

Chamrád I., Uřinovská J., Petrovská B., Jeřábková H., Lenobel R., Vrána J., et al. . (2018). Identification of plant nuclear proteins based on a combination of flow sorting, SDS-PAGE, and LC-MS/MS analysis. Methods Mol. Biol. 1696, 57–79. 10.1007/978-1-4939-7411-5_4, PMID: PubMed DOI

Cheeseman I. M. (2014). The kinetochore. Cold Spring Harb. Perspect. Biol. 6:a015826. 10.1101/cshperspect.a015826, PMID: PubMed DOI PMC

Chi S. M., Nam D. (2012). WegoLoc: accurate prediction of protein subcellular localization using weighted gene ontology terms. Bioinformatics 28, 1028–1030. 10.1093/bioinformatics/bts062, PMID: PubMed DOI

Cuylen S., Blaukopf C., Politi A. Z., Müller-Reichert T., Neumann B., Poser I., et al. . (2016). Ki-67 acts as a biological surfactant to disperse mitotic chromosomes. Nature 535, 308–312. 10.1038/nature18610, PMID: PubMed DOI PMC

Cuylen-Haering S., Petrovic M., Hernandez-Armendariz A., Schneider M. W., Samwer M., Blaukopf C., et al. . (2020). Chromosome clustering by Ki-67 excludes cytoplasm during nuclear assembly. Nature 587, 285–290. 10.1038/s41586-020-2672-3, PMID: PubMed DOI PMC

Djeghloul D., Patel B., Kramer H., Dimond A., Whilding C., Brown K., et al. . (2020). Identifying proteins bound to native mitotic ESC chromosomes reveals chromatin repressors are important for compaction. Nat. Commun. 11, 1–15. 10.1038/s41467-020-17823-z, PMID: PubMed DOI PMC

Doležel J., Binarová P., Lucretti S. (1989). Analysis of nuclear DNA content in plant cells by flow cytometry. Biol. Plant. 31, 113–120. 10.1007/BF02907241 DOI

Doležel J., Kubaláková M., Číhalíková J., Suchánková P., Šimková H. (2011). Chromosome analysis and sorting using flow cytometry. Methods Mol. Biol. 701, 221–238. 10.1007/978-1-61737-957-4_12, PMID: PubMed DOI

Doležel J., Sgorbati S., Lucretti S. (1992). Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiol. Plant. 85, 625–631. 10.1111/j.1399-3054.1992.tb04764.x DOI

Doležel J., Vrána J., Šafář J., Bartoš J., Kubaláková M., Šimková H. (2012). Chromosomes in the flow to simplify genome analysis. Funct. Integr. Genomics 12, 397–416. 10.1007/s10142-012-0293-0, PMID: PubMed DOI PMC

Festuccia N., Dubois A., Vandormael-Pournin S., Tejeda E. G., Mouren A., Bessonnard S. (2016). Mitotic binding of Esrrb marks key regulatory regions of the pluripotency network. Nat. Cell Biol. 18, 1139–1148. 10.1038/ncb3418, PMID: PubMed DOI

Fierz B., Poirer M. G. (2019). Biophysics of chromatin dynamics. Annu. Rev. Biophys. 48, 321–345. 10.1146/annurev-biophys-070317-032847 PubMed DOI

Franc V., Řehulka P., Medda R., Padiglia A., Floris G., Šebela M. (2013a). Analysis of the glycosylation pattern of plant copper amine oxidases by MALDI-TOF/TOF MS coupled to a manual chromatographic separation of glycans and glycopeptides. Electrophoresis 34, 2357–2367. 10.1002/elps.201200622, PMID: PubMed DOI

Franc V., Řehulka P., Raus M., Stulík J., Novak J., Renfrow M. B., et al. . (2013b). Elucidating heterogeneity of IgA1 hinge-region O-glycosylation by use of MALDI-TOF/TOF mass spectrometry: role of cysteine alkylation during sample processing. J. Proteomics 92, 299–312. 10.1016/j.jprot.2013.07.013, PMID: PubMed DOI PMC

Fujimura A., Hayashi Y., Kato K., Kogure Y., Kameyama M., Shimamoto H., et al. . (2020). Identification of a novel nucleolar protein complex required for mitotic chromosome segregation through centromeric accumulation of Aurora B. Nucleic Acids Res. 48, 6583–6596. 10.1093/nar/gkaa449, PMID: PubMed DOI PMC

Ganji M., Shaltiel I. A., Bisht S., Kim E., Kalichava A., Haering C. H., et al. . (2018). Real-time imaging of DNA loop extrusion by condensin. Science 360, 102–105. 10.1126/science.aar7831, PMID: PubMed DOI PMC

Gassmann R., Henzing A. J., Earnshaw W. C. (2005). Novel components of human mitotic chromosomes identified by proteomic analysis of the chromosome scaffold fraction. Chromosoma 113, 385–397. 10.1007/s00412-004-0326-0, PMID: PubMed DOI

Ginno P. A., Burger L., Seebacher J., Iesmantavicius V., Schübeler D. (2018). Cell cycle-resolved chromatin proteomics reveals the extent of mitotic preservation of the genomic regulatory landscape. Nat. Commun. 9, 1–12. 10.1038/s41467-018-06007-5, PMID: PubMed DOI PMC

Hara M., Fukagawa T. (2020). Dynamics of kinetochore structure and its regulations during mitotic progression. Cell. Mol. Life Sci. 77, 1–15. 10.1007/s00018-020-03472-4 PubMed DOI PMC

Hayashi Y., Kato K., Kimura K. (2017). The hierarchical structure of the perichromosomal layer comprises Ki67, ribosomal RNAs, and nucleolar proteins. Biochem. Biophys. Res. Commun. 493, 1043–1049. 10.1016/j.bbrc.2017.09.092, PMID: PubMed DOI

Hsiung C. C. S., Morrissey C. S., Udugama M., Frank C. L., Keller C. A., Baek S., et al. . (2015). Genome accessibility is widely preserved and locally modulated during mitosis. Genome Res. 25, 213–225. 10.1101/gr.180646.114, PMID: PubMed DOI PMC

Huang D. W., Sherman B. T., Lempicki R. A. (2009). Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1–13. 10.1093/nar/gkn923, PMID: PubMed DOI PMC

International Barley Genome Sequencing Consortium, Mayer K. F. X., Waugh R., Brown J. W. S., Schulman A., Langridge P., et al. . (2012). A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711–716. 10.1038/nature11543, PMID: PubMed DOI

Jasenčáková Z., Meister A., Schubert I. (2001). Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley. Chromosoma 110, 83–92. 10.1007/s004120100132, PMID: PubMed DOI

Kalinina N. O., Makarova S., Makhotenko A., Love A. J., Taliansky M. (2018). The multiple functions of the nucleolus in plant development, disease and stress responses. Front. Plant Sci. 9:132. 10.3389/fpls.2018.00132, PMID: PubMed DOI PMC

Kintlová M., Blavet N., Cegan R., Hobza R. (2017). Transcriptome of barley under three different heavy metal stress reaction. Genom. Data 13, 15–17. 10.1016/j.gdata.2017.05.016, PMID: PubMed DOI PMC

Kubaláková M., Macas J., Dolezel J. (1997). Mapping of repeated DNA sequences in plant chromosomes by PRINS and C-PRINS. Theor. Appl. Genet. 94, 758–763. 10.1007/s001220050475 DOI

Laemmli U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685. 10.1038/227680a0, PMID: PubMed DOI

Liu Y., Deng Y., Li G., Zhao J. (2013). Replication factor C1 (RFC1) is required for double-strand break repair during meiotic homologous recombination in Arabidopsis. Plant J. 73, 154–165. 10.1111/tpj.12024, PMID: PubMed DOI

Lysák M. A., Číhalíková J., Kubaláková M., Šimková H., Künzel G., Doležel J. (1999). Flow karyotyping and sorting of mitotic chromosomes of barley (Hordeum vulgare L.). Chromosom. Res. 7, 431–444. 10.1023/A:1009293628638, PMID: PubMed DOI

Marchler-Bauer A., Bryant S. H. (2004). CD-search: protein domain annotations on the fly. Nucleic Acids Res. 32, W327–W331. 10.1093/nar/gkh454, PMID: PubMed DOI PMC

Marthe C., Kumlehn J., Hensel G. (2015). Barley (Hordeum vulgare L.) transformation using immature embryos. Methods Mol. Biol. 1223, 71–83. 10.1007/978-1-4939-1695-5_6 PubMed DOI

Martínez-Balbás M. A., Dey A., Rabindran S. K., Ozato K., Wu C. (1995). Displacement of sequence-specific transcription factors from mitotic chromatin. Cell 83, 29–38. 10.1016/0092-8674(95)90231-7, PMID: PubMed DOI

Mascher M., Gundlach H., Himmelbach A., Beier S., Twardziok S. O., Wicker T., et al. . (2017). A chromosome conformation capture ordered sequence of the barley genome. Nature 544, 427–433. 10.1038/nature22043, PMID: PubMed DOI

Meier I., Griffis A. H., Groves N. R., Wagner A. (2016). Regulation of nuclear shape and size in plants. Curr. Opin. Cell Biol. 40, 114–123. 10.1016/j.ceb.2016.03.005, PMID: PubMed DOI

Mikulski P., Hohenstatt M. L., Farrona S., Smaczniak C., Stahl Y., Kaufmann K., et al. . (2019). The chromatin-associated protein PWO1 interacts with plant nuclear Lamin-like components to regulate nuclear size. Plant Cell 31, 1141–1154. 10.1105/tpc.18.00663, PMID: PubMed DOI PMC

Montaño-Gutierrez L. F., Ohta S., Kustatscher G., Earnshaw W. C., Rappsilber J. (2017). Nano random forests to mine protein complexes and their relationships in quantitative proteomics data. Mol. Biol. Cell 28, 673–680. 10.1091/mbc.E16-06-0370, PMID: PubMed DOI PMC

Moravcová D., Kahle V., Řehulková H., Chmelík J., Řehulka P. (2009). Short monolithic columns for purification and fractionation of peptide samples for matrix-assisted laser desorption/ionization time-of-flight/time-of-flight mass spectrometry analysis in proteomics. J. Chromatogr. A 1216, 3629–3636. 10.1016/j.chroma.2009.01.075, PMID: PubMed DOI

Morrison C., Henzing A. J., Jensen O. N., Osheroff N., Dodson H., Kandels-Lewis S. E., et al. . (2002). Proteomic analysis of human metaphase chromosomes reveals topoisomerase II alpha as an Aurora B substrate. Nucleic Acids Res. 30, 5318–5327. 10.1093/nar/gkf665, PMID: PubMed DOI PMC

Ohta S., Bukowski-Wills J. C., Sanchez-Pulido L., de Lima Alves F., Wood L., Chen Z., et al. . (2010). The protein composition of mitotic chromosomes determined using multiclassifier combinatorial proteomics. Cell 142, 810–821. 10.1016/j.cell.2010.07.047, PMID: PubMed DOI PMC

Ohta S., Kimura M., Takagi S., Toramoto I., Ishihama Y. (2016b). Identification of mitosis-specific phosphorylation in mitotic chromosome-associated proteins. J. Proteome Res. 15, 3331–3341. 10.1021/acs.jproteome.6b00512, PMID: PubMed DOI

Ohta S., Montaño-Gutierrez L. F., de Lima Alves F., Ogawa H., Toramoto I., Sato N., et al. . (2016a). Proteomics analysis with a nano random Forest approach reveals novel functional interactions regulated by SMC complexes on mitotic chromosomes. Mol. Cell. Proteomics 15, 2802–2818. 10.1074/mcp.m116.057885, PMID: PubMed DOI PMC

Ohta S., Taniguchi T., Sato N., Hamada M., Taniguchi H., Rappsilber J. (2019). Quantitative proteomics of the mitotic chromosome scaffold reveals the association of BAZ1B with chromosomal axes. Mol. Cell. Proteomics 18, 169–181. 10.1074/mcp.RA118.000923, PMID: PubMed DOI PMC

Palozola K. C., Donahue G., Liu H., Grant G. R., Becker J. S., Cote A., et al. . (2017). Mitotic transcription and waves of gene reactivation during mitotic exit. Science 358, 119–122. 10.1126/science.aal4671, PMID: PubMed DOI PMC

Parsons G. G., Spencer C. A. (1997). Mitotic repression of RNA polymerase II transcription is accompanied by release of transcription elongation complexes. Mol. Cell. Biol. 17, 5791–5802. 10.1128/MCB.17.10.5791, PMID: PubMed DOI PMC

Perez-Riverol Y., Csordas A., Bai J., Bernal-Llinares M., Hewapathirana S., Kundu D. J., et al. . (2019). The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47, D442–D450. 10.1093/nar/gky1106, PMID: PubMed DOI PMC

Pesenti M. E., Prumbaum D., Auckland P., Smith C. M., Faesen A. C., Petrovic A., et al. . (2018). Reconstitution of a 26-subunit human kinetochore reveals cooperative microtubule binding by CENP-OPQUR and NDC80. Mol. Cell 71, 923–939. 10.1016/j.molcel.2018.07.038, PMID: PubMed DOI PMC

Petrovská B., Jeřábková H., Chamrád I., Vrána J., Lenobel R., Uřinovská J., et al. . (2014). Proteomic analysis of barley cell nuclei purified by flow sorting. Cytogenet. Genome Res. 143, 78–86. 10.1159/000365311, PMID: PubMed DOI

Raccaud M., Suter D. M. (2018). Transcription factor retention on mitotic chromosomes: regulatory mechanisms and impact on cell fate decisions. FEBS Lett. 592, 878–887. 10.1002/1873-3468.12828, PMID: PubMed DOI

Rapazote-Flores P., Bayer M., Milne L., Mayer C. D., Fuller J., Guo W., et al. . (2019). BaRTv1. 0: an improved barley reference transcript dataset to determine accurate changes in the barley transcriptome using RNA-seq. BMC Genomics 20:968. 10.1186/s12864-019-6243-7, PMID: PubMed DOI PMC

Rappsilber J., Mann M., Ishihama Y. (2007). Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using stagetips. Nat. Protoc. 2, 1896–1906. 10.1038/nprot.2007.261, PMID: PubMed DOI

Reichow S. L., Hamma T., Ferré-D'Amaré A. R., Varani G. (2007). The structure and function of small nucleolar ribonucleoproteins. Nucleic Acids Res. 35, 1452–1464. 10.1093/nar/gkl1172, PMID: PubMed DOI PMC

Samejima I., Earnshaw W. C. (2018). Isolation of mitotic chromosomes from vertebrate cells and characterization of their proteome by mass spectrometry. Methods Cell Biol. 144, 329–348. 10.1016/bs.mcb.2018.03.021, PMID: PubMed DOI

Sarnowski T. J., Ríos G., Jásik J., Świeżewski S., Kaczanowski S., Li Y., et al. . (2005). SWI3 subunits of putative SWI/SNF chromatin-remodeling complexes play distinct roles during Arabidopsis development. Plant Cell 17, 2454–2472. 10.1105/tpc.105.031203, PMID: PubMed DOI PMC

Šebela M., Štosová T., Havliš J., Wielsch N., Thomas H., Zdráhal Z., et al. . (2006). Thermostable trypsin conjugates for high-throughput proteomics: synthesis and performance evaluation. Proteomics 6, 2959–2963. 10.1002/pmic.200500576, PMID: PubMed DOI

Shevchenko A., Tomas H., Havliš J., Olsen J. V., Mann M. (2006). In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856–2860. 10.1038/nprot.2006.468, PMID: PubMed DOI

Sirri V., Jourdan N., Hernandez-Verdun D., Roussel P. (2016). Sharing of mitotic pre-ribosomal particles between daughter cells. J. Cell Sci. 129, 1592–1604. 10.1242/jcs.180521, PMID: PubMed DOI

Skibbens R. V. (2019). Condensins and cohesins – one of these things is not like the other! J. Cell Sci. 132:jcs220491. 10.1242/jcs.220491, PMID: PubMed DOI PMC

Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., et al. . (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76–85. 10.1016/0003-2697(85)90442-7, PMID: PubMed DOI

Sperschneider J., Catanzariti A. M., DeBoer K., Petre B., Gardiner D. M., Singh K. B., et al. . (2017). LOCALIZER: subcellular localization prediction of both plant and effector proteins in the plant cell. Sci. Rep. 7:44598. 10.1038/srep44598, PMID: PubMed DOI PMC

Stenström L., Mahdessian D., Gnann C., Cesnik A. J., Ouyang W., Leonetti M. D., et al. . (2020). Mapping the nucleolar proteome reveals a spatiotemporal organization related to intrinsic protein disorder. Mol. Syst. Biol. 16:e9469. 10.15252/msb.20209469, PMID: PubMed DOI PMC

Takagi M., Matsuoka Y., Kurihara T., Yoneda Y. (1999). Chmadrin: a novel Ki-67 antigen-related perichromosomal protein possibly implicated in higher order chromatin structure. J. Cell Sci. 112, 2463–2472. 10.1242/jcs.112.15.2463, PMID: PubMed DOI

Takagi M., Natsume T., Kanemaki M. T., Imamoto N. (2016). Perichromosomal protein Ki67 supports mitotic chromosome architecture. Genes Cells 21, 1113–1124. 10.1111/gtc.12420, PMID: PubMed DOI

Takata H., Uchiyama S., Nakamura N., Nakashima S., Kobayashi S., Sone T., et al. . (2007). A comparative proteome analysis of human metaphase chromosomes isolated from two different cell lines reveals a set of conserved chromosome-associated proteins. Genes Cells 12, 269–284. 10.1111/j.1365-2443.2007.01051.x, PMID: PubMed DOI

Tan F., Li G., Chitteti B. R., Peng Z. (2007). Proteome and phosphoproteome analysis of chromatin associated proteins in rice (Oryza sativa). Proteomics 7, 4511–4527. 10.1002/pmic.200700580, PMID: PubMed DOI

Tiang C. L., He Y., Pawlowski W. P. (2012). Chromosome organization and dynamics during interphase, mitosis, and meiosis in plants. Plant Physiol. 158, 26–34. 10.1104/pp.111.187161, PMID: PubMed DOI PMC

Tuteja N., Tran N. Q., Dang H. Q., Tuteja R. (2011). Plant MCM proteins: role in DNA replication and beyond. Plant Mol. Biol. 77, 537–545. 10.1007/s11103-011-9836-3, PMID: PubMed DOI

Tyanova S., Temu T., Sinitcyn P., Carlson A., Hein M. Y., Geiger T., et al. . (2016). The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740. 10.1038/nmeth.3901, PMID: PubMed DOI

Uchiyama S., Kobayashi S., Takata H., Ishihara T., Hori N., Higashi T., et al. . (2005). Proteome analysis of human metaphase chromosomes. J. Biol. Chem. 280, 16994–17004. 10.1074/jbc.M412774200, PMID: PubMed DOI

Wisniewski J. R., Gaugaz F. Z. (2015). Fast and sensitive total protein and peptide assays for proteomic analysis. Anal. Chem. 87, 4110–4116. 10.1021/ac504689z, PMID: PubMed DOI

Yano A., Kodama Y., Koike A., Shinya T., Kim H. J., Matsumoto M. (2006). Interaction between methyl CpG-binding protein and ran GTPase during cell division in tobacco cultured cells. Ann. Bot. 98, 1179–1187. 10.1093/aob/mcl211, PMID: PubMed DOI PMC

Yu C. S., Cheng C. W., Su W. C., Chang K. C., Huang S. W., Hwang J. K., et al. . (2014). CELLO2GO: a web server for protein subCELlular LOcalization prediction with functional gene ontology annotation. PLoS One 9:e99368. 10.1371/journal.pone.0099368, PMID: PubMed DOI PMC

Zaidi S. S. E. A., Mukhtar M. S., Mansoor S. (2018). Genome editing: targeting susceptibility genes for plant disease resistance. Trends Biotechnol. 36, 898–906. 10.1016/j.tibtech.2018.04.005, PMID: PubMed DOI

Zeng Z., Jiang J. (2016). Isolation and proteomics analysis of barley centromeric chromatin using PICh. J. Proteome Res. 15, 1875–1882. 10.1021/acs.jproteome.6b00063, PMID: PubMed DOI

Zwyrtková J., Šimková H., Doležel J. (2020). Chromosome genomics uncovers plant genome organization and function. Biotechnol. Adv. 46:107659. 10.1016/j.biotechadv.2020.107659, PMID: PubMed DOI

Zybailov B., Mosley A. L., Sardiu M. E., Coleman M. K., Florens L., Washburn M. P. (2006). Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 5, 2339–2347. 10.1021/pr060161n, PMID: PubMed DOI

Advanced environmental scanning electron microscopy reveals natural surface nano-morphology of condensed mitotic chromosomes in their native state

Flow Cytometric Analysis and Sorting of Plant Chromosomes