How diverse is heterochromatin in the Caesalpinia group? Cytogenomic characterization of Erythrostemon hughesii Gagnon & G.P. Lewis (Leguminosae: Caesalpinioideae)

Mata-Sucre, Yennifer; Sader, Mariela; Van-Lume, Brena; Gagnon, Edeline; Pedrosa-Harand, Andrea; Leitch, Ilia J.; Lewis, Gwilym P.; Souza, Gustavo

doi:10.1007/s00425-020-03453-8

How diverse is heterochromatin in the Caesalpinia group? Cytogenomic characterization of Erythrostemon hughesii Gagnon & G.P. Lewis (Leguminosae: Caesalpinioideae)

Original Article
Published: 12 September 2020

Volume 252, article number 49, (2020)
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Yennifer Mata-Sucre¹,
Mariela Sader¹,
Brena Van-Lume¹,
Edeline Gagnon²,
Andrea Pedrosa-Harand¹,
Ilia J. Leitch³,
Gwilym P. Lewis³ &
…
Gustavo Souza ORCID: orcid.org/0000-0002-5700-6097¹

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Abstract

Main conclusion

Cytogenomic characterization of Erythrostemon hughesii reveals a heterogeneity of repeats in its subtelomeric heterochromatin. Comparative analyses with other Caesalpinia group species reveal a significant reduction in the abundance of Ty3-gypsy/Chromovirus Tekay retrotransposons during its evolution.

In numerically stable karyotypes, repetitive DNA variability is one of the main causes of genome and chromosome variation and evolution. Species from the Caesalpinia group (Leguminosae) are karyotypically characterized by 2n = 24, with small chromosomes and highly variable CMA⁺ heterochromatin banding patterns that correlate with environmental variables. Erythrostemon hughesii differs from other species of the group examined to date for having subtelomeric CMA⁺ bands; this contrasts with most species in the group which have proximal bands. Here we analyse the repeatome of E. hughesii using genome skimming and chromosomal mapping approaches to characterize the identity of the most abundant repetitive elements and their physical location. The repetitive fraction of E. hughesii comprises 28.73% of the genome. The most abundant elements were retrotransposons (RT) with long terminal repeats (LTR-RT; 9.76%) and satellite DNAs (7.83%). Within the LTR-RTs, the most abundant lineages were: Ty1/copia-Ale (1%), Ty3/gypsy CRM (0.88%) and Ty3/gypsy Athila (0.75%). Using fluorescent in situ hybridization four satellite DNAs and several LTR-RT elements were shown to be present in most subtelomeric CMA⁺ bands. These results highlight how the repeatome in E. hughesii, a species from Oaxaca state in Mexico, is clearly distinct from Northeast Brazilian species of the Caesalpinia group, mainly due to its high diversity of repeats in its subtelomeric heterochromatic bands and low amount of LTR-RT Ty3/gypsy-Tekay elements. Comparative sequence analysis of Tekay elements from different species is congruent with a clade-specific origin of this LTR-RT after the divergence of the Caesalpinia group. We hypothesize that repeat-rich heterochromatin may play a role in leading to faster genomic divergence between individuals, increasing speciation and diversification.

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Evolutionary convergence or homology? Comparative cytogenomics of Caesalpinia group species (Leguminosae) reveals diversification in the pericentromeric heterochromatic composition

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Abbreviations

CMA:: Chromomycin A3
DANTE:: Domain-based annotation of transposable elements
DAPI:: 4′, 6-Diamidino-2-phenylindole
FISH:: Fluorescent in situ hybridization
LTR:: Long terminal repeat
NGS:: Next Generation Sequencing
rDNA:: Ribosomal DNA
RT:: Retrotransposons
satDNA:: Satellite DNA
TAREAN:: TAndem REpeat ANalyser
TE:: Transposable elements

References

Aïnouche A, Paris A, Giraud D, Keller J, Raimondeau P, Mahé F, Neuman P, Novak P, Macas J, Aïnouche M et al (2020) The repetitive content in lupin genomes. In: Singh KB, Kamphuis LG, Nelson MN (eds) The Lupin Genome. Springer International Publishing, Cham, pp 161–186
Chapter Google Scholar
Ambrožová K, Mandáková T, Bureš P, Neumann P, Leitch IJ, Koblížková A, Macas J, Lysak MA (2011) Diverse retrotransposon families and an AT-rich satellite DNA revealed in giant genomes of Fritillaria lilies. Ann Bot 107:255–268
Article PubMed Google Scholar
Baniaga A, Barker M (2019) Nuclear genome size is positively correlated with median LTR-retroelement insertion time in fern and lycophyte genomes. Am Fern J 109(3):248–266. https://doi.org/10.1640/0002-8444-109.3.248
Article Google Scholar
Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A, Deragon JM et al (2009) (2009) Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet 5:e1000732. https://doi.org/10.1371/journal.pgen.1000732
Article CAS PubMed PubMed Central Google Scholar
Beltrão GTA, Guerra M (1990) Citogenética de angiospermas coletadas em Pernambuco-III. Ciência e Cultura 42(10):839–845
Google Scholar
Belyayev A, Josefiová J, Jandová M, Kalendar R, Krak K, Mandák B (2019) Natural history of a satellite DNA family: from the ancestral genome component to species-specific sequences, concerted and non-concerted evolution. Int J Mol Sci 20(5):1201. https://doi.org/10.3390/ijms20051201
Article CAS PubMed Central Google Scholar
Belyayev A, Raskina O, Nevo E (2001) Chromosomal distribution of reverse transcriptase-containing retroelements in two Triticeae species. Chrom Res 9(2):129–136. https://doi.org/10.1023/A:1009231019833
Article CAS PubMed Google Scholar
Bennetzen JL, Wang H (2014) The contributions of transposable elements to the structure, function, and evolution of plant genomes. Ann Rev Plant Biol 65(1):505–530. https://doi.org/10.1146/annurev-arplant-050213-035811
Article CAS Google Scholar
Bergman CM, Quesneville H, Anxolabéhère D, Ashburner M (2006) Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome. Genome Biol 7:R112. https://doi.org/10.1186/gb-2006-7-11-r112
Article CAS PubMed PubMed Central Google Scholar
Borges LA, Souza LGR, Guerra M, Machado IC, Lewis GP, Lopes AV (2012) Reproductive isolation between diploid and tetraploid cytotypes of Libidibia ferrea (= Caesalpinia ferrea) (Leguminosae): ecological and taxonomic implications. Plant Syst Evol 298(7):1371–1381. https://doi.org/10.1007/s00606-012-0643-3
Article Google Scholar
Bourque G, Burns KH, Gehring M, Gorbunova V, Seluanov A, Hammell M, Imbeault M, Izsvák Z, Levin HL, Macfarlan TS et al (2018) Ten things you should know about transposable elements. Genome Biol 19:199. https://doi.org/10.1186/s13059-018-1577-z
Article CAS PubMed PubMed Central Google Scholar
Brodie R, Roper RL, Upton C (2004) JDotter: a Java interface to multiple dotplots generated by dotter. Bioinformatics 20(2):279–281. https://doi.org/10.1093/bioinformatics/btg406
Article CAS PubMed Google Scholar
Coline G, Théron E, Brasset E, Vaury C (2014) History of the discovery of a master locus producing piRNAs: the flamenco/COM locus in Drosophila melanogaster. Front Genet 5:257. https://doi.org/10.3389/fgene.2014.00257
Article CAS PubMed Central Google Scholar
De Setta N, Metcalfe CJ, Cruz GM, Ochoa EA, Van Sluys MA (2012) Noise or symphony: comparative evolutionary analysis of sugarcane transposable elements with other grasses. In: Grandbastien MA, Casacuberta J (eds) Plant Transposable Elements. Springer, Berlin, Heidelberg, pp 169–192. https://doi.org/10.1007/978-3-642-31842-9_10
Chapter Google Scholar
Dierckxsens N, Mardulyn P, Smits G (2016) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45(4):e18–e18. https://doi.org/10.1093/nar/gkw955
Article CAS PubMed Central Google Scholar
Feschotte C, Zhang X, Wessler SR (2002) Miniature inverted-repeat transposable elements and their relationship to established DNA transposons. In: Craig N, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II. ASM Press, Washington, DC, pp 1147–1158. https://doi.org/10.1128/9781555817954.ch50
Chapter Google Scholar
Gaeta ML, Yuyama PM, Sartori D, Fungaro MHP, Vanzela ALL (2010) Occurrence and chromosome distribution of retroelements and NUPT sequences in Copaifera langsdorffii Desf (Caesalpinioideae). Chromosome Res 18(4):515–524. https://doi.org/10.1007/s10577-010-9131-1
Article CAS PubMed Google Scholar
Gagnon E, Bruneau A, Hughes CE, de Queiroz LP, Lewis GP (2016) A new generic system for the pantropical Caesalpinia group (Leguminosae). PhytoKeys 71:1–160. https://doi.org/10.3897/phytokeys.71.9203
Article Google Scholar
Gagnon E, Ringelberg JJ, Bruneau A, Lewis GP, Hughes CE (2019) Global succulent biome phylogenetic conservatism across the pantropical Caesalpinia group (Leguminosae). New Phytol 222(4):1994–2008. https://doi.org/10.1111/nph.15633
Article PubMed Google Scholar
Gao D, Jiang N, Wing RA, Jiang J, Jackson SA (2015) Transposons play an important role in the evolution and diversification of centromeres among closely related species. Front Plant Sci 6:216. https://doi.org/10.3389/fpls.2015.00216
Article PubMed PubMed Central Google Scholar
Garrido-Ramos MA (2015) Satellite DNA in plants: more than just rubbish. Cytogenet Genome Res 146(2):153–170. https://doi.org/10.1159/000437008
Article CAS PubMed Google Scholar
Garrido-Ramos MA (2017) Satellite DNA: an evolving topic. Genes 8(9):230. https://doi.org/10.3390/genes8090230
Article CAS PubMed Central Google Scholar
Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7(7):1869–1885. https://doi.org/10.1093/nar/7.7.1869
Article CAS PubMed PubMed Central Google Scholar
Giordano J, Ge Y, Gelfand Y, Abrusán G, Benson G, Warburton PE (2007) Evolutionary history of mammalian transposons determined by genome-wide defragmentation. PLoS Comput Biol 3:e137. https://doi.org/10.1371/journal.pcbi.0030137
Article CAS PubMed PubMed Central Google Scholar
Goubert C, Modolo L, Vieira C, ValienteMoro C, Mavingui P, Boulesteix M (2015) De novo assembly and annotation of the Asian tiger mosquito (Aedes albopictus) repeatome with dnaPipeTE from raw genomic reads and comparative analysis with the yellow fever mosquito (Aedes aegypti). Genome Biol Evol 7(4):1192–1205. https://doi.org/10.1093/gbe/evv050
Article CAS PubMed PubMed Central Google Scholar
Hannan AJ (2018) Tandem repeats and repeatomes: delving deeper into the ‘Dark Matter’ of genomes. EBioMedicine 31:3–4. https://doi.org/10.1016/j.ebiom.2018.04.004
Article PubMed PubMed Central Google Scholar
Heslop-Harrison JS, Schwarzacher T (2007) Domestication, genomics and the future for banana. Ann Bot-Lond 100(5):1073–1084. https://doi.org/10.1093/aob/mcm191
Article CAS Google Scholar
Heslop-Harrison JS, Schwarzacher T (2011) Organisation of the plant genome in chromosomes. Plant J 66(1):18–33. https://doi.org/10.1111/j.1365-313X.2011.04544.x
Article CAS PubMed Google Scholar
Horváth V, Merenciano M, González J (2017) Revisiting the relationship between transposable elements and the eukaryotic stress response. Trends Genet 33(11):832–841. https://doi.org/10.1016/j.tig.2017.08.007
Article CAS PubMed Google Scholar
Hloušková P, Mandáková T, Pouch M, Trávníček P, Lysak MA (2019) The large genome size variation in the Hesperis clade was shaped by the prevalent proliferation of DNA repeats and rarer genome downsizing. Ann Bot-Lond 124:103–120. https://doi.org/10.1093/aob/mcz036
Article CAS Google Scholar
Janssen A, Colmenares SU, Karpen GH (2018) Heterochromatin: guardian of the genome. Annu Rev Cell Dev Biol 34:265–288. https://doi.org/10.1146/annurev-cellbio-100617-062653
Article CAS PubMed Google Scholar
Jouffroy O, Saha S, Mueller L, Quesneville H, Maumus F (2016) Comprehensive repeatome annotation reveals strong potential impact of repetitive elements on tomato ripening. BMC Genomics 17(1):624. https://doi.org/10.1186/s12864-016-2980-z
Article CAS PubMed PubMed Central Google Scholar
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780. https://doi.org/10.1093/molbev/mst010
Article CAS PubMed PubMed Central Google Scholar
Kazazian HH (2004) Mobile elements: drivers of genome evolution. Science 303(5664):1626–1632. https://doi.org/10.1126/science.1089670
Article CAS PubMed Google Scholar
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Article PubMed PubMed Central Google Scholar
Kelly LJ, Renny-Byfield S, Pellicer J, Macas J, Novák P, Neumann P et al (2015) Analysis of the giant genomes of Fritillaria (Liliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size. New Phytol 208:596–607. https://doi.org/10.1111/nph.13471
Article CAS PubMed PubMed Central Google Scholar
Koukalova B, Moraes AP, Renny-Byfield S, Matyasek R, Leitch A, Kovarik A (2009) Fall and rise of satellite repeats in allopolyploids of Nicotiana over c. 5 million years. New Phytol 186:148–160
Article PubMed Google Scholar
Krupovic M, Blomberg J, Coffin JM, Dasgupta I, Fan H, Geering AD et al (2018) Ortervirales: new virus order unifying five families of reverse-transcribing viruses. J Virol 92:1–5. https://doi.org/10.1128/JVI.00515-18
Article Google Scholar
Lee YI, Yap JW, Izan S, Leitch IJ, Fay MF, Lee YC, Leitch AR et al (2018) Satellite DNA in Paphiopedilum subgenus Parvisepalum as revealed by high-throughput sequencing and fluorescent in situ hybridization. BMC Genomics 19(1):578. https://doi.org/10.1186/s12864-018-4956-7
Article CAS PubMed PubMed Central Google Scholar
Li SF, Guo YJ, Li JR, Zhang DX, Wang BX, Li N, Gao WJ et al (2019) The landscape of transposable elements and satellite DNAs in the genome of a dioecious plant spinach (Spinacia oleracea L.). Mobile DNA 10(1):3. https://doi.org/10.1186/s13100-019-0147-6
Article CAS PubMed PubMed Central Google Scholar
Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61. https://doi.org/10.1038/nrg3374
Article CAS PubMed Google Scholar
Liu Q, Li X, Zhou X, Li M, Zhang F, Schwarzacher T, Heslop-Harrison JS (2019) The repetitive DNA landscape in Avena (Poaceae): chromosome and genome evolution defined by major repeat classes in whole-genome sequence reads. BMC Plant Biol 19(1):226. https://doi.org/10.1186/s12870-019-1769-z
Article CAS PubMed PubMed Central Google Scholar
Mata-Sucre Y, Costa L, Gagnon E, Lewis GP, Leitch IJ, Souza G (2020) Revisiting the cytomolecular evolution of the Caesalpinia group (Leguminosae): a broad sampling reveals new correlations between cytogenetic and environmental variables. Plant Syst Evol 306:1–13. https://doi.org/10.1007/s00606-020-01674-8
Article CAS Google Scholar
Ma J, Wing RA, Bennetzen JL, Jackson SA (2007) Plant centromere organization: a dynamic structure with conserved functions. Trends Genet 23(3):134–139. https://doi.org/10.1016/j.tig.2007.01.004
Article CAS PubMed Google Scholar
Macas J, Novák P, Pellicer J, Čížková J, Koblížková A, Neumann P, Leitch IJ et al (2015) In depth characterization of repetitive DNA in 23 plant genomes reveals sources of genome size variation in the legume tribe Fabeae. PLoS ONE 10(11):e0143424. https://doi.org/10.1371/journal.pone.0143424
Article CAS PubMed PubMed Central Google Scholar
Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Gwadz M et al (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39(1):225–229. https://doi.org/10.1093/nar/gkq1189
Article CAS Google Scholar
Maumus F, Quesneville H (2016) Impact and insights from ancient repetitive elements in plant genomes. Curr Opin Plant Biol 30:41–46. https://doi.org/10.1016/j.pbi.2016.01.003
Article CAS PubMed Google Scholar
Neumann P, Novák P, Hoštáková N, Macas J (2019) Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mobile DNA 10(1):1. https://doi.org/10.1186/s13100-018-0144-1
Article PubMed PubMed Central Google Scholar
Nie Q, Qiao G, Peng L, Wen X (2019) Transcriptional activation of long terminal repeat retrotransposons sequences in the genome of pitaya under abiotic stress. Plant Physiol Bioch 135:460–468. https://doi.org/10.1016/j.plaphy.2018.11.014
Article CAS Google Scholar
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(12):e111–e111. https://doi.org/10.1093/nar/gkx257
Article CAS PubMed PubMed Central Google Scholar
Novák P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform 11(1):378. https://doi.org/10.1186/1471-2105-11-378
Article CAS Google Scholar
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
Article CAS PubMed Google Scholar
Paço A, Freitas R, Vieira-da-Silva A (2019) Conversion of DNA sequences: from a transposable element to a tandem repeat or to a gene. Genes 10(12):1014. https://doi.org/10.3390/genes10121014
Article CAS PubMed Central Google Scholar
Pedrosa A, Sandal N, Stougaard J, Schweizer D, Bachmair A (2002) Chromosomal map of the model legume Lotus japonicus. Genetics 161(4):1661–1672
CAS PubMed PubMed Central Google Scholar
Piccoli MCA, Bardella VB, Cabral-de-Mello DC (2018) Repetitive DNAs in Melipona scutellaris (Hymenoptera: Apidae: Meliponidae): chromosomal distribution and test of multiple heterochromatin amplification in the genus. Apidologie 49(4):497–504. https://doi.org/10.1007/s13592-018-0577-z
Article CAS Google Scholar
Pita S, Díaz-Viraqué F, Iraola G, Robello C (2019) The Tritryps comparative repeatome: insights on repetitive element evolution in Trypanosomatid pathogens. Genome Biol Evol 11(2):546–551. https://doi.org/10.1093/gbe/evz017
Article CAS PubMed PubMed Central Google Scholar
Plohl M, Meštrović N, Mravinac B (2012) Satellite DNA evolution. In: Garrido-Ramos MA (ed) Repetitive DNA. Karger Publishers, Berlin, pp 126–152
Chapter Google Scholar
Rebollo R, Karimi MM, Bilenky M, Gagnier L, Miceli-Royer K, Zhang Y, Lorincz MC et al (2011) Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms. PLoS Genet 7(9):e1002301. https://doi.org/10.1371/journal.pgen.1002301
Article CAS PubMed PubMed Central Google Scholar
Ren L, Huang W, Cannon EKS, Bertioli DJ, Cannon SB (2018) A mechanism for genome size reduction following genomic rearrangements. Front Genet 9:454–454. https://doi.org/10.3389/fgene.2018.00454
Article CAS PubMed PubMed Central Google Scholar
Ribeiro T, dos Santos KG, Richard MM, Sévignac M, Thareau V, Geffroy V, Pedrosa-Harand A (2017) Evolutionary dynamics of satellite DNA repeats from Phaseolus beans. Protoplasma 254(2):791–801. https://doi.org/10.1007/s00709-016-0993-8
Article CAS PubMed Google Scholar
Ribeiro T, Vasconcelos E, dos Santos KG, Vaio M, Brasileiro-Vidal AC, Pedrosa-Harand A (2019) Diversity of repetitive sequences within compact genomes of Phaseolus L. beans and allied genera Cajanus L. and Vigna Savi. Chromosome Res. https://doi.org/10.1007/s10577-019-09618-w
Article PubMed Google Scholar
Richard GF, Kerrest A, Dujon B (2008) Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiol Mol Biol Rev 72(4):686–727. https://doi.org/10.1128/MMBR.00011-08
Article CAS PubMed PubMed Central Google Scholar
Robledillo LÁ, Koblížková A, Novák P, Böttinger K, Vrbová I, Neumann P, Macas J et al (2018) Satellite DNA in Vicia faba is characterized by remarkable diversity in its sequence composition, association with centromeres, and replication timing. Sci Rep-UK 8(1):1–11. https://doi.org/10.1038/s41598-018-24196-3
Article CAS Google Scholar
Rodrigues PS, Souza MM, Corrêa RX (2014) Karyomorphology and karyotype asymmetry in the South American Caesalpinia species (Leguminosae: Caesalpinioideae). Genet Mol Biol 13:8278–8293. https://doi.org/10.4238/2014.October.20.4
Article CAS Google Scholar
Rodrigues PS, Souza MM, Melo CAF, Pereira TNS, Corrêa RX (2018) Karyotype diversity and 2C DNA content in species of the Caesalpinia group. BMC Genet 19(1):25. https://doi.org/10.1186/s12863-018-0610-2
Article CAS PubMed PubMed Central Google Scholar
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Misener S, Krawetz SA (eds) Bioinformatics Methods and Protocols. Methods in Molecular Biology™ vol 132. Humana Press, Totowa, pp 365–386
Ruban A, Fuchs J, Marques A, Schubert V, Soloviev A, Raskina O, Houben A (2014) B chromosomes of Aegilops speltoides are enriched in organelle genome-derived sequences. PLoS ONE 9(2):e90214. https://doi.org/10.1371/journal.pone.0090214
Article CAS PubMed PubMed Central Google Scholar
Ruiz-Ruano FJ, López-León MD, Cabrero J, Camacho JPM (2016) High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep-UK 6:28333. https://doi.org/10.1038/srep28333
Article CAS Google Scholar
Samoluk SS, Chalup LM, Chavarro C, Robledo G, Bertioli DJ, Jackson SA, Seijo G (2019) Heterochromatin evolution in Arachis investigated through genome-wide analysis of repetitive DNA. Planta 249(5):1405–1415. https://doi.org/10.1007/s00425-019-03096-4
Article CAS PubMed Google Scholar
Samoluk SS, Robledo G, Bertioli D, Seijo JG (2017) Evolutionary dynamics of an at-rich satellite DNA and its contribution to karyotype differentiation in wild diploid Arachis species. Mol Genet Genomics 292(2):283–296. https://doi.org/10.1007/s00438-016-1271-3
Article CAS PubMed Google Scholar
Souza G, Costa L, Guignard MS, Van-Lume B, Pellicer J, Gagnon E, Lewis GP (2019) Do tropical plants have smaller genomes? Correlation between genome size and climatic variables in the Caesalpinia Group (Caesalpinioideae, Leguminosae). Persp Plant Ecol 38:13–23. https://doi.org/10.1016/j.ppees.2019.03.002
Article Google Scholar
Van-Lume B, Esposito T, Diniz-filho J, Gagnon E, Lewis G, Souza G (2017) Heterochromatic and cytomolecular diversification in the Caesalpinia group (Leguminosae): relationships between phylogenetic and cytogeographical data. Persp Plant Ecol 29:51–63. https://doi.org/10.1016/j.ppees.2017.11.004
Article Google Scholar
Van-Lume B, Mata-Sucre Y, Báez M, Ribeiro T, Huettel B, Gagnon E, Souza G et al (2019) Evolutionary convergence or homology? Comparative cytogenomics of Caesalpinia group species (Leguminosae) reveals diversification in the proximal heterochromatic composition. Planta 250(6):2173–2186. https://doi.org/10.1007/s00425-019-03287-z
Article CAS PubMed Google Scholar
Van’t Hof AE, Campagne P, Rigden DJ, Yung CJ, Lingley J, Quail MA, Hall N, Darby AC, Saccheri IJ (2016) The industrial melanism mutation in Britishpeppered moths is a transposable element. Nature 534:102–105. https://doi.org/10.1038/nature17951
Article CAS PubMed Google Scholar
Vitte C, Estep MC, Leebens-Mack J, Bennetzen JL (2013) Young, intact and nested retrotransposons are abundant in the onion and asparagus genomes. Ann Bot 112(5):881–889. https://doi.org/10.1093/aob/mct155
Article CAS PubMed PubMed Central Google Scholar
Weising K, Nybom H, Pfenninger M, Wolff K, Kahl G (2005) DNA fingerprinting in plants: principles, methods, and applications. CRC Press, Boca Raton
Book Google Scholar
Wendel JF, Jackson SA, Meyers BC, Wing RA (2016) Evolution of plant genome architecture. Genome Biol 17(1):1–14. https://doi.org/10.1186/s13059-016-0908-1
Article CAS Google Scholar
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Paux E et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982. https://doi.org/10.1038/nrg2165
Article CAS PubMed Google Scholar
Wicker T, Gundlach H, Spannagl M, Uauy C, Borrill P, Ramírez-González RH et al (2018) Impact of transposable elements on genome structure and evolution in bread wheat. Genome Biol 19:103. https://doi.org/10.1186/s13059-018-1479-0
Article CAS PubMed PubMed Central Google Scholar
Zhang QJ, Gao LZ (2017) Rapid and recent evolution of LTR retrotransposon drives rice genome evolution during the speciation of AAgenome Oryza species. G3 Genes Genom Genet 7(6):1875–1885. https://doi.org/10.1534/g3.116.037572
Article CAS Google Scholar
Zhang S, Zhu M, Shang Y, Wang J, Zhuang DL, Qi Z et al (2019) Physical organization of repetitive sequences and chromosome diversity of barley revealed by fluorescence in situ hybridization (FISH). Genome 62(5):329–339. https://doi.org/10.1139/gen-2018-0182
Article CAS PubMed Google Scholar

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Acknowledgements

The authors wish to thank Dra. Magdalena Vaio for her suggestions which improved the manuscript. We thank the Brazilian agencies Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Ciência e Tecnologia de Pernambuco (FACEPE—APQ- 0970- 2.03/15) for financial support. This study was partly financed by the CAPES (finance Code 001). G.S. receives a productivity fellowship from CNPq (Process Number PQ—310693/2018-7).

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Authors and Affiliations

Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Federal University of Pernambuco, Rua Nelson Chaves S/N, Cidade Universitaria, Recife, PE, 50670-420, Brazil
Yennifer Mata-Sucre, Mariela Sader, Brena Van-Lume, Andrea Pedrosa-Harand & Gustavo Souza
Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5NZ, UK
Edeline Gagnon
Comparative Plant and Fungal Biology Department, Royal Botanic Gardens, Kew, Richmond, TW9 3AB, Surrey, UK
Ilia J. Leitch & Gwilym P. Lewis

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Yennifer Mata-Sucre
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Mariela Sader
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Brena Van-Lume
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Edeline Gagnon
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Andrea Pedrosa-Harand
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Ilia J. Leitch
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Gwilym P. Lewis
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Gustavo Souza
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Correspondence to Gustavo Souza.

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Communicated by Anastasios Melis.

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Mata-Sucre, Y., Sader, M., Van-Lume, B. et al. How diverse is heterochromatin in the Caesalpinia group? Cytogenomic characterization of Erythrostemon hughesii Gagnon & G.P. Lewis (Leguminosae: Caesalpinioideae). Planta 252, 49 (2020). https://doi.org/10.1007/s00425-020-03453-8

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Received: 21 May 2020
Accepted: 27 August 2020
Published: 12 September 2020
DOI: https://doi.org/10.1007/s00425-020-03453-8

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How diverse is heterochromatin in the Caesalpinia group? Cytogenomic characterization of Erythrostemon hughesii Gagnon & G.P. Lewis (Leguminosae: Caesalpinioideae)