Highly divergent satellitomes of two barley species of agronomic importance, Hordeum chilense and H. vulgare.
Hordeum chilense
Hordeum evolution
Hordeum vulgare
Centromeres
Cereal evolution
Chromosome recognition
Fluorescence in situ hybridization (FISH)
Genome evolution
Homologous pairing
Satellite DNA
Satellitome
Subtelomeres
TEs
Journal
Plant molecular biology
ISSN: 1573-5028
Titre abrégé: Plant Mol Biol
Pays: Netherlands
ID NLM: 9106343
Informations de publication
Date de publication:
02 Oct 2024
02 Oct 2024
Historique:
received:
17
05
2024
accepted:
02
09
2024
medline:
2
10
2024
pubmed:
2
10
2024
entrez:
2
10
2024
Statut:
epublish
Résumé
In this paper, we have performed an in-depth study of the complete set of the satellite DNA (satDNA) families (i.e. the satellitomes) in the genome of two barley species of agronomic value in a breeding framework, H. chilense (H1 and H7 accessions) and H. vulgare (H106 accession), which can be useful tools for studying chromosome associations during meiosis. The study has led to the analysis of a total of 18 satDNA families in H. vulgare, 25 satDNA families in H. chilense (accession H1) and 27 satDNA families in H. chilense (accession H7) that constitute 46 different satDNA families forming 36 homology groups. Our study highlights different important contributions of evolutionary and applied interests. Thus, both barley species show very divergent satDNA profiles, which could be partly explained by the differential effects of domestication versus wildlife. Divergence derives from the differential amplification of different common ancestral satellites and the emergence of new satellites in H. chilense, usually from pre-existing ones but also random sequences. There are also differences between the two H. chilense accessions, which support genetically distinct groups. The fluorescence in situ hybridization (FISH) patterns of some satDNAs yield distinctive genetic markers for the identification of specific H. chilense or H. vulgare chromosomes. Some of the satellites have peculiar structures or are related to transposable elements which provide information about their origin and expansion. Among these, we discuss the existence of different (peri)centromeric satellites that supply this region with some plasticity important for centromere evolution. These peri(centromeric) satDNAs and the set of subtelomeric satDNAs (a total of 38 different families) are analyzed in the framework of breeding as the high diversity found in the subtelomeric regions might support their putative implication in chromosome recognition and pairing during meiosis, a key point in the production of addition/substitution lines and hybrids.
Identifiants
pubmed: 39356367
doi: 10.1007/s11103-024-01501-5
pii: 10.1007/s11103-024-01501-5
doi:
Substances chimiques
DNA, Satellite
0
DNA, Plant
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
108Subventions
Organisme : Ministerio de Ciencia e Innovación
ID : PID2019-103996RB-I00
Organisme : Consejería de Transformación Económica, Industria, Conocimiento y Universidades
ID : QUAL21_023 IAS
Informations de copyright
© 2024. The Author(s).
Références
Aguilar M, Prieto P (2020) Sequence analysis of wheat subtelomeres reveals a high polymorphism among homoeologous chromosomes. Plant Genome. https://doi.org/10.1002/tpg2.20065
doi: 10.1002/tpg2.20065
pubmed: 33029942
Aguilar M, Prieto P (2021) Telomeres and subtelomeres dynamics in the context of early chromosome interactions during meiosis and their implications in plant breeding. Front Plant Sci. https://doi.org/10.3389/fpls.2021.672489
doi: 10.3389/fpls.2021.672489
pubmed: 34149773
pmcid: 8212018
Almeida C, Fonsêca A, dos Santos KGB, Mosiolek M, Pedrosa-Harand A (2012) Contrasting evolution of a satellite DNA and its ancestral IGS rDNA in Phaseolus (Fabaceae). Genome 55:683–689. https://doi.org/10.1139/g2012-059
doi: 10.1139/g2012-059
pubmed: 23050694
Baden C, von Bothmer R (1994) A taxonomìc revision of Hordeum sect. Critesion. Nord J Bot 14:117–136. https://doi.org/10.1111/j.1756-1051.1994.tb00579.x
doi: 10.1111/j.1756-1051.1994.tb00579.x
Bedbrook JR, Jones J, O’Dell M, Thompson RD, Flavell RB (1980) A molecular description of telomeric heterochromatin in secale species. Cell 19:545–560. https://doi.org/10.1016/0092-8674(80)90529-2
doi: 10.1016/0092-8674(80)90529-2
pubmed: 6244112
Belostotsky DA, Ananiev EV (1990) Characterization of relic DNA from barley genome. Theor Appl Genet 80:374–380. https://doi.org/10.1007/BF00210075
doi: 10.1007/BF00210075
pubmed: 24220972
Bennett MD, Smith JB (1976) Nuclear DNA amounts in angiosperms. Philos Trans R Soc Lond Ser B 274:227–274. https://doi.org/10.1098/rstb.1976.0044
doi: 10.1098/rstb.1976.0044
Bilinski P, Distor K, Gutierrez-Lopez J, Mendoza GM, Shi J, Dawe RK, Ross-Ibarra J (2015) Diversity and evolution of centromere repeats in the maize genome. Chromosoma 124:57–65. https://doi.org/10.1007/s00412-014-0483-8
doi: 10.1007/s00412-014-0483-8
pubmed: 25190528
Blattner FR (2009) Progress in phylogenetic analysis and a new infrageneric classification of the barley genus Hordeum (Poaceae: Triticeae). Breed Sci 59:471–480. https://doi.org/10.1270/jsbbs.59.471
doi: 10.1270/jsbbs.59.471
Blattner FR (2018) Taxonomy of the genus Hordeum and Barley (Hordeum vulgare) BT—the Barley genome. In: Muehlbauer GJ (ed) Stein N. Springer International Publishing, Cham, pp 11–23
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
doi: 10.1093/bioinformatics/btu170
pubmed: 24695404
pmcid: 4103590
Bothmer R, Jacobsen N, Baden C, Jørgensen R, Linde-Laursen I (1995) An ecogeographical study of the genus Hordeum. 2nd edition. In: Systematic and ecogeographical studies on crop genepool. International Plant Genetic Resources Institute, Rome
Brown TA, Jones MK, Powell W, Allaby RG (2009) The complex origins of domesticated crops in the Fertile Crescent. Trends Ecol Evol 24:103–109. https://doi.org/10.1016/j.tree.2008.09.008
doi: 10.1016/j.tree.2008.09.008
pubmed: 19100651
Cabrera A, Martín A, Barro F (2002) In-situ comparative mapping (ISCM) of Glu-1 loci in Triticum and Hordeum. Chromosom Res 10:49–54. https://doi.org/10.1023/A:1014270227360
doi: 10.1023/A:1014270227360
Calderón MC, Ramírez MC, Martín A, Prieto P (2012) Development of Hordeum chilense 4Hch introgression lines in durum wheat: a tool for breeders and complex trait analysis. Plant Breed 131:733–738. https://doi.org/10.1111/j.1439-0523.2012.02010.x
doi: 10.1111/j.1439-0523.2012.02010.x
Calderón MDC, Rey MD, Cabrera A, Prieto P (2014) The subtelomeric region is important for chromosome recognition and pairing during meiosis. Sci Rep 4:1–6. https://doi.org/10.1038/srep06488
doi: 10.1038/srep06488
Calderón MC, Rey MD, Martín A, Prieto P (2018) Homoeologous chromosomes from two hordeum species can recognize and associate during meiosis in wheat in the presence of the Ph1 locus. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00585
doi: 10.3389/fpls.2018.00585
pubmed: 29765389
pmcid: 5938817
Carmona A, Friero E, de Bustos A, Jouve N, Cuadrado A (2013) Cytogenetic diversity of SSR motifs within and between Hordeum species carrying the H genome: H. vulgare L. and H. bulbosum L. Theor Appl Genet 126:949–961. https://doi.org/10.1007/s00122-012-2028-y
doi: 10.1007/s00122-012-2028-y
pubmed: 23242107
Cuadrado A, Jouve N (2007) Similarities in the chromosomal distribution of AG and AC repeats within and between Drosophila, human and barley chromosomes. Cytogenet Genome Res 119:91–99. https://doi.org/10.1159/000109624
doi: 10.1159/000109624
pubmed: 18160787
Dennis ES, Gerlach WL, Peacock WJ (1980) Identical polypyrimidine-polypurine satellite DNAs in wheat and barley. Heredity (Edinb) 44:349–366. https://doi.org/10.1038/hdy.1980.33
doi: 10.1038/hdy.1980.33
Doležel J, Čížková J, Šimková H, Bartoš J (2018) One major challenge of sequencing large plant genomes is to know how big they really are. Int J Mol Sci 19:3554
doi: 10.3390/ijms19113554
pubmed: 30423889
pmcid: 6274785
Forster BP, Phillips MS, Miller TE, Baird E, Powell W (1990) Chromosome location of genes controlling tolerance to salt (NaCl) and vigour in Hordeum vulgare and H. chilense. Heredity (Edinb) 65:99–107. https://doi.org/10.1038/hdy.1990.75
doi: 10.1038/hdy.1990.75
Fry K, Salser W (1977) Nucleotide sequences of HS-α satellite DNA from kangaroo rat dipodomys ordii and characterization of similar sequences in other rodents. Cell 12:1069–1084. https://doi.org/10.1016/0092-8674(77)90170-2
doi: 10.1016/0092-8674(77)90170-2
pubmed: 597857
Gálvez-Galván A, Garrido-Ramos MA, Prieto P (2024) Bread wheat satellitome: a complex scenario in a huge genome. Plant Mol Biol 114:8. https://doi.org/10.1007/s11103-023-01404-x
doi: 10.1007/s11103-023-01404-x
pubmed: 38291213
pmcid: 10827815
Garrido-Ramos MA (2015) Satellite DNA in plants: more than just rubbish. Cytogenet Genome Res 146:153–170. https://doi.org/10.1159/000437008
doi: 10.1159/000437008
pubmed: 26202574
Garrido-Ramos MA (2017) Satellite DNA: an evolving topic. Genes (Basel). https://doi.org/10.3390/genes8090230
doi: 10.3390/genes8090230
pubmed: 29039766
Garrido-Ramos MA (2021) The genomics of plant satellite DNA. Prog Mol Subcell Biol 60:103–143
doi: 10.1007/978-3-030-74889-0_5
pubmed: 34386874
Gong Z, Wu Y, Koblížková A, Torres GA, Wang K, Iovene M, Neumann P, Zhang W, Novák P, Robin Buell C, Macas J, Jianga J (2012) Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24:3559–3574. https://doi.org/10.1105/tpc.112.100511
doi: 10.1105/tpc.112.100511
pubmed: 22968715
pmcid: 3480287
Guerra AP, Calvo E, Wasserman M, Chaparro-Olaya J (2016) Producción de proteínas recombinantes de Plasmodium falciparum en Escherichia coli. Biomedica 36:97–108
pubmed: 27622630
Hernández P, Dorado G, Prieto P, Giménez MJ, Ramírez MC, Laurie DA, Snape JW, Martín A (2001) A core genetic map of Hordeum chilense and comparisons with maps of barley (Hordeum vulgare) and wheat (Triticum aestivum). Theor Appl Genet 102:1259–1264. https://doi.org/10.1007/s001220000514
doi: 10.1007/s001220000514
Houben A, Schroeder-Reiter E, Nagaki K, Nasuda S, Wanner G, Murata M, Endo TR (2007) CENH3 interacts with the centromeric retrotransposon cereba and GC-rich satellites and locates to centromeric substructures in barley. Chromosoma 116:275–283. https://doi.org/10.1007/s00412-007-0102-z
doi: 10.1007/s00412-007-0102-z
pubmed: 17483978
Hudakova S, Michalek W, Presting GG, ten Hoopen R, dos Santos K, Jasencakova Z, Schubert I (2001) Sequence organization of barley centromeres. Nucleic Acids Res 29:5029–5035. https://doi.org/10.1093/nar/29.24.5029
doi: 10.1093/nar/29.24.5029
pubmed: 11812833
pmcid: 97617
Islam AKMR, Shepherd KW, Sparrow DHB (1978) Production and characterization of wheat-barley addition lines. In: Proceedings of 5th international wheat genetics symposium (New Delhi). pp 365–371
Islam AKMR, Shepherd KW, Sparrow DHB (1981) Isolation and characterization of euplasmic wheat-barley chromosome addition lines. Heredity (Edinb) 46:161–174. https://doi.org/10.1038/hdy.1981.24
doi: 10.1038/hdy.1981.24
Jo S-H, Koo D-H, Kim JF, Hur C-G, Lee S, Yang T, Kwon S-Y, Choi D (2009) Evolution of ribosomal DNA-derived satellite repeat in tomato genome. BMC Plant Biol 9:42. https://doi.org/10.1186/1471-2229-9-42
doi: 10.1186/1471-2229-9-42
pubmed: 19351415
pmcid: 2679016
Jouve N, Carmona A, De Bustos A, Cuadrado A (2018) The phylogenetic relationships of species and cytotypes in the genus Hordeum based on molecular karyotyping. Curr Res Phylogenet Evol Biol. https://doi.org/10.29011/CRPEB
Kato A (2011) High-density fluorescence in situ hybridization signal detection on barley (Hordeum vulgare L.) chromosomes with improved probe screening and reprobing procedures. Genome 54:151–159. https://doi.org/10.1139/G10-098
doi: 10.1139/G10-098
pubmed: 21326371
Kruppa K, Türkösi E, Szakács É, Cseh A, Molnár-Láng M (2013) Development and identification of a 4HL.5DL wheat/barley centric fusion using GISH, FISH and SSR markers. Cereal Res Commun 41:221–229. https://doi.org/10.1556/CRC.2012.0038
doi: 10.1556/CRC.2012.0038
Langdon T, Seago C, Mende M, Leggett M, Thomas H, Forster JW, Thomas H, Jones RN, Jenkins G (2000) Retrotransposon evolution in diverse plant genomes. Genetics 156:313–325. https://doi.org/10.1093/genetics/156.1.313
doi: 10.1093/genetics/156.1.313
pubmed: 10978295
pmcid: 1461242
Martin A, Martin L, Ballesteros J (1998) The potential of Hordeum chilense in breeding Triticeae species. Science Publishers Inc., Enfield, pp 377–386
Martín A, Alvarez JB, Martin LM, Barro F, Ballesteros J (1999) The development of Tritordeum: a novel cereal for food processing. J Cereal Sci 30:85–95. https://doi.org/10.1006/jcrs.1998.0235
doi: 10.1006/jcrs.1998.0235
Martín AC, Atienza SG, Ramírez MC, Barro F, Martín A (2010) Molecular and cytological characterization of an extra acrocentric chromosome that restores male fertility of wheat in the msH1 CMS system. Theor Appl Genet 121:1093–1101. https://doi.org/10.1007/s00122-010-1374-x
doi: 10.1007/s00122-010-1374-x
pubmed: 20549484
Mascher M, Wicker T, Jenkins J, Plott C, Lux T, Koh CS, Ens J, Gundlach H, Boston LB, Tulpová Z, Holden S, Hernández-Pinzón I, Scholz U, Mayer KFX, Spannagl M, Pozniak CJ, Sharpe AG, Šimková H, Moscou MJ, Grimwood J, Schmutz J, Stein N (2021) Long-read sequence assembly: a technical evaluation in barley. Plant Cell 33:1888–1906. https://doi.org/10.1093/plcell/koab077
doi: 10.1093/plcell/koab077
pubmed: 33710295
pmcid: 8290290
Meštrović N, Mravinac B, Pavlek M, Vojvoda-Zeljko T, Šatović E, Plohl M (2015) Structural and functional liaisons between transposable elements and satellite DNAs. Chromosom Res 23:583–596. https://doi.org/10.1007/s10577-015-9483-7
doi: 10.1007/s10577-015-9483-7
Miller TE, Reader SM, Chapman V (1982) The addition of Hordeum chilense chromosomes to wheat [Phenotypes]. Induced variability in plant breeding : international symposium/of the section Mutation and Polyploidy of the European Association for Research on Plant Breeding, Wageningen, August 31–September 4, 1981/Chairman, C. Broertjes
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326. https://doi.org/10.1093/NAR/8.19.4321
doi: 10.1093/NAR/8.19.4321
pubmed: 7433111
pmcid: 324241
Nagaki K, Tsujimoto H, Isono K, Sasakuma T (1995) Molecular characterization of a tandem repeat, Afa family, and its distribution among Triticeae. Genome 38:479–486. https://doi.org/10.1139/g95-063
doi: 10.1139/g95-063
pubmed: 7557360
Naranjo T (2015) Contribution of structural chromosome mutants to the study of meiosis in plants. Cytogenet Genome Res 147:55–69. https://doi.org/10.1159/000442219
doi: 10.1159/000442219
pubmed: 26658116
Nasuda S, Hudakova S, Schubert I, Houben A, Endo TR (2005) Stable barley chromosomes without centromeric repeats. Proc Natl Acad Sci USA 102:9842–9847. https://doi.org/10.1073/pnas.0504235102
doi: 10.1073/pnas.0504235102
pubmed: 15998740
pmcid: 1175009
Navajas-Pérez R, la de Herrán R, Jamilena M, Lozano R, Rejón CR, Rejón MR, Garrido-Ramos MA (2005) Reduced rates of sequence evolution of Y-linked satellite DNA in Rumex (polygonaceae). J Mol Evol 60:391–399. https://doi.org/10.1007/s00239-004-0199-0
doi: 10.1007/s00239-004-0199-0
pubmed: 15871049
Navrátilová P, Toegelová H, Tulpová Z, Kuo Y-T, Stein N, Doležel J, Houben A, Šimková H, Mascher M (2022) Prospects of telomere-to-telomere assembly in barley: analysis of sequence gaps in the MorexV3 reference genome. Plant Biotechnol J 20:1373–1386. https://doi.org/10.1111/pbi.13816
doi: 10.1111/pbi.13816
pubmed: 35338551
pmcid: 9241371
Neumann P, Požárková D, Macas J (2003) Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced. Plant Mol Biol 53:399–410. https://doi.org/10.1023/B:PLAN.0000006945.77043.ce
doi: 10.1023/B:PLAN.0000006945.77043.ce
pubmed: 14750527
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 29:792–793. https://doi.org/10.1093/bioinformatics/btt054
doi: 10.1093/bioinformatics/btt054
pubmed: 23376349
Novák P, Ávila Robledillo L, Koblížková A, Vrbová I, Neumann P, Macas J (2017) TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Res 45:e111–e111. https://doi.org/10.1093/nar/gkx257
doi: 10.1093/nar/gkx257
pubmed: 28402514
pmcid: 5499541
Novák P, Neumann P, Macas J (2020) Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nat Protoc 15:3745–3776. https://doi.org/10.1038/s41596-020-0400-y
doi: 10.1038/s41596-020-0400-y
pubmed: 33097925
Pedersen C, Langridge P (1997) Identification of the entire chromosome complement of bread wheat by two-colour FISH. Genome 40:589–593. https://doi.org/10.1139/G97-077
doi: 10.1139/G97-077
pubmed: 18464850
Pedersen C, Rasmussen SK, LindeLaursen I (1996) Genome and chromosome identification in cultivated barley and related species of the Triticeae (Poaceae) by in situ hybridization with the GAA-satellite sequence. Genome 39:93–104. https://doi.org/10.1139/g96-013
doi: 10.1139/g96-013
pubmed: 8851798
Presting GG, Malysheva L, Fuchs J, Schubert I (1998) A Ty3/gypsy retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes. Plant J 16:721–728. https://doi.org/10.1046/j.1365-313x.1998.00341.x
doi: 10.1046/j.1365-313x.1998.00341.x
pubmed: 10069078
Prieto P, Ramíarez MC, Ballesteros J, Cabrera A (2001) Identification of intergenomic translocations involving wheat, Hordeum vulgare and Hordeum chilense chromosomes by FISH. Hereditas 135:171–174. https://doi.org/10.1111/j.1601-5223.2001.t01-1-00171.x
doi: 10.1111/j.1601-5223.2001.t01-1-00171.x
pubmed: 12152330
Prieto P, Martín A, Martín M, Cabrera A, Martín A, Cabrera A (2004a) Chromosomal distribution of telomeric and telomeric-associated sequences in Hordeum chilense by in situ hybridization. Hereditas. https://doi.org/10.1111/j.1601-5223.2004.01825.x
doi: 10.1111/j.1601-5223.2004.01825.x
pubmed: 15660972
Prieto P, Shaw P, Moore G (2004b) Homologue recognition during meiosis is associated with a change in chromatin conformation. Nat Cell Biol 6:906–908. https://doi.org/10.1038/ncb1168
doi: 10.1038/ncb1168
pubmed: 15340450
Rayburn AL, Gill BS (1986) Isolation of a D-genome specific repeated DNA sequence fromAegilops squarrosa. Plant Mol Biol Rep 4:102–109. https://doi.org/10.1007/BF02732107
doi: 10.1007/BF02732107
Rey MD, Moore G, Martín AC, Scoles G (2018) Identification and comparison of individual chromosomes of three accessions of Hordeum chilense, Hordeum vulgare, and Triticum aestivum by FISH. Genome 61:387–396. https://doi.org/10.1139/gen-2018-0016
doi: 10.1139/gen-2018-0016
pubmed: 29544080
Rubiales D, Reader SM, Martín A (2000) Chromosomal location of resistance to Septoria tritici in Hordeum chilense determined by the study of chromosomal addition and substitution lines in “Chinese Spring” wheat. Euphytica 115:221–224. https://doi.org/10.1023/A:1004097830103
doi: 10.1023/A:1004097830103
Ruiz-Ruano FJ, López-León MD, Cabrero J, Camacho JPM (2016) High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep 6:28333. https://doi.org/10.1038/srep28333
doi: 10.1038/srep28333
pubmed: 27385065
pmcid: 4935994
Ruiz-Ruano FJ, Navarro-Domínguez B, Camacho JPM, Garrido-Ramos MA (2019) Characterization of the satellitome in lower vascular plants: the case of the endangered fern Vandenboschia speciosa. Ann Bot 123:587–599. https://doi.org/10.1093/aob/mcy192
doi: 10.1093/aob/mcy192
pubmed: 30357311
Sales-Oliveira VC, dos Santos RZ, Goes CAG, Calegari RM, Garrido-Ramos MA, Altmanová M, Ezaz T, Liehr T, Porto-Foresti F, Utsunomia R, Cioffi MB (2024) Evolution of ancient satellite DNAs in extant alligators and caimans (Crocodylia, Reptilia). BMC Biol 22:47. https://doi.org/10.1186/s12915-024-01847-8
doi: 10.1186/s12915-024-01847-8
pubmed: 38413947
pmcid: 10900743
Sanmiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82:37–44. https://doi.org/10.1006/anbo.1998.0746
doi: 10.1006/anbo.1998.0746
Šatović-Vukšić E, Plohl M (2023) Satellite DNAs—from localized to highly dispersed genome components. Genes (Basel) 14
Schmieder R, Edwards R (2011) Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS ONE 6:e17288
doi: 10.1371/journal.pone.0017288
pubmed: 21408061
pmcid: 3052304
Serrano-León IM, Prieto P, Aguilar M (2023) Telomere and subtelomere high polymorphism might contribute to the specificity of homologous recognition and pairing during meiosis in barley in the context of breeding. BMC Genomics 24:642. https://doi.org/10.1186/s12864-023-09738-y
doi: 10.1186/s12864-023-09738-y
pubmed: 37884878
pmcid: 10601145
Sharma A, Wolfgruber TK, Presting GG (2013) Tandem repeats derived from centromeric retrotransposons. BMC Genomics 14:142. https://doi.org/10.1186/1471-2164-14-142
doi: 10.1186/1471-2164-14-142
pubmed: 23452340
pmcid: 3648361
Smit A, Hubley R, Green P (2015) RepeatMasker Open-4.0. http://www.repeatmasker.org
Smith GP (1976) Evolution of repeated DNA sequences by unequal crossover. Science (80-) 191:528–535. https://doi.org/10.1126/science.1251186
doi: 10.1126/science.1251186
Stupar RM, Song J, Tek AL, Cheng Z, Dong F, Jiang J (2002) Highly condensed potato pericentromeric heterochromatin contains rDNA-related tandem repeats. Genetics 162:1435–1444. https://doi.org/10.1093/genetics/162.3.1435
doi: 10.1093/genetics/162.3.1435
pubmed: 12454086
pmcid: 1462313
Szakács É, Kruppa K, Molnár-Láng M (2013) Analysis of chromosomal polymorphism in barley (Hordeum vulgare L. ssp. vulgare) and between H. vulgare and H. chilense using three-color fluorescence in situ hybridization (FISH). J Appl Genet 54:427–433. https://doi.org/10.1007/s13353-013-0167-8
doi: 10.1007/s13353-013-0167-8
pubmed: 23990510
Thormann I, Reeves P, Reilley A, Engels JMM, Lohwasser U, Börner A, Pillen K, Richards CM (2016) Geography of Genetic Structure in Barley Wild Relative Hordeum vulgare subsp. spontaneum in Jordan. PLoS ONE 11:e0160745
doi: 10.1371/journal.pone.0160745
pubmed: 27513459
pmcid: 4981475
Vondrak T, Robledillo LÁ, Novák P, Koblížková A, Neumann P, Macas J (2020) Characterization of repeat arrays in ultra-long nanopore reads reveals frequent origin of satellite DNA from retrotransposon-derived tandem repeats. Plant J 101:484–500. https://doi.org/10.1111/tpj.14546
doi: 10.1111/tpj.14546
pubmed: 31559657
Zhang J, Zhang B, Su H, Birchler JA, Han F (2014) Molecular mechanisms of homologous chromosome pairing and segregation in plants. J Genet Genomics 41(3):117–123
doi: 10.1016/j.jgg.2013.12.003
pubmed: 24656232