Skip to main content

Advertisement

Log in

Location of low copy genes in chromosomes of Brachiaria spp.

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Repetitive DNA sequences have been widely used in cytogenetic analyses. The use of gene sequences with a low-copy-number, however, is little explored especially in plants. To date, the karyotype details in Brachiaria spp. are limited to the location of rDNA sites. The challenge lies in developing new probes based on incomplete sequencing data for the genus or complete sequencing of related species, since there are no model species with a sequenced genome in Brachiaria spp. The present study aimed at the physical location of conserved genes in chromosomes of Brachiaria ruziziensis, Brachiaria brizantha, and Brachiaria decumbens using RNAseq data, as well as sequences of Setaria italica and Sorghum bicolor through the fluorescent in situ hybridization technique. Five out of approximately 90 selected sequences generated clusters in the chromosomes of the species of Brachiaria studied. We identified genes in synteny with 5S and 45S rDNA sites, which contributed to the identification of chromosome pairs carrying these genes. In some cases, the species of Brachiaria evaluated had syntenic segments conserved across the chromosomes. The use of genomic sequencing data is essential for the enhancement of cytogenetic analyses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

(Adapted from Nani et al. [20]). (Color figure online)

Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Wang CJ, Harper L, Cande WZ (2006) High-resolution single-copy gene fluorescence in situ hybridization and its use in the construction of a cytogenetic map of maize chromosome 9. Plant Cell 18:529–544. https://doi.org/10.1105/tpc.105.037838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Huang PL, Hahlbrock K, Somssich IE (1988) Detection of a single-copy gene on plant chromosomes by in situ hybridization. Mol Genet Genom 211:143 147. https://doi.org/10.1007/BF00338405

    Google Scholar 

  3. Dong H, Quick JS (1995) Detection of 2.6 kb single-low copy DNA sequence on chromosomes of wheat (Triticum aestivum) and rye (Secale cereale). Genome 38:246–249. https://doi.org/10.1139/g95-030

    Article  CAS  PubMed  Google Scholar 

  4. Fransz PF et al (1996) Detection of single-copy genes and chromosome rearrangements in Petunia hybrida by fluorescence in situ hybridization. Plant J 9:767–774. https://doi.org/10.1046/j.1365-313X.1996.9050767.x

    Article  CAS  Google Scholar 

  5. Lamb JC et al (2007) Single-gene detection and karyotyping using small-target fluorescence in situ hybridization on maize somatic chromosomes. Genetics 175:1047–1058. https://doi.org/10.1534/genetics.106.065573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Gerhard DS, Kawasaki ES, Bancroft FC, Szabo P (1981) Localization of a unique gene by direct hybridization in situ. Proc Natl Acad Sci USA 78:3755–3759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Harper ME, Ullrich A, Saunders GR (1981) Localization of the human insulin gene to the distal end of the short arm of chromosome 11. Proc Natl Acad Sci USA 78:4458–4460. https://doi.org/10.1073/pnas.78.7.4458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Harper ME, Marselle LM (1985) In situ hybridization: applicabon to gene localization and RNA detection. Can Genet Cytogenet 19:73–80. https://doi.org/10.1016/0165-4608(86)90374-2

    Article  Google Scholar 

  9. Lawrence JB, Villnave CA, Singer RH (1988) Sensitive, high resolution chromatin and chromosome mapping in situ: presence and orientation of two closely integrated copies of EBV in a lymphoma line. Cell 52:51–61. https://doi.org/10.1016/0092-8674(88)90530-2

    Article  CAS  PubMed  Google Scholar 

  10. Henry HQ, Heng JS, Tsui LC (1992) High-resolution mapping of mammalian genes by in situ hybridization to free chromatin. Proc Natl Acad Sci USA 89:9509–9513. https://doi.org/10.1073/pnas.89.20.9509

    Article  Google Scholar 

  11. Lehfer H, Busch W, Martin R, Herrmann RG (1993) Localization of the B-hordein locus on barley chromosomes using fluorescence in situ hybridization. Chromosoma 102:428–432. https://doi.org/10.1007/BF00360408

    Article  Google Scholar 

  12. Jiang J, Gill BS, Wang GL, Ronald PC, Ward DC (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491. https://doi.org/10.1073/pnas.92.10.4487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Greilhuber J (1977) Why plant chromosomes do not show G-bands. Theor Appl Genet 50:121–124. https://doi.org/10.1007/BF00276805

    CAS  PubMed  Google Scholar 

  14. Schubert I, Rieger R, Döbel P (1984) G and/or C-bands in plant chromosomes? J Cell Sci 71:11–120

    Google Scholar 

  15. Mehrotra S, Goyal V (2014) Repetitive sequences in plant nuclear DNA: types, distribution, evolution and function. Genom Proteom Bioinform 12:164–171. https://doi.org/10.1016/j.gpb.2014.07.003

    Article  Google Scholar 

  16. Ohmido N, Akiyama Y, Fukui K (1998) Physical mapping of unique nucleotide sequences on identified rice chromosomes. Plant Mol Biol 38:1043–1052. https://doi.org/10.1023/A:1006062905742

    Article  CAS  PubMed  Google Scholar 

  17. Bernini C, Marin- Morales MA (2001) Karyotype analysis in Brachiaria (Poaceae) species. Cytobios 104:157–171

    CAS  PubMed  Google Scholar 

  18. Akiyama Y, Yamada-Akiyama H, Ebina M (2010) Morphological diversity of chromosomes bearing ribosomal DNA loci in Brachiaria species. Grassl Sci 56:217–223. https://doi.org/10.1111/j.1744-697X.2010.00197.x

    Article  Google Scholar 

  19. Nielen S, Almeida LM, Carneiro VT, Araujo AC (2010) Physical mapping of rDNA genes corroborates allopolyploid origin in apomictic Brachiaria brizantha. Sex Plant Reprod 23:45–51. https://doi.org/10.1007/s00497-009-0124-1

    Article  CAS  PubMed  Google Scholar 

  20. Nani TF, Pereira DL, Sobrinho FS, Techio VH (2016) Physical map of repetitive DNA sites in Brachiaria spp.: intravarietal and interspecific polymorphisms. Crop Sci 56:1769–1783. https://doi.org/10.2135/cropsci2015.12.0760 2016.

    Article  CAS  Google Scholar 

  21. Santos FC, Guyot R, do Valle CB, Chiari L, Techio VH, Heslop-Harrison P, Vanzela AL (2015) Chromosome distribution and evolution of abundant retrotransposons in plants: gypsy elements in diploid and polyploid Brachiaria forage grasses. Chromosom Res 23:571–582. https://doi.org/10.1007/s10577-015-9492-6

    Article  CAS  Google Scholar 

  22. Bennetzen JL et al (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30:555–561. https://doi.org/10.1038/nbt.2196

    Article  CAS  PubMed  Google Scholar 

  23. Peterson DG, Lapitan NLV, Stack SM (1999) Localization of single- and low-copy sequences on tomato synaptonemal complex spreads using fluorescence in situ hybridization (FISH). Genetics 152:427–439

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Giussani LM, Cota-Sánchez JH, Zuloaga FO, Kellogg EA (2001) A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis. Am J Bot 88:1993–2012. https://doi.org/10.2307/3558427

    Article  CAS  PubMed  Google Scholar 

  25. Schnable JC, Freeling M, Lyons E (2012) Genome-wide analysis of syntenic gene deletion in the grasses. Genome Biol Evol 4:265–277. https://doi.org/10.1093/gbe/evs009

    Article  PubMed  PubMed Central  Google Scholar 

  26. Lyons E, Pedersen B, Kane J, Freeling M (2008) The value of nonmodel genomes and an example using SynMap within CoGe to dissect the hexaploidy that predates the rosids. Trop Plant Biol 1:181–190. https://doi.org/10.1007/s12042-008-9017-y

    Article  CAS  Google Scholar 

  27. Wang L, Si Y, Dedow LK, Shao Y, Liu P, Brutnell TP (2011) A low-cost library construction protocol and data analysis pipeline for illumina-based strand-specific multiplex RNA-Seq. PLoS ONE 6/11:e26426. https://doi.org/10.1371/journal.pone.0026426

    Article  Google Scholar 

  28. Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kibbe WA (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35:W43–W46. https://doi.org/10.1093/nar/gkm234

    Article  PubMed  PubMed Central  Google Scholar 

  30. Kato A, Lamb JC, Birchler JA (2004) Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc Natl Acad Sci USA 101:13554–13559. https://doi.org/10.1073/pnas.0403659101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Washburn JD, Schnable JC, Davidse G, Pires JC (2015) Phylogeny and photosynthesis of the grass tribe Paniceae. Am J Bot 102:1–13. https://doi.org/10.3732/ajb.1500222

    Article  Google Scholar 

  32. Lamb JC, Birchler JA (2006) Retroelement genome painting: cytological visualization of retroelement expansions in the genera Zea and Tripsacum. Genetics 173:1007–1021. https://doi.org/10.1534/genetics.105.053165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Silva PIT, Martins AM, Gouvea EG, Pessoa-Filho M, Ferreira ME (2013) Development and validation of microsatellite markers for Brachiaria ruziziensis obtained by partial genome assembly of Illumina single-end reads. Genomics 14:2–9. https://doi.org/10.1186/1471-2164-14-17

    Google Scholar 

  34. Sumner AT (2008) Chromosomes, the karyotype and evolution, in chromosomes: organization and function. Blackwell Science Ltd, Oxford

    Google Scholar 

  35. Paula CMP de, Souza Sobrinho F, Techio VH (2015) Genome constitution and relantioship in Urochloa (Poaceae) species and hybrids. Crop Sci 57:2605–2616. https://doi.org/10.2135/cropsci2017.05.0307

    Article  Google Scholar 

  36. Mendes DV, Boldrini KR, Mendes-Bonato AB, Pagliarini MS, Valle CB do (2006) Cytological evidence of natural hybridization in Brachiaria brizantha Stapf (Gramineae). Bot J Linn Soc 150:441–446. https://doi.org/10.1111/j.1095-8339.2006.00493.x

    Article  Google Scholar 

  37. Leitch IJ, Heslop-Harrison JS (1993) Physical mapping of four sites of 5 s rDNA sequences and one site of the a-amylase-2 gene in barley (Hordeum vulgare). Genome 36:517–523. https://doi.org/10.1139/g93-071

    Article  CAS  PubMed  Google Scholar 

  38. Webb CA, Richter TE, Collins NC, Nicolas M, Trick HN, Pryor T, Hulbert SH (2002) Genetic and molecular characterization of the maize rp3 rust resistance locus. Genetics 162:381–394

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Smith SM, Pryor AJ, Hulbert SH (2004) Allelic and haplotypic diversity at the rp1 rust resistance locus of maize. Genetics 167:1939–1947. https://doi.org/10.1534/genetics.104.029371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Woo YM, Hu DW, Larkins BA, Jung R (2001) Genomics analysis of genes expressed in maize endosperm identifies novel seed proteins and clarifies patterns of zein gene expression. Plant Cell 13:2297–2317. https://doi.org/10.1105/tpc.010240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Wu Y, Meeley RB, Cosgrove DJ (2001) Analysis and expression of the alpha-expansin and beta-expansin gene families in maize. Plant Physiol 126:222–232. https://doi.org/10.1104/pp.126.1.222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Abrouk M, Murat F, Pont C, Messing J, Jackson S, Faraut T, Tannier E, Plomion C, Cooke R, Feuillet C, Salse J (2010) Palaeogenomics of plants: synteny-based modelling of extinct ancestors. Trends Plant Sci 15:479–487. https://doi.org/10.1016/j.tplants.2010.06.001

    Article  CAS  PubMed  Google Scholar 

  43. Yu W, Lamb JC, Han F, Birchler JA (2007) Cytological visualization of transposable elements and their transposition pattern in somatic cells of maize. Genetics 175:31–39. https://doi.org/10.1534/genetics.106.064238

    Article  PubMed  PubMed Central  Google Scholar 

  44. Song R, Messing J (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci USA 100:9055–9060. https://doi.org/10.1073/pnas.1032999100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Brunner S, Fengler K, Morgante M, Tingey S, Rafalskia A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17:343–360. https://doi.org/10.1105/tpc.104.025627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lai J, Li Y, Messing J, Dooner HK (2005) Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci USA 102:9068–9073. https://doi.org/10.1073/pnas.0502923102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Richard F, Vogt N, Muleris M, Malfoy B, Dutrillaux B (1994) Increased FISH efficiency using APC probes generated by direct incorporation of labelled nucleotides by PCR. Cytogenet Cell Genet 65:169–171. https://doi.org/10.1159/000133624

Download references

Acknowledgements

The authors are thankful to Dr. Ryan Douglas at University of Missouri for helping in designing the centromeric retrotransposons of maize 1 probe (CRM1), and to the Brazilian agencies of research support as Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and the program “Science without Borders” of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vânia Helena Techio.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 143 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nani, T.F., Schnable, J.C., Washburn, J.D. et al. Location of low copy genes in chromosomes of Brachiaria spp.. Mol Biol Rep 45, 109–118 (2018). https://doi.org/10.1007/s11033-018-4144-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-018-4144-5

Keywords

Navigation