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Molecular Biology Reports

, Volume 40, Issue 11, pp 6245–6253 | Cite as

Long non-coding genes implicated in response to stripe rust pathogen stress in wheat (Triticum aestivum L.)

  • Hong Zhang
  • Xueyan Chen
  • Changyou Wang
  • Zhongyang Xu
  • Yajuan Wang
  • Xinlun Liu
  • Zhensheng Kang
  • Wanquan Ji
Article

Abstract

The non-protein-coding genes have been reported as a critical control role in the regulation of gene expression in abiotic stress. We previously identified four expressed sequence tags numbered S18 (EL773024), S73 (EL773035), S106 (EL773041) and S108 (EL773042) from a SSH-cDNA library of bread wheat Shaanmai 139 infected with Puccinia striiformis f. sp. tritici (Pst). Here, we isolated four cDNA clones and referred them as TalncRNA18, TalncRNA73, TalncRNA106 and TalncRNA108 (GenBank: KC549675–KC549678). These cDNA separately consisted of 1,393, 667, 449 and 647 nucleotides but without any open reading frame. The alignment result showed that TalncRNA18 is a partial cDNA of E3 ubiquitin-protein ligase UPL1-like gene, TalncRNA73 is an antisense transcript of hypothetical protein, TalncRNA108 is a homolog to RRNA intron-encoded homing endonuclease, and lncRNA106 had no similarly sequence. Quantitative RT-PCR studies confirmed that these four lncRNAs were differentially expressed in three near isogenic lines. TalncRNA108 was significantly stepwise decreased at early stage of inoculation with Pst, while the others were upregulated, especially at 1 and 3 dpi (days post-inoculation). Using Chinese Spring nulli-tetrasomic lines and its ditelosomic lines, TalncRNA73 and TalncRNA108 were located to wheat chromosome 7A and the short arm of chromosome 4B, respectively, while TalncRNA18 and TalncRNA106 were located to chromosome 5B. Comparing the sequence of DNA and cDNA of four lncRNAs with polymerase chain reaction primers, the results showed that all of them have no introns. The kinetics analyses of lncRNAs expression as a result of pathogen challenge in immune resistant genotype indicated that they may play the roles of modulating or silencing the protein-coding gene into pathogen-defence response.

Keywords

Wheat Long non-coding RNA Puccinia striiformis f. sp. tritici Pathogen induction Expression 

Notes

Acknowledgments

This work was financially supported by National Key Basic Research Program of China (2013CB127700), the National Natural Science Foundation of China (31371612) and the Fundamental Research Funds for the Central Universities (Northwest A&F University, QN2011002).

References

  1. 1.
    Huang H, Jiao R (2012) Roles of chromatin assembly factor 1 in the epigenetic control of chromatin plasticity. Sci China Life Sci 55:15–19PubMedCrossRefGoogle Scholar
  2. 2.
    Bi X (2012) Functions of chromatin remodeling factors in heterochromatin formation and maintenance. Sci China Life Sci 55:89–96PubMedCrossRefGoogle Scholar
  3. 3.
    Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43:904–914PubMedCrossRefGoogle Scholar
  4. 4.
    Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou MM (2010) Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 38:662–674PubMedCrossRefGoogle Scholar
  5. 5.
    Wapinski O, Chang HY (2011) Long noncoding RNAs and human disease. Trends Cell Biol 21:354–361PubMedCrossRefGoogle Scholar
  6. 6.
    Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA et al (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472:120–124PubMedCrossRefGoogle Scholar
  7. 7.
    Martianov I, Ramadass A, Serra Barros A, Chow N, Akoulitchev A (2007) Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445:666–670PubMedCrossRefGoogle Scholar
  8. 8.
    Mariner PD, Walters RD, Espinoza CA, Drullinger LF, Wagner SD, Kugel JF, Goodrich JA (2008) Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol Cell 29:499–509PubMedCrossRefGoogle Scholar
  9. 9.
    Atkinson SR, Marguerat S, Bähler J (2012) Exploring long non-coding RNAs through sequencing. Semin Cell Dev Biol 23:200–205PubMedCrossRefGoogle Scholar
  10. 10.
    Gong ZJ, Zhang SS, Zhang WL, Huang HB, LI Q, Deng H, Ma J, Zhou M, Xiang J, Wu MH, Li XY, Xiong W, Li XL, Li Y, Zeng ZY, Li GY (2012) Long non-coding RNAs in cancer. Sci China Life Sci 55(12):1120–1124. doi: 10.1007/s11427-012-4413-9 PubMedCrossRefGoogle Scholar
  11. 11.
    Lewis A, Reik W (2006) How imprinting centres work. Cytogenet Genome Res 113:81–89PubMedCrossRefGoogle Scholar
  12. 12.
    Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS (2010) Non-coding RNAs: regulators of disease. J Pathol 220:126–139PubMedCrossRefGoogle Scholar
  13. 13.
    Yang ZM, Xie CJ, Sun QX (2003) Situation of the sources of stripe rust resistance of wheat in the post-CY32 era in China. Acta Agronomica Sin 29(2):161–168Google Scholar
  14. 14.
    Coram TE, Settles ML, Chen XM (2008) Transcriptome analysis of high-temperature adult-plant resistance conditioned by Yr39 during the wheat-Puccinia striiformis f. sp. tritici interaction. Mol Plant Pathol 9(4):479–493PubMedCrossRefGoogle Scholar
  15. 15.
    Yu X, Wang X, Wang C, Chen X, Qu Z, Yu X, Han Q, Zhao J, Guo J, Huang L, Kang Z (2010) Wheat defense genes in fungal (Puccinia striiformis) infection. Funct Integr Genomics 10:227–239PubMedCrossRefGoogle Scholar
  16. 16.
    Zhang H, Hu YG, Wang CY, Ji WQ (2011) Gene expression in wheat induced by inoculation with Puccinia striiformis West. Plant Mol Biol Rep 29(2):458–465CrossRefGoogle Scholar
  17. 17.
    Zhang H, Hu YG, Yang BJ, Xue F, Kang ZS, Ji WQ (2013) Isolation and characterization of a wheat IF2 homologue required for innate immunity to stripe rust. Plant Cell Rep 32:591–600PubMedCrossRefGoogle Scholar
  18. 18.
    Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC (2005) NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr Biol 15:968–973PubMedCrossRefGoogle Scholar
  19. 19.
    Liu B, Xue XD, Cui SP, Zhang XY, Han QM, Zhu L, Liang XF, Wang XJ, Huang LL, Chen XM, Kang ZS (2010) Cloning and characterization of a wheat β-1, 3-glucanase gene induced by the stripe rust pathogen Puccinia striiformis f. sp. tritici. Mol Biol Rep 37:1045–1052PubMedCrossRefGoogle Scholar
  20. 20.
    Zhang H, Ren ZL, Hu YG, Wang CY, Ji WQ (2010) Characterization of wheat stripe rust resistance genes in Shaanmai 139. Acta Agron Sin 36(1):109–114CrossRefGoogle Scholar
  21. 21.
    Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31(13):3406–3415PubMedCrossRefGoogle Scholar
  22. 22.
    Zhang H, Yang BJ, Wang YJ, Wang CY, Liu XL, Ji WQ (2013) Molecular characterisation and expression of a pathogen-induced senescence-associated gene in wheat (Triticum aestivum). Australasian Plant Pathol 42:53–61CrossRefGoogle Scholar
  23. 23.
    De Lucia F, Dean C (2011) Long non-coding RNAs and chromatin regulation. Curr Opin Plant Biol 14:168–173PubMedCrossRefGoogle Scholar
  24. 24.
    Wen J, Parker BJ, Weiller GF (2007) In Silico identification and characterization of mRNA-like noncoding transcripts in Medicago truncatula. In Silico Biol 7:485–505PubMedGoogle Scholar
  25. 25.
    Okamoto M, Tatematsu K, Matsui A, Morosawa T, Ishida J, Tanaka M, Endo TA, Mochizuki Y, Toyoda T, Kamiya Y, Shinozaki K, Nambara E, Seki M (2010) Genome-wide analysis of endogenous abscisic acidmediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. Plant J 62:39–51PubMedCrossRefGoogle Scholar
  26. 26.
    Yamada K, Lim J, Dale JM, Chen H, Shinn P, Palm CJ, Southwick AM, Wu HC, Kim C, Nguyen M et al (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302:842–846PubMedCrossRefGoogle Scholar
  27. 27.
    Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-DiNardo D, Kanduri C (2008) Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 32:232–246PubMedCrossRefGoogle Scholar
  28. 28.
    Jaskiewicz L, Filipowicz W (2008) Role of Dicer in posttranscriptional RNA silencing. Curr Top Microbiol Immunol 320:77–97PubMedCrossRefGoogle Scholar
  29. 29.
    Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermüller J, Hofacker IL, Bell I, Cheung E, Drenkow J, Dumais E, Patel S, Helt G, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316:1484–1488PubMedCrossRefGoogle Scholar
  30. 30.
    Ganesan G, Rao SMR (2008) A novel noncoding RNA processed by Drosha is restricted to nucleus in mouse. RNA 14:1399–1410PubMedCrossRefGoogle Scholar
  31. 31.
    Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, Hannon GJ (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453:534–538PubMedCrossRefGoogle Scholar
  32. 32.
    Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, Chiba H, Kohara Y, Kono T, Nakano T, Surani MA, Sakaki Y, Sasaki H (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453:539–544PubMedCrossRefGoogle Scholar
  33. 33.
    Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619PubMedCrossRefGoogle Scholar
  34. 34.
    Kanellopoulou C, Muljo SA, Dimitrov SD, Chen X, Colin C, Plath K, Livingston DM (2009) X chromosome inactivation in the absence of Dicer. Proc Natl Acad Sci USA 106(4):1122–1127PubMedCrossRefGoogle Scholar
  35. 35.
    Faghihi MA, Wahlestedt C (2009) Regulatory roles of natural antisense transcripts. Nat Rev Mol Cell Biol 10(9):637–643PubMedCrossRefGoogle Scholar
  36. 36.
    Beltran M, Puig I, Peña C, García JM, Álvarez AB, Peña R, Bonilla F, Herreros AG (2008) A natural antisense transcript regulates Zeb2/Sip1 gene expression during Snail1-induced epithelial–mesenchymal transition. Genes Dev 22:756–769PubMedCrossRefGoogle Scholar
  37. 37.
    Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–803PubMedCrossRefGoogle Scholar
  38. 38.
    Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJM (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21:367–376PubMedCrossRefGoogle Scholar
  39. 39.
    Furuno M, Pang KC, Ninomiya N, Fukuda S, Frith MC, Bult C et al (2006) Clusters of internally-primed transcripts reveal novel long noncoding RNAs. PLoS Genet 2(4):e37. doi: 10.1371/journal.pgen.0020037 PubMedCrossRefGoogle Scholar
  40. 40.
    Mehler MF, Mattick JS (2006) Non-coding RNAs in the nervous system. J Physiol 575:333–341PubMedCrossRefGoogle Scholar
  41. 41.
    Arteaga-Vazquez M, Sidorenko L, Rabanal FA, Shrivistava R, Nobuta K, Green PJ, Meyers BC, Chandler VL (2010) RNA-mediated trans-communication can establish paramutation at the b1 locus in maize. Proc Natl Acad Sci USA 107:12986–12991PubMedCrossRefGoogle Scholar
  42. 42.
    Amor BB, Wirth S, Merchan F, Laporte P, d’Aubenton-Carafa Y, Hirsch J, Mallory A, Maizel A, Lucas A, Deragon JM, Vaucheret H, Thermes C, Crespi M (2009) Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 19:57–69PubMedCrossRefGoogle Scholar
  43. 43.
    Guo XL, Gao L, Liao Q, Xiao H, Ma XK, Yang XF, Luo HT, Zhao GG, Bu DC, Jiao F, Shao QX, Chen RS, Zhao Y (2013) Long non-coding RNAs function annotation: a global prediction method based on bi-colored networks. Nucleic Acids Res 41(2):e35. doi: 10.1093/nar/gks967 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.State Key Laboratory of Crop Stress Biology for Arid AreaCollege of Agronomy, Northwest A&F UniversityYanglingChina
  2. 2.State Key Laboratory of Crop Stress Biology for Arid AreaCollege of Plant Protection, Northwest A&F UniversityYanglingChina

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