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Subgenomic analysis of microRNAs in polyploid wheat

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Abstract

In this study, a survey of miRNAs using the next-generation sequencing data was performed at subgenomic level. After analyzing shotgun sequences from chromosome 4A of bread wheat (Triticum aestivum L.), a total of 68 different miRNAs were predicted in silico, of which 37 were identified in wheat for the first time. The long arm of the chromosome was found to harbor a higher variety (51) and representation (3,928) of miRNAs compared with the short arm (49; 2,226). Out of the 68 miRNAs, 32 were detected to be common to both arms, revealing the presence of separate miRNA clusters in the two chromosome arms. The differences in degree of representation of the different miRNAs were found to be highly variable, ranging 592-fold, which may have an effect on target regulation. Targets were retrieved for 62 (out of 68) of wheat-specific, newly identified miRNAs indicated that fundamental aspects of plant morphology such as height and flowering were predicted to be affected. In silico expression blast analysis indicated 24 (out of 68) were found to give hits to expressed sequences. This is the first report of species- and chromosome-specific miRNAs.

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Abbreviations

miRNA:

MicroRNA

4AS:

Short arm of chromosome 4A

4AL:

Long arm of chromosome 4A

e value:

Expectation value

ΔG :

Folding-free energies

EST:

Expressed sequence tag

MFE:

Minimal folding-free energy

MFEI:

Minimal folding-free energy index

miRNA*:

miRNA star strand

NCBI:

National center for biotechnology information

nt:

Nucleotide(s)

premiRNA:

MicroRNA precursor

siRNA:

Small interfering RNA

TE:

Transposable element

mRNA:

Messenger RNA

References

  • Bonnet E, Wuyts J et al (2004) Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc Natl Acad Sci U S A 101(31):11511–11516

    Article  PubMed  CAS  Google Scholar 

  • Budak H, Akpinar BA (2011) Dehydration stress-responsive miRNA in Brachypodium distachyon: evident by genome-wide screening of microRNAs expression. OMICS 15(11):791–799

    Article  PubMed  CAS  Google Scholar 

  • Camacho C, Coulouris G et al (2009) BLAST+: architecture and applications. BMC Bioinforma 10:421

    Article  Google Scholar 

  • Chartrain L, Berry ST, Brown JKM (2005) Resistance of wheat line Kavkaz-K4500 L.6.A.4 to Septoria tritici blotch controlled by isolate-specific resistance genes. Phytopathology 95(6):664–671

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Line RF, Jones SS (1995) Chromosomal location of genes for resistance to Puccinia striiformis in winter wheat cultivars Heines VII, Clement, Moro, Tyee, Tres, and Daws. Phytopathology 85(11):1362–1367

    Article  Google Scholar 

  • Czech B, Hannon GJ (2011) Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet 12(1):19–31

    Article  PubMed  CAS  Google Scholar 

  • Dolezel J, Kubalakova M et al (2007) Chromosome-based genomics in the cereals. Chromosome Res 15(1):51–66

    Article  PubMed  CAS  Google Scholar 

  • Dryanova A, Zakharov A et al (2008) Data mining for miRNAs and their targets in the Triticeae. Genome 51(6):433–443

    Article  PubMed  CAS  Google Scholar 

  • Dugas DV, Bartel B (2004) MicroRNA regulation of gene expression in plants. Curr Opin Plant Biol 7(5):512–520

    Article  PubMed  CAS  Google Scholar 

  • Fahim M, Mechanicos A, Ayala-Navarrete L, Haber S, Larkin PJ (2011) Resistance to wheat streak mosaic virus—a survey of resources and development of molecular markers. Plant Pathol. doi:10.1111/j.1365-3059.2011.02542.x

  • Griffiths-Jones S, Grocock RJ et al (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34(Database issue):D140–D144

    Article  PubMed  CAS  Google Scholar 

  • Hernandez P, Martis M et al (2012) Next-generation sequencing and syntenic integration integration of flow-sorted arms of wheat chromosome 4A exposes the chromosome structure and gene content. Plant J 69(30):377–386

    Article  PubMed  CAS  Google Scholar 

  • Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12(2):99–110

    Article  PubMed  CAS  Google Scholar 

  • International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768

    Google Scholar 

  • Jin W, Li N et al (2008) Identification and verification of microRNA in wheat (Triticum aestivum). J Plant Res 121(3):351–355

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP et al (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  PubMed  CAS  Google Scholar 

  • Kantar M, Unver T et al (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genomics 10(4):493–507

    Article  PubMed  CAS  Google Scholar 

  • Kantar M, Lucas SJ et al (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233(3):471–484

    Article  PubMed  CAS  Google Scholar 

  • Khraiwesh B, Zhu JK et al (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819(2):137–148

    Article  PubMed  CAS  Google Scholar 

  • Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6(5):376–385

    Article  PubMed  CAS  Google Scholar 

  • Krol J, Loedige I et al (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11(9):597–610

    PubMed  CAS  Google Scholar 

  • Li A, Mao L (2007) Evolution of plant microRNA gene families. Cell Res 17(3):212–218

    PubMed  CAS  Google Scholar 

  • Li W, Zhang P et al (2004) Sequence composition, organization, and evolution of the core Triticeae genome. Plant J 40(4):500–511

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Wang L, Yao J, Zheng Y, Zhao C (2010) Association mapping of six agronomic traits on chromosome 4A of wheat (Triticum aestivum L.). Mol Plant Breed 1(5)

  • Mares D, Mrva K et al (2005) A QTL located on chromosome 4A associated with dormancy in white- and red-grained wheats of diverse origin. Theor Appl Genet 111(7):1357–1364

    Article  PubMed  CAS  Google Scholar 

  • Markham NR, Zuker M (2008) UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 453:3–31

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Axtell MJ et al (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20(12):3186–3190

    Article  PubMed  CAS  Google Scholar 

  • Miftahudin, Ross K et al (2004) Analysis of expressed sequence tag loci on wheat chromosome group 4. Genetics 168:651–663

    Article  PubMed  CAS  Google Scholar 

  • Naik S, Gill KS, Prakasa Rao VS, Gupta VS, Tamhankar SA, Pujar S, Gill BS, Ranjekar PK (1998) Identification of a STS marker linked to the Aegilops speltoides-derived leaf rust resistance gene Lr28 in wheat. Theor Appl Genet 97(4):535–540

    Article  CAS  Google Scholar 

  • Navarro L, Dunoyer P et al (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312(5772):436–439

    Article  PubMed  CAS  Google Scholar 

  • Park MY, Wu G et al (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci U S A 102(10):3691–3696

    Article  PubMed  CAS  Google Scholar 

  • Paux E, Roger D et al (2006) Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plant J 48(3):463–474

    Article  PubMed  CAS  Google Scholar 

  • Phillips JR, Dalmay T et al (2007) The role of small RNAs in abiotic stress. FEBS Lett 581(19):3592–3597

    Article  PubMed  CAS  Google Scholar 

  • Piriyapongsa J, Jordan IK (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14(5):814–821

    Article  PubMed  CAS  Google Scholar 

  • Rhoades MW, Reinhart BJ et al (2002) Prediction of plant microRNA targets. Cell 110(4):513–520

    Article  PubMed  CAS  Google Scholar 

  • Sabot F, Guyot R et al (2005) Updating of transposable element annotations from large wheat genomic sequences reveals diverse activities and gene associations. Mol Genet Genomics 274(2):119–130

    Article  PubMed  CAS  Google Scholar 

  • Schreiber AW, Shi BJ et al (2011) Discovery of barley miRNAs through deep sequencing of short reads. BMC Genomics 12:129

    Article  PubMed  CAS  Google Scholar 

  • Schwab R, Palatnik JF et al (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8(4):517–527

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Girke T et al (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17(5):1397–1411

    Article  PubMed  CAS  Google Scholar 

  • Unver T, Budak H (2009) Conserved microRNAs and their targets in model grass species Brachypodium distachyon. Planta 230(4):659–669

    Article  PubMed  CAS  Google Scholar 

  • Unver T, Namuth-Covert DM, Budak H (2009) Review of current methodological approaches for characterizing microRNAs in plants. Int J Plant Genomics. doi:10.1155/2009/262463

  • Unver T, Bakar M et al (2010) Genome-wide profiling and analysis of Festuca arundinacea miRNAs and transcriptomes in response to foliar glyphosate application. Mol Genet Genomics 283(4):397–413

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 13(7):350–358

    Article  PubMed  CAS  Google Scholar 

  • Vitulo N, Albiero A et al (2011) First survey of the wheat chromosome 5A composition through a next generation sequencing approach. PLoS One 6(10):e26421

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687

    Article  PubMed  CAS  Google Scholar 

  • Wei B, Cai T et al (2009) Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct Integr Genomics 9(4):499–511

    Article  PubMed  CAS  Google Scholar 

  • Wu L, Zhou H et al (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38(3):465–475

    Article  PubMed  CAS  Google Scholar 

  • Yao Y, Guo G et al (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8(6):R96

    Article  PubMed  Google Scholar 

  • Zhang BH, Pan XP et al (2006a) Identification of 188 conserved maize microRNAs and their targets. Febs Letters 580(15):3753–3762

    Article  PubMed  CAS  Google Scholar 

  • Zhang BH, Pan XP et al (2006b) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289(1):3–16

    Article  PubMed  CAS  Google Scholar 

  • Zhang BH, Wang QL et al (2007a) MicroRNAs and their regulatory roles in animals and plants. J Cell Physiol 210(2):279–289

    Article  PubMed  CAS  Google Scholar 

  • Zhang BH, Wang QL et al (2007b) Identification of cotton microRNAs and their targets. Gene 397(1–2):26–37

    Article  PubMed  CAS  Google Scholar 

  • Zhang BH, Pan XP et al (2008) Identification of soybean microRNAs and their targets. Planta 229(1):161–182

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Chia JM et al (2009) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5(11):e1000716

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Financial support by the Sabanci University Internal Grant, Spanish Ministry of Science and Innovation (MICINN grants BIO2009-07443, AGL2010-17316, and BIO2011-15237) and the Ministry of Education, Youth and Sports of the Czech Republic and the European Regional Development Fund (Operational Program Research and Development for Innovations No. ED0007/01/01) is gratefully acknowledged. The authors also acknowledge the help of D. Adali, E. Toklu, R. Fayotorbay, and The International Wheat Genome Sequencing Consortium for access to the 4A survey sequence developed under the IWGSC Survey Sequencing Initiative.

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Correspondence to Hikmet Budak.

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Supplementary Table 1

A) Perl Program SUmirFind.pl This script uses NCBI BLAST to search for potential homologs of known miRNAs. B) Perl Program SumiRFold. This script uses a BLAST results table to retrieve sequences from the BLAST database and to obtain their predicted secondary structure using UNAfold, after which viable hairpins are detected and retrieved. (DOC 67 kb)

Supplementary Table 2

List of computer based, newly identified miRNAs of chromosome 4A in T. aestivum and their characteristics. This table lists characteristics of only one identified wheat miRNA, derived from one sequence read, corresponding to each query sequence (DOC 405 kb)

Supplementary Table 3

Number of sequence reads of 4AL from which potential miRNA stem-loop structures were retrieved. (DOC 3363 kb)

Supplementary Table 4

Number of sequence reads of 4AS from which potential miRNA stem-loop structures were retrieved. (DOC 1908 kb)

Supplementary Table 5

Homology of newly identified T. aestivum miRNAs to miRNAs in other plant species. A) Only 4AS; B) only 4AL; C) both chromosome arms (DOC 563 kb)

Supplementary Table 6

Predicted targets of newly identified T. aestivum miRNAs. Targets were retrieved using psRNATarget software. (DOC 256 kb)

Supplementary Table 7

Number of Blast hits for each miRNA (DOC 56 kb)

Supplementary Table 8

Distribution of conserved miRNAs on B. distachyon chromosomes. (DOC 82 kb)

Supplementary Table 9

Distribution of conserved miRNAs on O. sativa chromosomes. (DOC 249 kb)

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Kantar, M., Akpınar, B.A., Valárik, M. et al. Subgenomic analysis of microRNAs in polyploid wheat. Funct Integr Genomics 12, 465–479 (2012). https://doi.org/10.1007/s10142-012-0285-0

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