Extraordinary Sequence Diversity and Promiscuity of Centromeric Satellites in the Legume Tribe Fabeae

. 2020 Aug 01 ; 37 (8) : 2341-2356.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu srovnávací studie, časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32259249

Satellite repeats are major sequence constituents of centromeres in many plant and animal species. Within a species, a single family of satellite sequences typically occupies centromeres of all chromosomes and is absent from other parts of the genome. Due to their common origin, sequence similarities exist among the centromere-specific satellites in related species. Here, we report a remarkably different pattern of centromere evolution in the plant tribe Fabeae, which includes genera Pisum, Lathyrus, Vicia, and Lens. By immunoprecipitation of centromeric chromatin with CENH3 antibodies, we identified and characterized a large and diverse set of 64 families of centromeric satellites in 14 species. These families differed in their nucleotide sequence, monomer length (33-2,979 bp), and abundance in individual species. Most families were species-specific, and most species possessed multiple (2-12) satellites in their centromeres. Some of the repeats that were shared by several species exhibited promiscuous patterns of centromere association, being located within CENH3 chromatin in some species, but apart from the centromeres in others. Moreover, FISH experiments revealed that the same family could assume centromeric and noncentromeric positions even within a single species. Taken together, these findings suggest that Fabeae centromeres are not shaped by the coevolution of a single centromeric satellite with its interacting CENH3 proteins, as proposed by the centromere drive model. This conclusion is also supported by the absence of pervasive adaptive evolution of CENH3 sequences retrieved from Fabeae species.

Zobrazit více v PubMed

Akera T, Chmátal L, Trimm E, Yang K, Aonbangkhen C, Chenoweth DM, Janke C, Schultz RM, Lampson MA.. 2017. Spindle asymmetry drives non-Mendelian chromosome segregation. Science 358(6363):668–672. PubMed PMC

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ.. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25(17):3389–3402. PubMed PMC

Ávila Robledillo L, Koblížková A, Novák P, Böttinger K, Vrbová I, Neumann P, Schubert I, Macas J.. 2018. Satellite DNA in Vicia faba is characterized by remarkable diversity in its sequence composition, association with centromeres, and replication timing. Sci Rep. 8(1):5838. PubMed PMC

Badr SF. 2006. Karyotype analysis and chromosome evolution in species of Lathyrus (Fabaceae). Cytologia 71(4):447–455. PubMed

Bilinski P, Distor K, Gutierrez-Lopez J, Mendoza Mendoza G, Shi J, Dawe RK, Ross-Ibarra J.. 2015. Diversity and evolution of centromere repeats in the maize genome. Chromosoma 124(1):57–65. PubMed

Birney E, Clamp M, Durbin R.. 2004. GeneWise and Genomewise. Genome Res. 14(5):988–995. PubMed PMC

Brankovics B, Zhang H, van Diepeningen AD, van der Lee TAJ, Waalwijk C, de Hoog GS.. 2016. GRAbB: selective assembly of genomic regions, a new niche for genomic research. PLoS Comput Biol. 12(6):e1004753. PubMed PMC

Cheeseman I. 2014. The kinetochore. Cold Spring Harb Perspect Biol. 6(7):a015826. PubMed PMC

Cooper JL, Henikoff S.. 2004. Adaptive evolution of the histone fold domain in centromeric histones. Mol Biol Evol. 21(9):1712–1718. PubMed

Dellaporta SL, Wood J, Hicks JB.. 1983. A plant DNA minipreparation: version II. Plant Mol Biol Rep. 1(4):19–21.

Dluhošová J, Ištvánek J, Nedělník J, Řepková J.. 2018. Red clover (Trifolium pratense) and zigzag clover (T. medium) – a picture of genomic similarities and differences. Front Plant Sci. 9:724. PubMed PMC

Dong F, Song J, Naess SK, Helgeson JP, Gebhardt C, Jiang J.. 2000. Development and applications of a set of chromosome-specific cytogenetic DNA markers in potato. Theor Appl Genet. 101:1001–1007.

Duda Z, Trusiak S, O’Neill R.. 2017. Centromere transcription: means and motive In: Black BE, editor. Centromeres and kinetochores, progress in molecular and subcellular biology. Cham (Switzerland: ): Springer; p. 257–281. PubMed

Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5):1792–1797. PubMed PMC

Finseth FR, Dong Y, Saunders A, Fishman L.. 2015. Duplication and adaptive evolution of a key centromeric protein in Mimulus, a genus with female meiotic drive. Mol Biol Evol. 32(10):2694–2706. PubMed

Fuchs J, Schubert I.. 2012. Chromosomal distribution and functional interpretation of epigenetic histone marks in plants In: Bass HW, Birchler JA, editors. Plant Cytogenetics. New York: Springer; p. 232–246.

Garrido-Ramos MA. 2015. Satellite DNA in plants: more than just rubbish. Cytogenet Genome Res. 146(2):153–170. PubMed

Garrido-Ramos MA. 2017. Satellite DNA: an evolving topic. Genes. 8(9):230. PubMed PMC

Gent JI, Wang N, Dawe RK.. 2017. Stable centromere positioning in diverse sequence contexts of complex and satellite centromeres of maize and wild relatives. Genome Biol. 18(1):121. PubMed PMC

Gong Z, Wu Y, Koblížková A, Torres GA, Wang K, Iovene M, Neumann P, Zhang W, Novák P, Buell CR, et al. 2012. Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24(9):3559–3574. PubMed PMC

Gouy M, Guindon S, Gascuel O.. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 27(2):221–224. PubMed

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O.. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 59(3):307–321. PubMed

Han F, Lamb JC, Mccaw ME, Gao Z, Zhang B, Swyers NC, Birchler JA, Anderson L.. 2018. Meiotic studies on combinations of chromosomes with different sized centromeres in maize. Front Plant Sci. 9:785. PubMed PMC

Hara M, Fukagawa T.. 2017. Critical foundation of the kinetochore: the Constitutive Centromere-Associated Network (CCAN) In: Black BE, editor. Centromeres and kinetochores, progress in molecular and subcellular biology. Vol. 56 Cham (Switzerland: ): Springer; p. 29–57. PubMed

Hartley G, O’Neill RJ.. 2019. Centromere repeats: hidden gems of the genome. Genes 10(3):223. PubMed PMC

Heckmann S, Macas J, Kumke K, Fuchs J, Schubert V, Ma L, Novák P, Neumann P, Taudien S, Platzer M, et al. 2013. The holocentric species Luzula elegans shows interplay between centromere and large-scale genome organization. Plant J. 73(4):555–565. PubMed

Henikoff S, Ahmad K, Malik HS.. 2001. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293(5532):1098–1102. PubMed

Hirsch CD, Wu Y, Yan H, Jiang J.. 2009. Lineage-specific adaptive evolution of the centromeric protein CENH3 in diploid and allotetraploid Oryza species. Mol Biol Evol. 26(12):2877–2885. PubMed

Iwata-Otsubo A, Dawicki-McKenna JM, Akera T, Falk SJ, Chmátal L, Yang K, Sullivan BA, Schultz RM, Lampson MA, Black BE.. 2017. Expanded satellite repeats amplify a discrete CENP-A nucleosome assembly site on chromosomes that drive in female meiosis. Curr Biol. 27(15):2365–2373. PubMed PMC

Kasinathan S, Henikoff S.. 2018. Non-B-form DNA is enriched at centromeres. Mol Biol Evol. 35(4):949–962. PubMed PMC

Kato A, Kato A, Albert PS, Vega JM, Kato A, Albert PS, Vega JM, Birchler JA.. 2006. Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotech Histochem. 81(2–3):71–78. PubMed

Kawabe A, Nasuda S, Charlesworth D.. 2006. Duplication of centromeric histone H3 (HTR12) gene in Arabidopsis halleri and A. lyrata, plant species with multiple centromeric satellite sequences. Genetics 174(4):2021–2032. PubMed PMC

Kosakovsky Pond SL, Frost S.. 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol. 22(5):1208–1222. PubMed

Kowar T, Zakrzewski F, Macas J, Koblížková A, Viehoever P, Weisshaar B, Schmidt T.. 2016. Repeat composition of CenH3-chromatin and H3K9me2-marked heterochromatin in sugar beet (Beta vulgaris). BMC Plant Biol. 16(1):120. PubMed PMC

Kumar S, Stecher G, Li M, Knyaz C, Tamura K.. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 35(6):1547–1549. PubMed PMC

Lavin M, Herendeen PS, Wojciechowski MF.. 2005. Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst Biol. 54(4):575–594. PubMed

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. PubMed PMC

Lefort V, Longueville J-E, Gascuel O.. 2017. SMS: smart model selection in PhyML. Mol Biol Evol. 34(9):2422–2424. PubMed PMC

Lermontova I, Sandmann M, Demidov D.. 2014. Centromeres and kinetochores of Brassicaceae. Chromosome Res. 22(2):135–152. PubMed

Letunic I, Bork P.. 2019. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47(W1):W256–W259. PubMed PMC

Logsdon GA, Gambogi CW, Liskovykh MA, Barrey EJ, Larionov V, Miga KH, Heun P, Black BE.. 2019. Human artificial chromosomes that bypass centromeric DNA. Cell 178(3):624–639. PubMed PMC

Macas J, Koblížková A, Navrátilová A, Neumann P.. 2009. Hypervariable 3’ UTR region of plant LTR-retrotransposons as a source of novel satellite repeats. Gene 448(2):198–206. PubMed

Macas J, Mészáros T, Nouzová M.. 2002. PlantSat: a specialized database for plant satellite repeats. Bioinformatics 18(1):28–35. PubMed

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(1):427. PubMed PMC

Macas J, Novák P, Pellicer J, Čížková J, Koblížková A, Neumann P, Fuková I, Doležel J, Kelly LJ, Leitch IJ.. 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. PubMed PMC

Maheshwari S, Ishii T, Brown CT, Houben A, Comai L.. 2017. Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence. Genome Res. 27(3):471–478. PubMed PMC

Malik HS. 2009. The centromere-drive hypothesis: a simple basis for centromere complexity. Prog Mol Subcell Biol. 48:33–52. PubMed

Masonbrink RE, Gallagher JP, Jareczek JJ, Renny-Byfield S, Grover CE, Gong L, Wendel JF.. 2014. CenH3 evolution in diploids and polyploids of three angiosperm genera. BMC Plant Biol. 14(1):383. PubMed PMC

McFarlane RJ, Humphrey TC.. 2010. A role for recombination in centromere function. Trends Genet. 26(5):209–213. PubMed

McNulty SM, Sullivan BA.. 2018. Alpha satellite DNA biology: finding function in the recesses of the genome. Chromosome Res. 26(3):115–138. PubMed PMC

Mello B. 2018. Estimating TimeTrees with MEGA and the TimeTree Resource. Mol Biol Evol. 35(9):2334–2342. PubMed

Murrell B, Weaver S, Smith MD, Wertheim JO, Murrell S, Aylward A, Eren K, Pollner T, Martin DP, Smith DM, et al. 2015. Gene-wide identification of episodic selection. Mol Biol Evol. 32(5):1365–1371. PubMed PMC

Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL.. 2012. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 8(7):e1002764. PubMed PMC

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 Genet. 8(6):e1002777. PubMed PMC

Neumann P, Nouzová M, Macas J.. 2001. Molecular and cytogenetic analysis of repetitive DNA in pea (Pisum sativum L.). Génome 44(4):716–728. PubMed

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. Mob DNA. 10:1. PubMed PMC

Neumann P, Pavlíková Z, Koblížková A, Fuková I, Jedličková V, Novák P, Macas J.. 2015. Centromeres off the hook: massive changes in centromere size and structure following duplication of CENH3 gene in Fabeae species. Mol Biol Evol. 32(7):1862–1879. PubMed PMC

Neumann P, Požárková D, Vrána J, Doležel J, Macas J.. 2002. Chromosome sorting and PCR-based physical mapping in pea (Pisum sativum L.). Chromosome Res. 10(1):63–71. PubMed

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. PubMed PMC

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. PubMed

Oliveira LC, Torres GA.. 2018. Plant centromeres: genetics, epigenetics and evolution. Mol Biol Rep. 45(5):1491–1497. PubMed

Park PJ. 2009. ChIP-seq: advantages and challenges of a maturing technology. Nat Rev Genet. 10(10):669–680. PubMed PMC

Perea-Resa C, Blower MD.. 2018. Centromere biology: transcription goes on stage. Mol Cell Biol. 38:e00263–e00318. PubMed PMC

Piras FM, Nergadze SG, Magnani E, Bertoni L, Attolini C, Khoriauli L, Raimondi E, Giulotto E.. 2010. Uncoupling of satellite DNA and centromeric function in the genus Equus. PLoS Genet. 6(2):e1000845. PubMed PMC

Plohl M, Meštrović N, Mravinac B.. 2014. Centromere identity from the DNA point of view. Chromosoma 123(4):313–325. PubMed PMC

Pond SLK, Frost SDW, Muse SV.. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21(5):676–679. PubMed

Reinert G, Chew D, Sun F, Waterman MS.. 2009. Alignment-free sequence comparison (I): statistics and power. J Comput Biol. 16(12):1615–1634. PubMed PMC

Rice P, Longden I, Bleasby A.. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16(6):276–277. PubMed

Schaefer H, Hechenleitner P, Santos-Guerra A, de Sequeira MM, Pennington RT, Kenicer G, Carine MA.. 2012. Systematics, biogeography, and character evolution of the legume tribe Fabeae with special focus on the middle-Atlantic island lineages. BMC Evol Biol. 12(1):250. PubMed PMC

Schneider KL, Xie Z, Wolfgruber TK, Presting GG.. 2016. Inbreeding drives maize centromere evolution. Proc Natl Acad Sci U S A. 113(8):E987–E996. PubMed PMC

Sonnhammer EL, Durbin R.. 1995. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167(1–2):GC1–GC10. PubMed

Talbert P, Kasinathan S, Henikoff S.. 2018. Simple and complex centromeric satellites in Drosophila sibling species. Genetics 208(3):977–990. PubMed PMC

Vondrak T, Ávila Robledillo L, 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(2):484–500. PubMed PMC

Wei K-C, Reddy HM, Rathnam C, Lee J, Lin D, Ji S, Mason JM, Clark AG, Barbash DA.. 2017. A pooled sequencing approach identifies a candidate meiotic driver in Drosophila. Genetics 206(1):451–465. PubMed PMC

Yang X, Zhao H, Zhang T, Zeng Z, Zhang P, Zhu B, Han Y, Braz GT, Casler MD, Schmutz J, et al. 2018. Amplification and adaptation of centromeric repeats in polyploid switchgrass species. New Phytol. 218(4):1645–1657. PubMed

Yu F, Dou Q, Liu R, Wang H.. 2017. A conserved repetitive DNA element located in the centromeres of chromosomes in Medicago genus. Genes Genom. 39(8):903–911.

Zatloukalová P, Hřibová E, Kubaláková M, Suchánková P, Šimková H, Adoración C, Kahl G, Millán T, Doležel J.. 2011. Integration of genetic and physical maps of the chickpea (Cicer arietinum L.) genome using flow-sorted chromosomes. Chromosome Res. 19(6):729–739. PubMed

Zedek F, Bureš P.. 2016. CenH3 evolution reflects meiotic symmetry as predicted by the centromere drive model. Sci Rep. 6:33308. PubMed PMC

Zhang B, Dong Q, Su H, Birchler JA, Han F.. 2014. Histone phosphorylation: its role during cell cycle and centromere identity in plants. Cytogenet Genome Res. 143(1–3):144–149. PubMed

Zhang H, Koblížková A, Wang K, Gong Z, Oliveira L, Torres GA, Wu Y, Zhang W, Novák P, Buell CR, et al. 2014. Boom-bust turnovers of megabase-sized centromeric DNA in Solanum species: rapid evolution of DNA sequences associated with centromeres. Plant Cell 26(4):1436–1447. PubMed PMC

Zhang T, Talbert PB, Zhang W, Wu Y, Yang Z, Henikoff JG, Henikoff S, Jiang J.. 2013. The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres. Proc Natl Acad Sci U S A. 110(50):E4875–E4883. PubMed PMC

Zimin AV, Marçais G, Puiu D, Roberts M, Salzberg SL, Yorke JA.. 2013. The MaSuRCA genome assembler. Bioinformatics 29(21):2669–2677. PubMed PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

A chromosome-scale reference genome of grasspea (Lathyrus sativus)

. 2024 Sep 27 ; 11 (1) : 1035. [epub] 20240927

Satellite DNAs and the evolution of the multiple X1X2Y sex chromosomes in the wolf fish Hoplias malabaricus (Teleostei; Characiformes)

. 2024 Sep 02 ; 14 (1) : 20402. [epub] 20240902

Celine, a long interspersed nuclear element retrotransposon, colonizes in the centromeres of poplar chromosomes

. 2024 Jul 31 ; 195 (4) : 2787-2798.

Evolution of ancient satellite DNAs in extant alligators and caimans (Crocodylia, Reptilia)

. 2024 Feb 27 ; 22 (1) : 47. [epub] 20240227

KNL1 and NDC80 represent new universal markers for the detection of functional centromeres in plants

. 2024 Feb 26 ; 32 (1) : 3. [epub] 20240226

Fast satellite DNA evolution in Nothobranchius annual killifishes

. 2023 Nov 21 ; 31 (4) : 33. [epub] 20231121

The giant diploid faba genome unlocks variation in a global protein crop

. 2023 Mar ; 615 (7953) : 652-659. [epub] 20230308

Assembly of the 81.6 Mb centromere of pea chromosome 6 elucidates the structure and evolution of metapolycentric chromosomes

. 2023 Feb ; 19 (2) : e1010633. [epub] 20230203

Investigating the Origin and Evolution of Polyploid Trifolium medium L. Karyotype by Comparative Cytogenomic Methods

. 2023 Jan 04 ; 12 (2) : . [epub] 20230104

Adding New Pieces to the Puzzle of Karyotype Evolution in Harttia (Siluriformes, Loricariidae): Investigation of Amazonian Species

. 2021 Sep 16 ; 10 (9) : . [epub] 20210916

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace