Abstract
Simple sequence repeats (SSRs), also known as microsatellites, are one of the prominent DNA sequences shaping the repeated fraction of eukaryotic genomes. In spite of their profuse use as molecular markers for a variety of genetic and evolutionary studies, their genomic location, distribution, and function are not yet well understood. Here we report the first thorough joint analysis of microsatellite motifs at both genomic and chromosomal levels in animal species, by a combination of 454 sequencing and fluorescent in situ hybridization (FISH) techniques performed on two grasshopper species. The in silico analysis of the 454 reads suggested that microsatellite expansion is not driving size increase of these genomes, as SSR abundance was higher in the species showing the smallest genome. However, the two species showed the same uneven and nonrandom location of SSRs, with clear predominance of dinucleotide motifs and association with several types of repetitive elements, mostly histone gene spacers, ribosomal DNA intergenic spacers (IGS), and transposable elements (TEs). The FISH analysis showed a dispersed chromosome distribution of microsatellite motifs in euchromatic regions, in coincidence with chromosome location patterns previously observed for many mobile elements in these species. However, some SSR motifs were clustered, especially those located in the histone gene cluster.
Similar content being viewed by others
References
Agustinos AA, Asimakopoulou AK, Papadopoulos NT, Bourtzis K (2011) Cross-amplified microsatellites in the European cherry fly Rhagoletis cerasi: medium polymorphic-highly informative markers. Bull Entomol Res 101:45–52. doi:10.1017/S0007485310000167
Ananiev E, Chamberlin MA, Klaiber J, Svitashev S (2005) Microsatellite megatracts in the maize (Zea mays L.) genome. Genome 48:1061–1069. doi:10.1139/g05-061
Areshchenkova T, Ganal MW (1999) Long tomato microsatellites are predominantly associated with centromeric regions. Genome 42:536–544
Bakkali M, Camacho JPM (2004) The B chromosome polymorphism of the grasshopper Eyprepocnemis plorans in North Africa: III. Mutation rate of B chromosomes. Heredity 92:428–433. doi:10.1038/sj.hdy.6800437
Baltimore D (2001) Our genome unveiled. Nature 409:814–816. doi:10.1038/35057267
Bao Z, Eddy SR (2002) Automated de novo identification of repeats sequence families in sequenced genomes. Genome Res 12:1269–1276. doi:10.1101/gr.88502
Basset P, Yannic G, Yang F, O’Brien PCM, Graphodatsky AS, Ferguson-Smith MA, Balmus G, Volobouev VT, Hausser J (2006) Chromosome localization of microsatellite markers in the shrews of the Sorex araneus group. Chromosom Res 14:253–262. doi:10.1007/s10577-006-1041-x
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580. doi:10.1093/nar/27.2.573
Blondin L, Badisco L, Pagès C, Foucart A, Risterucci AM, Bazelet CS, Vanen Broeck J, Song H, Ould Ely S, Chapuis MP (2013) Characterization and comparison of microsatellite markers derived from genomic and expressed libraries for the desert locust. J App Entomol 137:673–683. doi:10.1111/jen.12052
Cabrero J, López-León MD, Bakkali M, Camacho JPM (1999) Common origin of B chromosomes variants in the grasshopper Eyprepocnemis plorans. Heredity 83:435–439. doi:10.1038/sj.hdy.6885960
Cabrero J, López-León MD, Teruel M, Camacho JPM (2009) Chromosome mapping of H3 and H4 histone genes clusters in 35 species of acridid grasshoppers. Chromosom Res 17:397–404. doi:10.1007/s10577-009-9030-5
Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier, London, pp 223–286
Camacho JPM, Cabrero J, Viseras E, López-León MD, Navas-Castillo J, Alché JD (1991) G-banding of two species of grasshoppers and its relationship to C, N, and fluorescence banding techniques. Genomes 34:638–643. doi:10.1139/g91-097
Carmona A, Friero E, de Bustos A, Jouve N, Cuadrado A (2013) Cytogenetics diversity of SSR motifs within in between Hordeum species carrying the H genome: H. vulgare L. and H. bulbosum L. Theor Appl Genet 126:949–961. doi:10.1007/s00122-012-2028-y
Castoe TA, Streicher W, Meik JM et al (2012) Thousands of microsatellite loci from the venomous coralsnake Micrurus fulvius and variability of selected loci across populations and related species. Mol Ecol Resour 12:1105–1113. doi:10.1111/1755-0998.12000
Coates BS, Kroemer JA, Summerford DV, Hellmich RL (2011) A novel class of miniature inverted repeat transposable elements (MITEs) that contain hitchhiking (GTCY)n microsatellites. Insect Mol Biol 20:15–27. doi:10.1111/1755-0998.12000
Cuadrado A, Jouve N (2007a) The nonrandom distribution of long cluster of all possible classes of trinucleotide repeats in barley chromosomes. Chromosom Res 15:711–720. doi:10.1007/s10577-007-1156-8
Cuadrado A, Jouve N (2007b) Similarities in the chromosomal distribution of AG and AC repeats within and between Drosophila, human and barley chromosomes. Cytogenet Genome Res 119:91–99. doi:10.1159/000109624
Cuadrado A, Jouve N (2010) Chromosome detection of simple sequence repeats (SSRs) using no denaturing FISH (ND-FISH). Chromosoma 119:495–503. doi:10.1007/s00412-010-0273-x
Cuadrado A, Jouve N (2011) Novel simple sequence repeats (SSRs) detected by ND-FISH in heterochromatin of Drosophila melanogaster. BMC Genomics 12:205. doi:10.1186/1471-2164-12-205
Cuadrado A, Schwarzacher T, Jouve N (2000) Identification of different chromatin classes in wheat using in situ hybridization with simple sequence repeat oligonucleotides. Theor Appl Genet 101:711–717. doi:10.1007/s001220051535
Dover GA (1993) Evolution of genetics redundancy for advanced player. Curr Opin Genet Dev 3:902–910. doi:10.1016/0959-437X(93)90012-E
Goldstein DB, Schlötterer C (1999) Microsatellites: evolution and applications. Oxford University Press, Oxford
Guo WJ, Ling J, Li P (2009) Consensus features of microsatellite distribution: microsatellite contents are universally correlated with recombination rates and are preferentially depressed by centromeres in multicellular eukaryotic genomes. Genomics 93:323–331. doi:10.1016/j.ygeno.2008.12.009
Haasl RJ, Payseur BA (2014) Remarkable selective constraints on exonic dinucleotide repeats. Evolution 68:2737–2744. doi:10.1111/evo.12460
Hancock JM (1996) Simple sequences and the expanding genome. Bioessays 18:421–425. doi:10.1002/bies.950180512
Hancock JM (2002) Genome size and the accumulation of simple sequence repeats: implications of new data from genome sequencing projects. Genetica 115:93–103. doi:10.1023/A:1016028332006
Hatanaka T, Henrique-Silva F, Galleti PM Jr (2002) A polymorphic telomeric-like sequence microsatellite in the Neotropical fish Prochilodus. Cytogenet Genome Res 98:308–310. doi:10.1159/000071054
Hunter ME, Hart KM (2013) Rapid microsatellite marker development using next generation pyrosequencing to inform invasive Burmese phyton—Phyton molurus bivittatus—management. Int J Mol Sci 14:4793–4804. doi:10.3390/ijms14034793
Insuan S, Deowanish S, Klinbunga S, Sittipraneed S, Sylvester HA, Wongsiri S (2007) Genetic differentiation of the giant honey bee (Apis dorsata) in Thailand analyzed by mitochondrial genes and microsatellites. Bioch Genet 45:345–361. doi:10.1007/s10528-007-9079-9
Iquebal MA, Sarika AV, Verma N, Rai A, Kumar D (2013) First whole genome based microsatellite DNA marker database of tomato for mapping and variety identification. BMC Plant Biol 13:197. doi:10.1186/1471-2229-13-197
Jamilena M, Garrido-Ramos M, Ruiz-Rejón C, Rejón MR (1994) Molecular relationship between A and B chromosomes of Crepis capillaries. Heredity 73:527–531. doi:10.1038/hdy.1994.151
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467. doi:10.1159/000084979
Kejnovský E, Michalovova M, Steflova P, Kejnovska I, Manzano S, Hobza R, Kubat Z, Kovarik J, Jamilena M, Vyskot B (2013) Expansion of microsatellites on evolutionary young Y chromosome. PLoS One 8(1):e45519. doi:10.1371/journal.pone.0045519
Khashnobish A, Hamann A, Osiewacz HD (1999) Modulation of gene expression by (CA)n microsatellites in the filamentous ascomycete Podospora anserine. Appl Microbiol Biot 52:191–195. doi:10.1007/s002530051508
Kubat Z, Hobza R, Vyskot B, Kejnovský E (2008) Microsatellite accumulation on the Y chromosome of Silene latifolia. Genome 51:350–356. doi:10.1139/G08-024
Langdon T, Seago C, Jones RN, Ougham H, Thomas H, Forster JW, Jenkins G (2000) De novo evolution of satellite DNA on the rye B chromosome. Genetics 154:869–884
Li YC, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–3465. doi:10.1046/j.1365-294X.2002.01643.x
Li S, Ying T, Wang M, Tuskan GA (2011) Characterization of microsatellites in coding regions of the Populus genome. Mol Breeding 27:59–66. doi:10.1007/s11032-010-9413-5
Lim S, Notley-McRobb L, Lim M, Carter DA (2004) A comparison of the nature and abundance of microsatellite in 12 fungal genomes. Fungal Genet Biol 41:1025–1036. doi:10.1016/j.fgb.2004.08.004
Lohe AR, Hilliker AJ, Roberts PA (1993) Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics 134:1149–1174
López-León MD, Cabrero J, Pardo MC, Viseras E, Camacho JPM, Santos JL (1993) Generating high variability of B chromosomes in Eyprepocnemis plorans (grasshopper). Heredity 71:352–362. doi:10.1038/hdy.1993.149
López-León MD, Neves N, Schwarzacher T, Heslop-Harrison JS, Hewitt GM, Camacho JPM (1994) Possible origin of B chromosome deduced from its DNA composition using double FISH technique. Chromosom Res 2:87–92. doi:10.1007/BF01553487
Malausa T, Gilles A, Méglecz E, Blanquart H, Duthoy S (2011) High-throughput microsatellite isolation through 454 GS-FLX Titanium pyrosequencing of enriched DNA libraries. Mol Ecol Resour 11:638–644. doi:10.1111/j.1755-0998.2011.02992.x
Manrique-Poyato MI, López-León MD, Gómez R, Perfectti F, Camacho JPM (2013) Population genetic structure of the grasshopper Eyprepocnemis plorans in the south and east of the Iberian Peninsula. PLoS One 8(3):e59041. doi:10.1371/journal.pone.0059041
Martin JF, Pech N, Meglécz E, Ferreira S, Costedoat C, Dubut V, Malusa T, Guilles A (2010) Representativeness of microsatellites distribution in genomes as revealed by 454 GS-FLX Titanium pyrosequencing. BMC Genomics 11:560–572. doi:10.1186/1471-2164-11-560
McMurray CT (1995) Mechanisms of DNA expansion. Chromosoma 104:2–13
Meglécz E, Nève G, Biffin ED, Gardner MG (2012) Breakdown of phylogenetic signal: a survey of microsatellite densities in 454 shotgun sequences from 154 non model eukaryotes species. PLoS One 7(7):e40861. doi:10.1371/journal.pone.0040861
Milani D, Cabral-de-Mello DC (2014) Microsatellite organization in the grasshopper Abracris flavolineata (Orthoptera: Acrididae) revealed by FISH mapping: remarkable spreading in the A and B chromosomes. PLoS One 9(5):e97956. doi:10.1371/journal.pone.0097956
Montiel EE, Cabrero J, Camacho JPM, López-León MD (2012) Gypsy, RTE and Mariner transposable elements populate Eyprepocnemis plorans genome. Genetica 140:365–374. doi:10.1007/s10709-012-9686-1
Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet 30:194–200. doi:10.1038/ng822
Muñoz-Pajares AJ, Martínez Rodriguez L, Teruel M, Cabrero J, Camacho JPM, Perfectti F (2011) A single, recent origin of the accessory B chromosome of the grasshopper Eyprepocnemis plorans. Genetics 187:853–863. doi:10.1534/genetics.110.122713
Nanda I, Zischler H, Epplen C, Guttenbach M, Schmid M (1991) Chromosome organization of simple repeated DNA sequences used for DNA fingerprinting. Electrophoresis 12:193–203. doi:10.1002/elps.1150120216
Novak 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. doi:10.1093/bioinformatics/btt054
Pannebakker BA, Niehuis O, Hedley A, Gadau J, Shuker DM (2010) The distribution of microsatellites in the Nasonia parasitoid wasp genome. Insect Mol Biol 19:91–98. doi:10.1111/j.1365-2583.2009.00915.x
Pardue ML, Lowenhaupt K, Rich A, Nordheiml A (1987) (dC-dA)n (d(G-dT)n sequences have evolutionary conserved chromosomal locations in Drosophila with implications for roles in chromosome structure and function. EMBO J 6:1781–1789
Poltronieri J, Marquioni V, Bertollo LAC, Kejnovsky E, Molina WF, Liehr T, Cioffi MB (2013) Comparative chromosomal mapping of microsatellites in Leporinus species (Characiformes, Anostomidae): unequal accumulation on the W chromosomes. Cytogenet Genome Res 142:40–45. doi:10.1159/000355908
Powell W, Machray GC, Provan J (1996) Polymorphism revealed by simple sequence repeats. Trends Plant Sci 1:215–222. doi:10.1016/1360-1385(96)86898-1
Primmer CR, Raudsepp T, Chowdhary BP, Moller AP, Ellegren H (1997) Low frequency of microsatellites in the avian genome. Genome Res 7:471–482. doi:10.1101/gr.7.5.471
Ross CL, Dyer KA, Erez T, Miller SJ, Jaenike J, Markow TA (2003) Rapid divergence of microsatellite abundance among species of Drosophila. Mol Biol Evol 20(7):1143–1157. doi:10.1093/molbev/msg137
Ruiz-Ruano FJ, Ruiz-Estévez M, Rodríguez-Pérez J, López-Pino JL, Cabrero J, Camacho JPM (2011) DNA amount of X and B chromosomes in the grasshoppers Eyprepocnemis plorans and Locusta migratoria. Cytogenet Genome Res 134:120–126. doi:10.1159/000324690
Santos J, Serra L, Solé E, Pascual M (2010) FISH mapping of microsatellite loci from Drosophila subobscura and its comparison to related species. Chromosom Res 18:213–216. doi:10.1007/s10577-010-9112-4
Sawaya S, Bagshaw A, Buschiazzo E, Kumar P, Chowdhury S, Black MA, Gemmel N (2013) Microsatellite tandem repeats are abundant in human promoters and are associated with regulatory elements. PLoS One 8(2):54710. doi:10.1371/journal.pone.0054710
Schlötterer C, Pemberton J (1998) The use of microsatellites for genetic analysis of natural populations—a critical review. In: DeSalle R, Schierwater B (eds) Molecular approaches to ecology and evolution. Birkhaäuser, Berlin, pp 71–86
Schoebel CN, Brodbeck S, Buehler D et al (2013) Lessons learned from microsatellites development for nonmodel organisms using 454 pyrosequencing. J Evol Biol 26:600–611. doi:10.1111/jeb.12077
Sharma PC, Grover A, Kahl G (2007) Mining of microsatellites in eukaryotic genomes. Trends in Biotech 25:490–498. doi:10.1016/j.tibtech.2007.07.013
Shi J, Huang S, Zhan Z, Yu J, Wang X, Hua W, Liu S, Liu G, Wang H (2014) Genome-wide microsatellite characterization and marker development in the sequenced Brassica crop species. DNA Res 21:53–68. doi:10.1093/dnares/dst040
Soltis DE, Gitzendanner M, Stull G et al. (2013) The potential of genomics in plant systematics. Taxon 62: 886–898. doi: http://dx.doi.org/10.12705/625.13
Tautz D, Renz C (1984) Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic Acids Res 12(4):127–4138. doi:10.1093/nar/12.10.4127
Teruel M, Cabrero J, Perfectti F, Camacho JPM (2010) B ancestry revealed by histone genes in the migratory locust. Chromosoma 119:217–225. doi:10.1007/s00412-009-0251-3
Tóth G, Gaspari Z, Jurka J (2000) Microsatellites in different eukaryotic genomes survey and analysis. Genome Res 10:967–981. doi:10.1101/gr.10.7.967
Ustinova J, Achmann R, Crèmer S, Mayer F (2006) Long repeats in a huge genome: microsatellites loci in the grasshopper Chorthippus biguttulus. LJ Mol Evol 62:158–167. doi:10.1007/s00239-005-0022-6
Wang X, Fang X, Yang P et al (2014) The locust provides insight into swarm formation and long-distance flight. Nat Commun 5:2957. doi:10.1038/ncomms3957
Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellites isolation: a review. Mol Ecol 11:1–16. doi:10.1046/j.0962-1083.2001.01418.x
Zhang DX, Yan LN, Ji YJ, Kang L, Hewitt GM, Huang ZS (2003) Isolation, characterization and cross-species amplification of eight microsatellite DNA loci in the migratory locust (Locusta migratoria). Mol Ecol Notes 3:483–486. doi:10.1046/j.1471-8286.2003.00485.x
Acknowledgments
This study was supported by grants from the Spanish Ministerio de Ciencia y Tecnología (CGL2009-11917) and Plan Andaluz de Investigacion (CVI-6649) and was partially performed by FEDER funds. E.E. Montiel was supported by a Junta de Andalucía fellowship.
Integrity of research
All experiments comply with the current Spanish laws.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ruiz-Ruano, F.J., Cuadrado, Á., Montiel, E.E. et al. Next generation sequencing and FISH reveal uneven and nonrandom microsatellite distribution in two grasshopper genomes. Chromosoma 124, 221–234 (2015). https://doi.org/10.1007/s00412-014-0492-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-014-0492-7