Advertisement

Tropical Plant Biology

, Volume 9, Issue 3, pp 117–135 | Cite as

Genome-Wide Comparative Analysis of Microsatellites in Pineapple

  • Jingping Fang
  • Chenyong Miao
  • Rukai Chen
  • Ray MingEmail author
Article

Abstract

Pineapple (Ananas comosus (L.) Merrill) is the second most important tropical fruit in term of international trade. The availability of whole genomic sequences and expressed sequence tags (ESTs) offers an opportunity to identify and characterize microsatellite or simple sequence repeat (SSR) markers in pineapple. A total of 278,245 SSRs and 41,962 SSRs with an overall density of 728.57 SSRs/Mb and 619.37 SSRs/Mb were mined from genomic and ESTs sequences, respectively. 5′-untranslated regions (5′-UTRs) had the greatest amount of SSRs, 3.6–5.2 fold higher SSR density than other regions. For repeat length, 12 bp was the predominant repeat length in both assembled genome and ESTs. Class I SSRs were underrepresented compared with class II SSRs. For motif length, dinucleotide repeats were the most abundant in genomic sequences, whereas trinucleotides were the most common motif in ESTs. Tri- and hexanucleotides of total SSRs were more prevalent in ESTs than in the whole genome. The SSR frequency decreased dramatically as repeat times increased. AT was the most frequent single motif across the entire genome while AG was the most abundant motif in ESTs. Across six examined plant species, the pineapple genome displayed the highest density, substantially more than the second-place cucumber. Annotation and expression analyses were also conducted for genes containing SSRs. This thorough analysis of SSR markers in pineapple provided valuable information on the frequency and distribution of SSRs in the pineapple genome. This genomic resource will expedite genomic research and pineapple improvement.

Keywords

Ananas comosus (L.) Merrill Expressed sequence tag (EST) Expression patterns Motif Repeat Simple sequence repeats (SSRs) 

Abbreviations

AFLP

amplified fragment length polymorphism

bp

Base pair

CAM

Crassulacean Acid Metabolism

CDS

Coding sequences

EST

Expressed sequence tag

FPKM

Number of fragments per kilobase of exon per million fragments mapped

GO

Gene Ontology

KEGG

Kyoto Encyclopedia of Genes and Genomes

kb

Kilo base pairs

MAS

Marker-assisted selection

Mb

Mega base pairs

RAPD

Randomly amplified polymorphic DNA

RFLP

Restriction fragment length polymorphism

SSR

Simple sequence repeat

STR

Short tandem repeat

UTR

Untranslated regions

Notes

Acknowledgments

This work was supported startup fund from Fujian Agriculture and Forestry University to R.M.

Supplementary material

12042_2016_9163_MOESM1_ESM.docx (85 kb)
ESM 1 (DOCX 85 kb)

References

  1. Aradhya MK, Zee F, Manshardt RM (1994) Isozyme variation in cultivated and wild pineapple. Euphytica 79:87–99CrossRefGoogle Scholar
  2. Arumuganathan K, Earle E (1991) Estimation of nuclear DNA content of plants by flow cytometry. Plant Mol Biol Report 9:229–241CrossRefGoogle Scholar
  3. Ayres N, McClung A, Larkin P, Bligh H, Jones C, Park W (1997) Microsatellites and a single-nucleotide polymorphism differentiate apparentamylose classes in an extended pedigree of US rice germ plasm. Theor Appl Genet 94:773–781CrossRefGoogle Scholar
  4. Biet E, Sun J-S, Dutreix M (1999) Conserved sequence preference in DNA binding among recombination proteins: an effect of ssDNA secondary structure. Nucleic Acids Res 27:596–600CrossRefPubMedPubMedCentralGoogle Scholar
  5. Biswas MK, Xu Q, Mayer C, Deng X (2014) Genome wide characterization of short tandem repeat markers in sweet Orange (Citrus sinensis). PLoS One 9. doi: 10.1371/journal.pone.0104182
  6. Carlier JD, Sousa NH, Santo TE, d’Eeckenbrugge GC, Leitão JM (2012) A genetic map of pineapple (Ananas comosus (L.) merr.) including SCAR, CAPS, SSR and EST-SSR markers. Mol Breed 29:245–260CrossRefGoogle Scholar
  7. Castillo A, Budak H, Varshney RK, Dorado G, Graner A, Hernandez P (2008) Transferability and polymorphism of barley EST-SSR markers used for phylogenetic analysis in Hordeum chilense. BMC Plant Biol 8:97CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cavagnaro PF et al. (2010) Genome-wide characterization of simple sequence repeats in cucumber (Cucumis sativus L.). BMC Genomics 11:569CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chen H et al. (2015) A high-density SSR genetic map constructed from a F2 population of Gossypium hirsutum and Gossypium darwinii. Gene 574:273–286CrossRefPubMedGoogle Scholar
  10. de Sousa N, Carlier J, Santo T, Leitão J (2013) An integrated genetic map of pineapple (Ananas comosus (L.) merr.). Sci Hortic-Amsterdam 157:113–118CrossRefGoogle Scholar
  11. DeWald M, Moore G, Sherman W (1992) Isozymes in Ananas (pineapple): genetics and usefulness in taxonomy. J Am Soc Hortic Sci 117:491–496Google Scholar
  12. Dresselhaus T, Cordts S, Heuer S, Sauter M, Lörz H, Kranz E (1999) Novel ribosomal genes from maize are differentially expressed in the zygotic and somatic cell cycles. Mol Gen Genet 261:416–427CrossRefPubMedGoogle Scholar
  13. Duval M, Noyer J, Perrier X, d’Eeckenbrugge C, Hamon P (2001) Molecular diversity in pineapple assessed by RFLP markers. Theor Appl Genet 102:83–90CrossRefGoogle Scholar
  14. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445CrossRefPubMedGoogle Scholar
  15. Feng S et al. (2013) Development of pineapple microsatellite markers and germplasm genetic diversity analysis. Biomed Res Int 2013:11Google Scholar
  16. Fraser L, Harvey C, Crowhurst R, De Silva H (2004) EST-derived microsatellites from Actinidia species and their potential for mapping. Theor Appl Genet 108:1010–1016CrossRefPubMedGoogle Scholar
  17. Gailing O, Bodénès C, Finkeldey R, Kremer A, Plomion C (2013) Genetic mapping of EST-derived simple sequence repeats (EST-SSRs) to identify QTL for leaf morphological characters in a Quercus robur full-sib family. Tree Genet Genomes 9:1361–1367CrossRefGoogle Scholar
  18. Garza JC, Slatkin M, Freimer NB (1995) Microsatellite allele frequencies in humans and chimpanzees, with implications for constraints on allele size. Mol Biol Evol 12:594–603PubMedGoogle Scholar
  19. Grabherr MG et al. (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29:644–652CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gur-Arie R, Cohen CJ, Eitan Y, Shelef L, Hallerman EM, Kashi Y (2000) Simple sequence repeats in Escherichia coli: abundance, distribution, composition, and polymorphism. Genome Res 10:62–71PubMedPubMedCentralGoogle Scholar
  21. Harding RM, Boyce A, Clegg J (1992) The evolution of tandemly repetitive DNA: recombination rules. Genetics 132:847–859PubMedPubMedCentralGoogle Scholar
  22. Huo N et al. (2008) The nuclear genome of Brachypodium distachyon: analysis of BAC end sequences. Funct Integr Genomics 8:135–147CrossRefPubMedGoogle Scholar
  23. Innan H, Terauchi R, Miyashita NT (1997) Microsatellite polymorphism in natural populations of the wild plant Arabidopsis thaliana. Genetics 146:1441–1452PubMedPubMedCentralGoogle Scholar
  24. Jaillon O et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467CrossRefPubMedGoogle Scholar
  25. Jena SN et al. (2012) Development and characterization of genomic and expressed SSRs for levant cotton (Gossypium herbaceum L.). Theor Appl Genet 124:565–576CrossRefPubMedGoogle Scholar
  26. Kalia RK, Rai MK, Kalia S, Singh R, Dhawan A (2011) Microsatellite markers: an overview of the recent progress in plants. Euphytica 177:309–334CrossRefGoogle Scholar
  27. Kantety RV, La Rota M, Matthews DE, Sorrells ME (2002) Data mining for simple sequence repeats in expressed sequence tags from barley, maize, rice, sorghum and wheat. Plant Mol Biol 48:501–510CrossRefPubMedGoogle Scholar
  28. Karaoglu H, Lee CMY, Meyer W (2005) Survey of simple sequence repeats in completed fungal genomes. Mol Biol Evol 22:639–649CrossRefPubMedGoogle Scholar
  29. Kato CY, Nagai C, Moore PH, Zee F, Kim MS, Steiger DL, Ming R (2005) Intra-specific DNA polymorphism in pineapple (Ananas comosus (L.) merr.) assessed by AFLP markers. Genet Resour Crop Ev 51:815–825CrossRefGoogle Scholar
  30. Katti MV, Ranjekar PK, Gupta VS (2001) Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol 18:1161–1167CrossRefPubMedGoogle Scholar
  31. Kinsuat M, Kumar S (2007) Polymorphic microsatellite and cryptic simple repeat sequence markers in pineapples (Ananas comosus var. comosus). Mol Ecol Notes 7:1032–1035CrossRefGoogle Scholar
  32. Labbé J, Murat C, Morin E, Le Tacon F, Martin F (2011) Survey and analysis of simple sequence repeats in the Laccaria bicolor genome, with development of microsatellite markers. Curr Genet 57:75–88CrossRefPubMedGoogle Scholar
  33. Lawson MJ, Zhang L (2006) Distinct patterns of SSR distribution in the Arabidopsis thaliana and rice genomes. Genome Biol 7:R14CrossRefPubMedPubMedCentralGoogle Scholar
  34. Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221PubMedGoogle Scholar
  35. Li YC, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–2465CrossRefPubMedGoogle Scholar
  36. Li B, Xia Q, Lu C, Zhou Z, Xiang Z (2004a) Analysis on frequency and density of microsatellites in coding sequences of several eukaryotic genomes. Genomics Proteomics Bioinform 2:24–31Google Scholar
  37. Li Y-C, Korol AB, Fahima T, Nevo E (2004b) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21:991–1007CrossRefPubMedGoogle Scholar
  38. Li W, Feng Y, Sun H, Deng Y, Yu H, Chen H (2014) Analysis of simple sequence repeats in the Gaeumannomyces graminis var. tritici genome and the development of microsatellite markers. Curr Genet 60:237–245CrossRefPubMedGoogle Scholar
  39. Liu S-R, Li W-Y, Long D, Hu C-G, Zhang J-Z (2013) Development and characterization of genomic and expressed ssrs in citrus by genome-wide analysis. PLoS One:8. doi: 10.1371/journal.pone.0075149
  40. Luo J et al. (2012) Microsatellite mutation rate during allohexaploidization of newly resynthesized wheat. Int J Mol Sci 13:12533–12543CrossRefPubMedPubMedCentralGoogle Scholar
  41. Luo H et al. (2015) Genome-Wide Analysis of Simple Sequence Repeats and Efficient Development of Polymorphic SSR Markers Based on Whole Genome Re-Sequencing of Multiple Isolates of the Wheat Stripe Rust Fungus. PLoS One:10. doi: 10.1371/journal.pone.0130362
  42. Mian MAR, Saha MC, Hopkins AA, Wang Z-Y (2005) Use of tall fescue EST-SSR markers in phylogenetic analysis of cool-season forage grasses. Genome 48:637–647CrossRefPubMedGoogle Scholar
  43. Ming R et al. (2015) The pineapple genome and the evolution of CAM photosynthesis. Nat Genet 47:1435–1442CrossRefPubMedPubMedCentralGoogle Scholar
  44. Molnar SJ, Rai S, Charette M, Cober ER (2003) Simple sequence repeat (SSR) markers linked to E1, E3, E4, and E7 maturity genes in soybean. Genome 46:1024–1036CrossRefPubMedGoogle Scholar
  45. Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet 30:194–200CrossRefPubMedGoogle Scholar
  46. Mrázek J, Guo X, Shah A (2007) Simple sequence repeats in prokaryotic genomes. P Natl Acad Sci 104:8472–8477CrossRefGoogle Scholar
  47. Mun J-H et al. (2006) Distribution of microsatellites in the genome of Medicago truncatula: a resource of genetic markers that integrate genetic and physical maps. Genetics 172:2541–2555CrossRefPubMedPubMedCentralGoogle Scholar
  48. Murat C et al. (2011) Distribution and localization of microsatellites in the perigord black truffle genome and identification of new molecular markers. Fungal Genet Biol 48:592–601CrossRefPubMedGoogle Scholar
  49. Ong W, Voo CLY, Kumar SV (2012) Development of ESTs and data mining of pineapple EST-SSRs. Mol Biol Rep 39:5889–5896CrossRefPubMedGoogle Scholar
  50. Paz EY et al. (2012) Genetic diversity of Cuban pineapple germplasm assessed by AFLP Markers. Crop Breed Appl Biot 12:104–110CrossRefGoogle Scholar
  51. Poncet V, Rondeau M, Tranchant C, Cayrel A, Hamon S, de Kochko A, Hamon P (2006) SSR mining in coffee tree EST databases: potential use of EST–SSRs as markers for the Coffea genus. Mol Gen Genomics 276:436–449CrossRefGoogle Scholar
  52. Powell W, Machray GC, Provan J (1996) Polymorphism revealed by simple sequence repeats. Trends Plant Sci 1:215–222CrossRefGoogle Scholar
  53. Project IRGS (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  54. Rodríguez D, Grajal-Martín M, Isidrón M, Petit S, Hormaza J (2013) Polymorphic microsatellite markers in pineapple (Ananas comosus (L.) Merrill). Sci Hortic-Amsterdam 156:127–130CrossRefGoogle Scholar
  55. Scaglione D, Acquadro A, Portis E, Taylor CA, Lanteri S, Knapp SJ (2009) Ontology and diversity of transcript-associated microsatellites mined from a globe artichoke EST database. BMC Genomics 10:454CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sharma AK, Ghosh I (1971) Cytotaxonomy of the family bromeliaceae. Cytologia 36:237–247CrossRefGoogle Scholar
  57. Sharma R, Gupta P, Sharma V, Sood A, Mohapatra T, Ahuja PS (2008) Evaluation of rice and sugarcane SSR markers for phylogenetic and genetic diversity analyses in bamboo. Genome 51:91–103CrossRefPubMedGoogle Scholar
  58. Shoda M et al. (2012) DNA profiling of pineapple cultivars in Japan discriminated by SSR markers. Breed Sci 62:352CrossRefPubMedPubMedCentralGoogle Scholar
  59. Sonah H et al. (2011) Genome-wide distribution and organization of microsatellites in plants: an insight into marker development in Brachypodium. PLoS One:6. doi: 10.1371/journal.pone.0021298
  60. Sripaoraya S, Blackhall N, Marchant R, Power J, Lowe K, Davey M (2001) Relationships in pineapple by random amplified polymorphic DNA (RAPD) analysis. Plant Breed 120:265–267CrossRefGoogle Scholar
  61. Steele K, Price A, Shashidhar H, Witcombe J (2006) Marker-assisted selection to introgress rice QTLs controlling root traits into an Indian upland rice variety. Theor Appl Genet 112:208–221CrossRefPubMedGoogle Scholar
  62. Tachida H, Iizuka M (1992) Persistence of repeated sequences that evolve by replication slippage. Genetics 131:471–478PubMedPubMedCentralGoogle Scholar
  63. Tangphatsornruang S et al. (2009) Characterization of microsatellites and gene contents from genome shotgun sequences of mungbean (Vigna radiata (L.) Wilczek). BMC Plant Bio 9:137CrossRefGoogle Scholar
  64. Tautz D (1989) Hypervariabflity of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Res 17:6463–6471CrossRefPubMedPubMedCentralGoogle Scholar
  65. Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452CrossRefPubMedPubMedCentralGoogle Scholar
  66. Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422PubMedGoogle Scholar
  67. Tóth G, Gáspári Z, Jurka J (2000) Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res 10:967–981CrossRefPubMedPubMedCentralGoogle Scholar
  68. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-seq. Bioinformatics 25:1105–1111CrossRefPubMedPubMedCentralGoogle Scholar
  69. Treco D, Arnheim N (1986) The evolutionarily conserved repetitive sequence d(TG. AC)n promotes reciprocal exchange and generates unusual recombinant tetrads during yeast meiosis. Mol Cell Biol 6:3934–3947CrossRefPubMedPubMedCentralGoogle Scholar
  70. Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23:48–55CrossRefPubMedGoogle Scholar
  71. Vásquez A, López C (2014) In silico genome comparison and distribution analysis of simple sequences repeats in cassava. Int J Genomics 2014Google Scholar
  72. Wahls WP, Wallace LJ, Moore PD (1990) Hypervariable minisatellite DNA is a hotspot for homologous recombination in human cells. Cell 60:95–103CrossRefPubMedGoogle Scholar
  73. Wang J et al. (2008) Genome-wide comparative analyses of microsatellites in papaya. Trop Plant Biol 1:278–292CrossRefGoogle Scholar
  74. Wöhrmann T, Weising K (2011) In silico mining for simple sequence repeat loci in a pineapple expressed sequence tag database and cross-species amplification of EST-SSR markers across bromeliaceae. Theor Appl Genet 123:635–647CrossRefPubMedGoogle Scholar
  75. Yu Y, Yuan D, Liang S, Li X, Wang X, Lin Z, Zhang X (2011) Genome structure of cotton revealed by a genome-wide SSR genetic map constructed from a BC1 population between Gossypium hirsutum and G. barbadense. BMC Genomics 12:15CrossRefPubMedPubMedCentralGoogle Scholar
  76. Zdobnov EM, Apweiler R (2001) InterProScan – An integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848CrossRefPubMedGoogle Scholar
  77. Zhang L et al. (2004) Preference of simple sequence repeats in coding and non-coding regions of Arabidopsis thaliana. Bioinformatics 20:1081–1086CrossRefPubMedGoogle Scholar
  78. Zhang L et al. (2006) Conservation of noncoding microsatellites in plants: implication for gene regulation. BMC Genomics 7:323CrossRefPubMedPubMedCentralGoogle Scholar
  79. Zhao Y, Williams R, Prakash C, He G (2012) Identification and characterization of gene-based SSR markers in date palm (Phoenix dactylifera L.). BMC Plant Biol 12:237CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Jingping Fang
    • 1
    • 2
  • Chenyong Miao
    • 2
  • Rukai Chen
    • 1
  • Ray Ming
    • 2
    • 3
    Email author
  1. 1.Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of AgricultureFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.FAFU and UIUC-SIB Joint Center for Genomics and BiotechnologyFujian Agriculture and Forestry UniversityFuzhouChina
  3. 3.Department of Plant BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations