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Genome-wide survey of rice microRNAs and microRNA–target pairs in the root of a novel auxin-resistant mutant

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Abstract

Auxin is one of the central hormones in plants, and auxin response factor (ARF) is a key regulator in the early auxin response. MicroRNAs (miRNAs) play an essential role in auxin signal transduction, but knowledge remains limited about the regulatory network between miRNAs and protein-coding genes (e.g. ARFs) involved in auxin signalling. In this study, we used a novel auxin-resistant rice mutant with plethoric root defects to investigate the miRNA expression patterns using microarray analysis. A number of miRNAs showed reduced auxin sensitivity in the mutant compared with the wild type, consistent with the auxin-resistant phenotype of the mutant. Four miRNAs with significantly altered expression patterns in the mutant were further confirmed by Northern blot, which supported our microarray data. Clustering analysis revealed some novel auxin-sensitive miRNAs in roots. Analysis of miRNA duplication and expression patterns suggested the evolutionary conservation between miRNAs and protein-coding genes. MiRNA promoter analysis suggested the possibility that most plant miRNAs might share the similar transcriptional mechanisms with other non-plant eukaryotic genes transcribed by RNA polymerase II. Auxin response elements were proved to be more frequently present in auxin-related miRNA promoters. Comparative analysis of miRNA and protein-coding gene expression datasets uncovered many reciprocally expressed miRNA–target pairs, which could provide some hints for miRNA downstream analysis. Based on these findings, we also proposed a feedback circuit between miRNA(s) and ARF(s). The results presented here could serve as the basis for further in-depth studies of plant miRNAs involved in auxin signalling.

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Abbreviations

α-NAA:

α-Naphthalene acetic acid

ARF:

Auxin response factor

AuxRE:

Auxin response element

EMS:

Ethyl methanesulfonate

GO:

Gene Ontology

IAA:

3-Indole acetic acid

MiRNA:

MicroRNA

MT:

osaxr mutant

osaxr :

Oryza sativa auxin resistant

TF:

Transcription factor

TSS:

Transcription start site

WT:

Wild type

References

  • Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36:1282–1290

    Article  CAS  PubMed  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    Article  CAS  PubMed  Google Scholar 

  • Axtell MJ, Bowman JL (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci 13:343–349

    Article  CAS  PubMed  Google Scholar 

  • Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193

    Article  CAS  PubMed  Google Scholar 

  • Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383

    Article  CAS  PubMed  Google Scholar 

  • Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332

    Article  CAS  PubMed  Google Scholar 

  • Cleveland WS, Devlin SJ (1988) Locally weighted regression: an approach to regression analysis by local fitting. J Am Stat Assoc 83:596–610

    Article  Google Scholar 

  • Cui X, Xu SM, Mu DS, Yang ZM (2009) Genomic analysis of rice microRNA promoters and clusters. Gene 431:61–66

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation. Trends Plant Sci 9:302–308

    Article  CAS  PubMed  Google Scholar 

  • Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O (2004) Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16:1235–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao X, Gulari E, Zhou X (2004) In situ synthesis of oligonucleotide microarrays. Biopolymers 73:579–596

    Article  CAS  PubMed  Google Scholar 

  • Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34:D140–D144

    Article  CAS  PubMed  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  CAS  PubMed  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gustafson AM, Allen E, Givan S, Smith D, Carrington JC, Kasschau KD (2005) ASRP: the Arabidopsis small RNA project database. Nucleic Acids Res 33:D637–D640

    Article  CAS  PubMed  Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314

    Google Scholar 

  • Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jain M, Kaur N, Garg R, Thakur JK, Tyagi AK, Khurana JP (2006) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genomics 6:47–59

    Article  CAS  PubMed  Google Scholar 

  • Jiang D, Yin C, Yu A, Zhou X, Liang W, Yuan Z, Xu Y, Yu Q, Wen T, Zhang D (2006) Duplication and expression analysis of multicopy miRNA gene family members in Arabidopsis and rice. Cell Res 16:507–518

    Article  CAS  PubMed  Google Scholar 

  • Johnson C, Bowman L, Adai AT, Vance V, Sundaresan V (2007) CSRDB: a small RNA integrated database and browser resource for cereals. Nucleic Acids Res 35:D829–D833

    Article  CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–4060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leyser O (2002) Molecular genetics of auxin signaling. Annu Rev Plant Biol 53:377–398

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31–36

    Article  CAS  PubMed  Google Scholar 

  • Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146

    Article  CAS  PubMed  Google Scholar 

  • Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    Article  CAS  PubMed  Google Scholar 

  • Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16:510–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Megraw M, Baev V, Rusinov V, Jensen ST, Kalantidis K, Hatzigeorgiou AG (2006) MicroRNA promoter element discovery in Arabidopsis. RNA 12:1612–1619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49:592–606

    Article  CAS  PubMed  Google Scholar 

  • Ru P, Xu L, Ma H, Huang H (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res 16:457–465

    Article  CAS  PubMed  Google Scholar 

  • Shahmuradov IA, Gammerman AJ, Hancock JM, Bramley PM, Solovyev VV (2003) PlantProm: a database of plant promoter sequences. Nucleic Acids Res 31:114–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309

    Article  CAS  PubMed  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    Article  CAS  PubMed  Google Scholar 

  • Tian CE, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J 40:333–343

    Article  CAS  PubMed  Google Scholar 

  • Tsang J, Zhu J, van Oudenaarden A (2007) MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 26:753–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci USA 102:9703–9708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133:4211–4218

    Article  CAS  PubMed  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang JH, Han SJ, Yoon EK, Lee WS (2006) Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res 34:1892–1899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. The International Rice Research Institute, Manila

    Google Scholar 

  • Zhang Y (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res 33:W701–W704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Ruan J, Wang G, Zhang W (2007) Characterization and identification of microRNA core promoters in four model species. PLoS Comput Biol 3:e37

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu Q, Hong A, Sheng N, Zhang X, Matejko A, Jun KY, Srivannavit O, Gulari E, Gao X, Zhou X (2007) microParaflo biochip for nucleic acid and protein analysis. Methods Mol Biol 382:287–312

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study is supported by 973 Program (2005CB120901), NSFC (30771326), 863 Program (2008AA10Z125), and Program for NCET.

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Correspondence to Ming Chen.

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Meng, Y., Huang, F., Shi, Q. et al. Genome-wide survey of rice microRNAs and microRNA–target pairs in the root of a novel auxin-resistant mutant. Planta 230, 883–898 (2009). https://doi.org/10.1007/s00425-009-0994-3

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  • DOI: https://doi.org/10.1007/s00425-009-0994-3

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