Hümeyra YILDIZ, Bilge Şevval YILDIRIM, Sevim Döndü KARA ÖZTÜRK, Ahmet L. TEK

Bitki kromozomlarında sentromerlerin önemi, moleküler yapısı ve organizasyonu

Sentromer hücre bölünmesi esnasında mikrotübüller aracılığıyla kromozomların yeni hücrelere eşit dağılımını sağlayan kompleks bir yapıdır. Böylesi bir kompleks yapı, tüm ökaryotlarda olduğu gibi bitki türlerinde de büyük ilgi çekerek farklı çalışma disiplinlerinin temelini oluşturmuştur. Çalışma disiplinlerinden birisi olan bitki sentromer biyolojisi, çeşitli bitki sentromerlerindeki benzerlik ve farklılıkları ortaya koyarak genom biyolojisi, taksonomi, filogeni gibi alanlara temel bilgiler sunmaktadır. Ökaryotlarda kromozomları üzerinde fonksiyonel olarak korunmuş sentromer, yapısal anlamda farklı özellikler gösterebilmektedir. Bu yapısal değişiklikler en yaygın anlamda iki yapısal unsur olan sentromere özgü histon H3 (CENH3) proteini ve sentromerik DNA dizileri bakımından ifade edilmektedir. Sentromer tiplerinin karakteristik yapısal özelliklerinin tanımlanabilmesi için klonlanarak dizilenmesi gerekmektedir. Ancak sentromerik DNA dizilerinde bulunan uzun tekrar DNA elementlerinden dolayı hatalı dizilemeler meydana gelebilmekte ve doğru fiziksel haritalar oluşturulamamaktadır. Bu nedenle bitki sentromer evrimi yeteri kadar çözümlenememiştir. Bitki sentromerini çözümleyebilmek amacıyla sentromer mühendisliği, bitki biyoteknolojisi ve biyoinformatik alanları birbiriyle entegre edilerek yeni analiz yöntemleri geliştirilmiştir. Bu çalışma kapsamında, tarihsel perspektiften yola çıkarak çeşitli model bitkiler ve devamında baklagiller (Fabaceae) özelinde farklı epigenetik özellikteki sentromerik DNA dizileri ve sentromer proteinleri irdelenerek evrensel bitki sentromer yapısının özellikleri ortaya konulacaktır. Ayrıca sentromer mühendisliği aracılığıyla uygulamalı tarım bilimlerinde bitki ıslahına büyük yenilikler katabilecek farklı bilimsel çalışmalar sunulacaktır.

Anahtar Kelimeler:

ardışık tekrarlar, CENH3, epigenetik, kinetokor, kromozom, sentromer mühendisliği

Centromere is a complex structure that ensures equal distribution of chromosomes to new cells via microtubules during cell division. Such a complex structure attracted great attention in plant species as well as in all eukaryotes and formed the basis of various study disciplines. Plant centromere biology, which is one of the study disciplines, provides basic information on genome biology, taxonomy, phylogeny by revealing the similarities and differences in various plant centromeres. In eukaryotes, the centromere, which is functionally conserved on chromosomes, may show various structural features. These structural changes are most commonly expressed in terms of the centromere-specific histone H3 (CENH3) protein and centromeric DNA sequences, which are two structural elements. To define the characteristic structural features of the centromere types, extensive studies must be performed involving cloning and sequencing. However, due to the long repeat DNA elements present in centromeric regions, erroneous sequences may occur and correct physical and genetic maps cannot be created. Therefore, plant centromere evolution has not been sufficiently resolved. To analyze the plant centromeres, new analysis methods have been developed by integrating the fields of centromere engineering, plant biotechnology and bioinformatics. Within the scope of this review, starting from a historical perspective, the centromere DNA sequences and centromere proteins with different epigenetic properties will be examined for various model plants and with special emphasis to legumes (Fabaceae), and the properties of the universal plant centromere structure will be revealed. In addition, different scientific studies will be presented that can add great innovations to plant breeding in applied agricultural sciences through centromere engineering.

Keywords:

tandem repeats, CENH3, epigenetics, kinetochore, chromosome, centromere engineering,

PDF

___

Mellone, B. G. (2009). Structural and temporal regulation of centromeric chromatin. Biochem Cell Biol, 87(1), 255-264. https://doi.org/10.1139/O08-121
Santos, A. P., Gaudin, V., Mozgová, I., Pontvianne, F., Schubert, D., Tek, A. L., Dvořáčková, M., Liu, C., Fransz, P., Rosa, S., & Farrona, S. (2020). Tidying-up the plant nuclear space: Domains, functions, and dynamics. J Exp Bot, 71(17), 5160-5178. https://doi.org/10.1093/jxb/eraa282
Henikoff, S., Ahmad, K., & Malik, H. S. (2001). The Centromere Paradox: Stable Inheritance with Rapidly Evolving DNA. Science, 293(5532), 1098-1102. https://doi.org/10.1126/science.1062939
Talbert, P. B., Masuelli, R., Tyagi, A. P., Comai, L., & Henikoff, S. (2002). Centromeric Localization and Adaptive Evolution of an Arabidopsis Histone H3 Variant. The Plant Cell, 14(5), 1053-1066. https://doi.org/10.1105/tpc.010425
Fukagawa, T., & Earnshaw, W. C. (2014). The Centromere: Chromatin Foundation for the Kinetochore Machinery. Dev Cell, 30(5), 496-508. https://doi.org/10.1016/j.devcel.2014.08.016
Jiang ve Birchler. (2013). Plant Centromere Biology (1. bs). John Wiley & Sons, Ltd. https://doi.org/10.1002/9781118525715
Robertis, D. (1987). Cell and molecular biology. 8th Edition. https://www.osti.gov/biblio/6157496
Bickmore, W. A. (2001). Karyotype Analysis and Chromosome Banding. eLS. https://doi.org/10.1038/npg.els.0001160
Rice, S. (1998). Endless Forms: Species and Speciation. Oxford University Press.
Schubert, I., & Lysak, M. A. (2011). Interpretation of karyotype evolution should consider chromosome structural constraints. Trends in Genetics, 27(6), 207-216. https://doi.org/10.1016/j.tig.2011.03.004
Doyle, S. R., Tracey, A., Laing, R., Holroyd, N., Bartley, D., Bazant, W., Beasley, H., Beech, R., Britton, C., Brooks, K., Chaudhry, U., Maitland, K., Martinelli, A., Noonan, J. D., Paulini, M., Quail, M. A., Redman, E., Rodgers, F. H., Sallé, G., Cotton, J. A. (2020). Extensive genomic and transcriptomic variation defines the chromosome-scale assembly of Haemonchus contortus, a model gastrointestinal worm. BioRxiv, https://doi.org/10.1101/2020.02.18.945246
Fu, S., Gao, Z., Birchler, J., & Han, F. (2012). Dicentric Chromosome Formation and Epigenetics of Centromere Formation in Plants. Journal of Genetics and Genomics, 39(3), 125-130. https://doi.org/10.1016/j.jgg.2012.01.006
Pluta, A. F., Mackay, A. M., Ainsztein, A. M., Goldberg, I. G., & Earnshaw, W. C. (1995). The centromere: Hub of chromosomal activities. Science, 270(5242), 1591-1594. https://doi.org/10.1126/science.270.5242.1591
Ekwall, K. (2007). Epigenetic control of centromere behavior. Annu Rev Genet, 41, 63-81. https://doi.org/10.1146/annurev.genet.41.110306.130127
Clarke, L. (1990). Centromeres of budding and fission yeasts. Trends Genet, 6(5), 150-154. https://doi.org/10.1016/0168-9525(90)90149-z
Stoler, S., Keith, K. C., Curnick, K. E., & Fitzgerald-Hayes, M. (1995). A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev., 9(5), 573-586. https://doi.org/10.1101/gad.9.5.573
McGrew, J., Diehl, B., & Fitzgerald-Hayes, M. (1986). Single base-pair mutations in centromere element III cause aberrant chromosome segregation in Saccharomyces cerevisiae. Mol Cell Biol, 6(2), 530-538. https://doi.org/10.1128/mcb.6.2.530
Wrensch, D. L., Kethley, J. B., & Norton, R. A. (1994). Cytogenetics of Holokinetic Chromosomes and Inverted Meiosis: Keys to the Evolutionary Success of Mites, with Generalizations on Eukaryotes. Springer, 282-343. https://doi.org/10.1007/978-1-4615-2389-5_11
Mandrioli, M., & Manicardi, G. C. (2012). Unlocking holocentric chromosomes: New perspectives from comparative and functional genomics? Curr. Genomics, 13(5), 343-349. https://doi.org/10.2174/138920212801619250
Voullaire, L., Saffery, R., Earle, E., Irvine, D. V., Slater, H., Dale, S., Sart, D. du, Fleming, T., & Choo, K. H. A. (2001). Mosaic inv dup(8p) marker chromosome with stable neocentromere suggests neocentromerization is a post-zygotic event. American Journal of Medical Genetics, 102(1), 86-94. https://doi.org/10.1002/1096-8628(20010722)102:1<86::AID-AJMG1390>3.0.CO;2-T
Nasuda, S., Hudakova, S., Schubert, I., Houben, A., & Endo, T. R. (2005). Stable barley chromosomes without centromeric repeats. Proc. Natl. Acad. Sci. U.S.A., 102(28), 9842-9847. https://doi.org/10.1073/pnas.0504235102
Peacock, W. J., Dennis, E. S., Rhoades, M. M., & Pryor, A. J. (1981). Highly repeated DNA sequence limited to knob heterochromatin in maize. PNAS, 78(7), 4490-4494. https://doi.org/10.1073/pnas.78.7.4490
Thomas, C. A. (1971). The genetic organization of chromosomes. Annu. Rev. Genet., 5, 237-256. https://doi.org/10.1146/annurev.ge.05.120171.001321
Choo, K. H. (1997). Centromere DNA dynamics: Latent centromeres and neocentromere formation. American Journal of Human Genetics, 61(6), 1225-1233. https://doi.org/10.1086/301657
Bennetzen, J. L., & Wang, H. (2014). The Contributions of Transposable Elements to the Structure, Function, and Evolution of Plant Genomes. Annual Review of Plant Biology, 65(1), 505-530. https://doi.org/10.1146/annurev-arplant-050213-035811
Talbert, P. B., & Henikoff, S. (2020). What makes a centromere? Experimental Cell Research, 389(2), 111895. https://doi.org/10.1016/j.yexcr.2020.111895
Ohno. (1972). Ohno “Junk” DNA paper in full, 1972. http://www.junkdna.com/ohno.html
Grewal, S. I. S., & Elgin, S. C. R. (2007). Transcription and RNA interference in the formation of heterochromatin. Nature, 447(7143), 399-406. https://doi.org/10.1038/nature05914
Plohl, M. (2010). Those mysterious sequences of satellite DNAs. Periodicum Biologorum, 112, 403-410.
Harrison, G. E., & Heslop-Harrison, J. S. (1995). Centromeric repetitive DNA sequences in the genus Brassica. Theoret. Appl. Genetics, 90(2), 157-165. https://doi.org/10.1007/BF00222197
Plohl, M., Meštrović, N., & Mravinac, B. (2014). Centromere identity from the DNA point of view. Chromosoma, 123(4), 313-325. https://doi.org/10.1007/s00412-014-0462-0
Iwata, A., Tek, A. L., Richard, M. M. S., Abernathy, B., Fonsêca, A., Schmutz, J., Chen, N. W. G., Thareau, V., Magdelenat, G., Li, Y., Murata, M., Pedrosa‐Harand, A., Geffroy, V., Nagaki, K., & Jackson, S. A. (2013). Identification and characterization of functional centromeres of the common bean. The Plant Journal, 76(1), 47-60. https://doi.org/10.1111/tpj.12269
Kunze, R., Saedler, H., & Lönnig, W.-E. (1997). Plant Transposable Elements. J. A. Callow (Ed.), Advances in Botanical Research (C. 27, ss. 331-470). https://doi.org/10.1016/S0065-2296(08)60284-0
Macas, J., Neumann, P., & Navrátilová, A. (2007). Repetitive DNA in the pea (Pisum sativum L.) genome: Comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics, 8, 427. https://doi.org/10.1186/1471-2164-8-427
Nagaki, K., Neumann, P., Zhang, D., Ouyang, S., Buell, C. R., Cheng, Z., & Jiang, J. (2005). Structure, Divergence, and Distribution of the CRR Centromeric Retrotransposon Family in Rice. Mol Biol Evol, 22(4), 845-855. https://doi.org/10.1093/molbev/msi069
Zhong, C. X., Marshall, J. B., Topp, C., Mroczek, R., Kato, A., Nagaki, K., Birchler, J. A., Jiang, J., & Dawe, R. K. (2002). Centromeric Retroelements and Satellites Interact with Maize Kinetochore Protein CENH3. The Plant Cell, 14(11), 2825-2836. https://doi.org/10.1105/tpc.006106
Lim, K.B., Yang, T.J., Hwang, Y.J., Kim, J. S., Park, J.Y., Kwon, S.J., Kim, J., Choi, B.S., Lim, M.H., Jin, M., Kim, H.I., Jong, H. de, Bancroft, I., Lim, Y., & Park, B.S. (2007). Characterization of the centromere and peri-centromere retrotransposons in Brassica rapa and their distribution in related Brassica species. The Plant Journal, 49(2), 173-183. https://doi.org/10.1111/j.1365-313X.2006.02952.x
Tek, A.L., Kashihara, K., Murata, M., & Nagaki, K. (2010). Functional centromeres in soybean include two distinct tandem repeats and a retrotransposon. Chromosome Res, 18(3), 337-347. https://doi.org/10.1007/s10577-010-9119-x
Nagaki, K., Song, J., Stupar, R. M., Parokonny, A. S., Yuan, Q., Ouyang, S., Liu, J., Hsiao, J., Jones, K. M., Dawe, R. K., Buell, C. R., & Jiang, J. (2003). Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics, 163(2), 759-770.
Schmidt, T., & Heslop-Harrison, J. S. (1998). Genomes, genes and junk: The large-scale organization of plant chromosomes. Trends in Plant Science, 3(5), 195-199. https://doi.org/10.1016/S1360-1385(98)01223-0
Mehrotra, S., & Goyal, V. (2014). Repetitive Sequences in Plant Nuclear DNA: Types, Distribution, Evolution and Function. Genomics, Proteomics & Bioinformatics, 12(4), 164-171. https://doi.org/10.1016/j.gpb.2014.07.003
John, H. A., Birnstiel, M. L., & Jones, K. W. (1969). RNA-DNA hybrids at the cytological level. Nature, 223(5206), 582-587. https://doi.org/10.1038/223582a0
Biscotti, M. A., Olmo, E., & Heslop-Harrison, J. S. (Pat). (2015). Repetitive DNA in eukaryotic genomes. Chromosome Res, 23(3), 415-420. https://doi.org/10.1007/s10577-015-9499-z
Charlesworth, B., Sniegowski, P., & Stephan, W. (1994). The evolutionary dynamics of repetitive DNA in eukaryotes. Nature, 371(6494), 215-220. https://doi.org/10.1038/371215a0
Tek, A. L., & Jiang, J. (2004). The centromeric regions of potato chromosomes contain megabase-sized tandem arrays of telomere-similar sequence. Chromosoma, 113(2), 77-83. https://doi.org/10.1007/s00412-004-0297-1
Tek, A. L., Song, J., Macas, J., & Jiang, J. (2005). Sobo, a Recently Amplified Satellite Repeat of Potato, and Its Implications for the Origin of Tandemly Repeated Sequences. Genetics, 170(3), 1231-1238. https://doi.org/10.1534/genetics.105.041087
Heslop-Harrison, J. S., Brandes, A., & Schwarzacher, T. (2003). Tandemly repeated DNA sequences and centromeric chromosomal regions of Arabidopsis species. Chromosome Res, 11(3), 241-253. https://doi.org/10.1023/A:1022998709969
Zhang, X., Li, X., Marshall, J. B., Zhong, C. X., & Dawe, R. K. (2005). Phosphoserines on Maize Centromeric histone H3 and Histone H3 Demarcate the Centromere and Pericentromere during Chromosome Segregation. The Plant Cell, 17(2), 572-583. https://doi.org/10.1105/tpc.104.028522
Birchler, J. A., & Han, F. (2009). Maize Centromeres: Structure, Function, Epigenetics. Annu. Rev. Genet, 43(1), 287-303. https://doi.org/10.1146/annurev-genet-102108-134834
Tek, A. L., Kashihara, K., Murata, M., & Nagaki, K. (2011). Functional centromeres in Astragalus sinicus include a compact centromere-specific histone H3 and a 20-bp tandem repeat. Chromosome Res, 19(8), 969-978. https://doi.org/10.1007/s10577-011-9247-y
Lee, H. R., Zhang, W., Langdon, T., Jin, W., Yan, H., Cheng, Z., & Jiang, J. (2005). Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species. Proc. Natl. Acad. Sci. U.S.A., 102(33), 11793-11798. https://doi.org/10.1073/pnas.0503863102
Cheng, Z., Dong, F., Langdon, T., Ouyang, S., Buell, C. R., Gu, M., Blattner, F. R., & Jiang, J. (2002). Functional Rice Centromeres Are Marked by a Satellite Repeat and a Centromere-Specific Retrotransposon. The Plant Cell, 14(8), 1691-1704. https://doi.org/10.1105/tpc.003079
Gill, N., Findley, S., Walling, J. G., Hans, C., Ma, J., Doyle, J., Stacey, G., & Jackson, S. A. (2009). Molecular and Chromosomal Evidence for Allopolyploidy in Soybean. Plant Physiology, 151(3), 1167-1174. https://doi.org/10.1104/pp.109.137935
Liu, Q., Chang, S., Hartman, G. L., & Domier, L. L. (2018). Assembly and annotation of a draft genome sequence for Glycine latifolia, a perennial wild relative of soybean. Plant J, 95(1), 71-85. https://doi.org/10.1111/tpj.13931
Mehrotra, S., Goel, S., Sharma, S., Raina, S. N., & Rajpal, V. R. (2013). Sequence analysis of KpnI repeat sequences to revisit the phylogeny of the Genus Carthamus L. Appl. Biochem. Biotechnol, 169(4), 1109-1125. https://doi.org/10.1007/s12010-012-0063-4
Silva, D. M. Z. A., Pansonato-Alves, J. C., Utsunomia, R., Daniel, S. N., Hashimoto, D. T., Oliveira, C., Porto-Foresti, F., & Foresti, F. (2013). Chromosomal organization of repetitive DNA sequences in Astyanax bockmanni (Teleostei, Characiformes): Dispersive location, association and co-localization in the genome. Genetica, 141(7-9), 329-336. https://doi.org/10.1007/s10709-013-9732-7
Keçeli, B. N., Jin, C., Van Damme, D., & Geelen, D. (2020). Conservation of centromeric histone 3 interaction partners in plants. J Exp Bot, 71(17), 5237-5246. https://doi.org/10.1093/jxb/eraa214
Macas, J., Požárková, D., Navrátilová, A., Nouzová, M., & Neumann, P. (2000). Two new families of tandem repeats isolated from genus Vicia using genomic self-priming PCR. Mol Gen Genet, 263(5), 741-751. https://doi.org/10.1007/s004380000245
Nagaki, K., Talbert, P. B., Zhong, C. X., Dawe, R. K., Henikoff, S., & Jiang, J. (2003). Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics, 163(3), 1221-1225.
Novák, P., Neumann, P., Pech, J., Steinhaisl, J., & Macas, J. (2013). RepeatExplorer: A Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics , 29(6), 792-793. https://doi.org/10.1093/bioinformatics/btt054
Earnshaw, W. C., & Rothfield, N. (1985). Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma, 91(3), 313-321. https://doi.org/10.1007/BF00328227
Palmer, D. K., O’Day, K., Wener, M. H., Andrews, B. S., & Margolis, R. L. (1987). A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J Cell Biol, 104(4), 805-815. https://doi.org/10.1083/jcb.104.4.805
Yu, H. G., Dawe, R. K., Hiatt, E. N., & Dawe, R. K. (2000). The plant kinetochore. Trends in Plant Science, 5(12), 543-547. https://doi.org/10.1016/S1360-1385(00)01789-1
Jiang, J., Birchler, J. A., Parrott, W. A., & Kelly Dawe, R. (2003). A molecular view of plant centromeres. Trends in Plant Science, 8(12), 570-575. https://doi.org/10.1016/j.tplants.2003.10.011
Warburton, P. E., Cooke, C. A., Bourassa, S., Vafa, O., Sullivan, B. A., Stetten, G., Gimelli, G., Warburton, D., Tyler-Smith, C., Sullivan, K. F., Poirier, G. G., & Earnshaw, W. C. (1997). Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Current Biology, 7(11), 901-904. https://doi.org/10.1016/s0960-9822(06)00382-4
Nagaki, K., Cheng, Z., Ouyang, S., Talbert, P. B., Kim, M., Jones, K. M., Henikoff, S., Buell, C. R., & Jiang, J. (2004). Sequencing of a rice centromere uncovers active genes. Nat. Genet., 36(2), 138-145. https://doi.org/10.1038/ng1289
Tek, A. L., Kashihara, K., Murata, M., & Nagaki, K. (2014). Identification of the centromere-specific histone H3 variant in Lotus japonicus. Gene, 538(1), 8-11. https://doi.org/10.1016/j.gene.2014.01.034
Tek, A. L., & Kara S. D. Ö. (2020). High allelic diversity of the centromere-specific histone H3 (CENH3) in the legume sainfoin (Onobrychis viciifolia). Mol Biol Rep. https://doi.org/10.1007/s11033-020-05926-1
Sullivan, K. F., Hechenberger, M., & Masri, K. (1994). Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol, 127(3), 581-592. https://doi.org/10.1083/jcb.127.3.581
Maheshwari, S., Tan, E. H., West, A., Franklin, F. C. H., Comai, L., & Chan, S. W. L. (2015). Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLoS Genetics, 11(1), e1004970. https://doi.org/10.1371/journal.pgen.1004970
Dawe, R. K., Reed, L. M., Yu, H. G., Muszynski, M. G., & Hiatt, E. N. (1999). A maize homolog of mammalian CENPC is a constitutive component of the inner kinetochore. Plant Cell, 11(7), 1227-1238. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC144275/
Ogura, Y., Shibata, F., Sato, H., & Murata, M. (2004). Characterization of a CENP-C homolog in Arabidopsis thaliana. Genes & Genetic Systems, 79(3), 139-144. https://doi.org/10.1266/ggs.79.139
Ravi, M., & Chan, S. W. L. (2010). Haploid plants produced by centromere-mediated genome elimination. Nature, 464(7288), 615-618. https://doi.org/10.1038/nature08842
Douglas, R. N., & Birchler, J. A. (2013). Plant Centromere Epigenetics. Plant Centromere Biology (ss. 147-158). John Wiley & Sons, Ltd. https://doi.org/10.1002/9781118525715.ch11
Gent, J. I., Dong, Y., Jiang, J., & Dawe, R. K. (2012). Strong epigenetic similarity between maize centromeric and pericentromeric regions at the level of small RNAs, DNA methylation and H3 chromatin modifications. Nucleic Acids Research, 40(4), 1550-1560. https://doi.org/10.1093/nar/gkr862
Strahl, B. D., & Allis, C. D. (2000). The language of covalent histone modifications. Nature, 403(6765), 41-45. https://doi.org/10.1038/47412
Demidov, D., Heckmann, S., Weiss, O., Rutten, T., Dvořák Tomaštíková, E., Kuhlmann, M., Scholl, P., Municio, C. M., Lermontova, I., & Houben, A. (2019). Deregulated Phosphorylation of CENH3 at Ser65 Affects the Development of Floral Meristems in Arabidopsis thaliana. Front Plant Sci, 10. https://doi.org/10.3389/fpls.2019.00928
Zhang, W., Lee, H.-R., Koo, D.-H., & Jiang, J. (2008). Epigenetic Modification of Centromeric Chromatin: Hypomethylation of DNA Sequences in the CENH3-Associated Chromatin in Arabidopsis thaliana and Maize. Plant Cell, 20(1), 25-34. https://doi.org/10.1105/tpc.107.057083
Yan, H., Kikuchi, S., Neumann, P., Zhang, W., Wu, Y., Chen, F., & Jiang, J. (2010). Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant Journal, 63(3), 353-365. https://doi.org/10.1111/j.1365-313X.2010.04246.x
Wu, Y., Kikuchi, S., Yan, H., Zhang, W., Rosenbaum, H., Iniguez, A. L., & Jiang, J. (2011). Euchromatic Subdomains in Rice Centromeres Are Associated with Genes and Transcription. Plant Cell, 23(11), 4054-4064. https://doi.org/10.1105/tpc.111.090043
McClintock, B. (1956). Controlling Elements and the Gene. Cold Spring Harbor Symposia on Quantitative Biology, 21, 197-216. https://doi.org/10.1101/SQB.1956.021.01.017
Talbert, P. B., & Henikoff, S. (2018). Transcribing Centromeres: Noncoding RNAs and Kinetochore Assembly. Trends in Genet, 34(8), 587-599. https://doi.org/10.1016/j.tig.2018.05.001
Topp, C. N., Zhong, C. X., & Dawe, R. K. (2004). Centromere-encoded RNAs are integral components of the maize kinetochore. PNAS, 101(45), 15986-15991. https://doi.org/10.1073/pnas.0407154101
May, B. P., Lippman, Z. B., Fang, Y., Spector, D. L., & Martienssen, R. A. (2005). Differential Regulation of Strand-Specific Transcripts from Arabidopsis Centromeric Satellite Repeats. PLoS Genetics, 1(6). https://doi.org/10.1371/journal.pgen.0010079
Yan, H., Ito, H., Nobuta, K., Ouyang, S., Jin, W., Tian, S., Lu, C., Venu, R. C., Wang, G., Green, P. J., Wing, R. A., Buell, C. R., Meyers, B. C., & Jiang, J. (2006). Genomic and Genetic Characterization of Rice Cen3 Reveals Extensive Transcription and Evolutionary Implications of a Complex Centromere. Plant Cell, 18(9), 2123-2133. https://doi.org/10.1105/tpc.106.043794
Han, F., Gao, Z., & Birchler, J. A. (2009). Reactivation of an Inactive Centromere Reveals Epigenetic and Structural Components for Centromere Specification in Maize. Plant Cell, 21(7), 1929-1939. https://doi.org/10.1105/tpc.109.066662
Dunwell, J. M. (2010). Haploids in flowering plants: Origins and exploitation. Plant Biotechnology Journal, 8(4), 377-424. https://doi.org/10.1111/j.1467-7652.2009.00498.x
Dwivedi, S. L., Britt, A. B., Tripathi, L., Sharma, S., Upadhyaya, H. D., & Ortiz, R. (2015). Haploids: Constraints and opportunities in plant breeding. Biotechnology Advances, 33(6, Part 1), 812-829. https://doi.org/10.1016/j.biotechadv.2015.07.001
Ishii, T., Karimi-Ashtiyani, R., & Houben, A. (2016). Haploidization via Chromosome Elimination: Means and Mechanisms. Annual Review of Plant Biology, 67(1), 421-438. https://doi.org/10.1146/annurev-arplant-043014-114714
Ravi, M., & Chan, S. W.-L. (2013). Centromere-Mediated Generation of Haploid Plants. Plant Centromere Biology (ss. 169-181). John Wiley & Sons, Ltd. https://doi.org/10.1002/9781118525715.ch13
Kuppu, S., Ron, M., Marimuthu, M. P. A., Li, G., Huddleson, A., Siddeek, M. H., Terry, J., Buchner, R., Shabek, N., Comai, L., & Britt, A. B. (2020). A variety of changes, including CRISPR/Cas9‐mediated deletions, in CENH3 lead to haploid induction on outcrossing. Plant Biotechnol J, pbi.13365. https://doi.org/10.1111/pbi.13365
Kalinowska, K., Chamas, S., Unkel, K., Demidov, D., Lermontova, I., Dresselhaus, T., Kumlehn, J., Dunemann, F., & Houben, A. (2019). State-of-the-art and novel developments of in vivo haploid technologies. Theor Appl Genet, 132(3), 593-605. https://doi.org/10.1007/s00122-018-3261-9
Tek, A. L., Stupar, R. M., & Nagaki, K. (2015). Modification of centromere structure: A promising approach for haploid line production in plant breeding. Turk J Agric For, 39(4), 557-562. http://journals.tubitak.gov.tr/agriculture/abstract.htm?id=16664
Kelliher, T., Starr, D., Wang, W., McCuiston, J., Zhong, H., Nuccio, M. L., & Martin, B. (2016). Maternal Haploids Are Preferentially Induced by CENH3-tailswap Transgenic Complementation in Maize. Front. Plant Sci., 7. https://doi.org/10.3389/fpls.2016.00414
De Storme, N., Keçeli, B. N., Zamariola, L., Angenon, G., & Geelen, D. (2016). CENH3-GFP: A visual marker for gametophytic and somatic ploidy determination in Arabidopsis thaliana. BMC Plant Biol, 16, 1. https://doi.org/10.1186/s12870-015-0700-5
Cuacos, M., H Franklin, F. C., & Heckmann, S. (2015). Atypical centromeres in plants-what they can tell us. Front Plant Sci, 6, 913. https://doi.org/10.3389/fpls.2015.00913
Martinez-Zapater, J. M., Estelle, M. A., & Somerville, C. R. (1986). A highly repeated DNA sequence in Arabidopsis thaliana. Molec Gen Genet, 204(3), 417-423. https://doi.org/10.1007/BF00331018
Murata, M., Ogura, Y., & Motoyoshi, F. (1994). Centromeric repetitive sequences in Arabidopsis thaliana. Jpn J Genet, 69(4), 361-370. https://doi.org/10.1266/jjg.69.361
Koukalová, B., Komarnitsky, I. K., & Kuhrová, V. (1993). The distribution of tobacco HRS60 DNA repeated sequences in species of the genus Nicotiana. Plant Science, 88(1), 39-44. https://doi.org/10.1016/0168-9452(93)90107-B
Ohmido, N., Ishimaru, A., Kato, S., Sato, S., Tabata, S., & Fukui, K. (2010). Integration of cytogenetic and genetic linkage maps of Lotus japonicus, a model plant for legumes. Chromosome Res, 18(2), 287-299. https://doi.org/10.1007/s10577-009-9103-5
Kulikova, O., Geurts, R., Lamine, M., Kim, D. J., Cook, D. R., Leunissen, J., de Jong, H., Roe, B. A., & Bisseling, T. (2004). Satellite repeats in the functional centromere and pericentromeric heterochromatin of Medicago truncatula. Chromosoma, 113(6), 276-283. https://doi.org/10.1007/s00412-004-0315-3
Neumann, P., Nouzová, M., & Macas, J. (2001). Molecular and cytogenetic analysis of repetitive DNA in pea (Pisum sativum L.). Genome, 44(4), 716-728.
Neumann, P., Navrátilová, A., Schroeder-Reiter, E., Koblížková, A., Steinbauerová, V., Chocholová, E., Novák, P., Wanner, G., & Macas, J. (2012). Stretching the rules: Monocentric chromosomes with multiple centromere domains. PLoS Genetics, 8(6), e1002777. https://doi.org/10.1371/journal.pgen.1002777
Galasso, I., Pignone, D. R., Harrison, G. E., Heslop Harrison, J. S (1999). Location of two repeated DNA sequences of Vigna unguiculata (L.) Walp. On chromosomes and extended DNA fibres by FISH. Journal of Genetics & Breeding (Italy).
Iwata-Otsubo, A., Radke, B., Findley, S., Abernathy, B., Vallejos, C. E., & Jackson, S. A. (2016). Fluorescence In Situ Hybridization (FISH)-Based Karyotyping Reveals Rapid Evolution of Centromeric and Subtelomeric Repeats in Common Bean (Phaseolus vulgaris) and Relatives. G3 (Bethesda), 6(4), 1013-1022. https://doi.org/10.1534/g3.115.024984
Ishii, T., Juranić, M., Maheshwari, S., Bustamante, F. de O., Vogt, M. M., Salinas-Gamboa, R., Dreissig, S., Gursanscky, N., How, T., Fuchs, J., Schubert, V., Spriggs, A., Vielle-Calzada, J. P., Comai, L., Koltunow, A. M. G., & Houben, A. (2020). Unequal contribution of two paralogous centromeric histones to function the cowpea centromere. BioRxiv, 2020.01.07.897074. https://doi.org/10.1101/2020.01.07.897074
Vahedian, M., Shi, L., Zhu, T., Okimoto, R., Danna, K., & Keim, P. (1995). Genomic organization and evolution of the soybean SB92 satellite sequence. Plant Molecular Biology, 29(4), 857-862. https://doi.org/10.1007/BF00041174
Morgante, M., Jurman, I., Shi, L., Zhu, T., Keim, P., & Rafalski, J. A. (1997). The STR120 satellite DNA of soybean: Organization, evolution and chromosomal specificity. Chromosome Res, 5(6), 363-373. https://doi.org/10.1023/A:1018492208247
Lin, J.-Y., Jacobus, B. H., SanMiguel, P., Walling, J. G., Yuan, Y., Shoemaker, R. C., Young, N. D., & Jackson, S. A. (2005). Pericentromeric regions of soybean (Glycine max L. Merr.) chromosomes consist of retroelements and tandemly repeated DNA and are structurally and evolutionarily labile. Genetics, 170(3), 1221-1230. https://doi.org/10.1534/genetics.105.041616
Heckmann, S., Macas, J., Kumke, K., Fuchs, J., Schubert, V., Ma, L., Novák, P., Neumann, P., Taudien, S., Platzer, M., & Houben, A. (2013). The holocentric species Luzula elegans shows interplay between centromere and large-scale genome organization. Plant J, 73(4), 555-565. https://doi.org/10.1111/tpj.12054
Neumann, P., Schubert, V., Fuková, I., Manning, J. E., Houben, A., & Macas, J. (2016). Epigenetic Histone Marks of Extended Meta-Polycentric Centromeres of Lathyrus and Pisum Chromosomes. Front Plant Sci, 7, 234. https://doi.org/10.3389/fpls.2016.00234