Abstract
Eukaryotic gene expression is regulated at least by two processes, RNA interference at the post-transcriptional level and chromatin modification at the transcriptional level. Distinct small RNAs (approximately 21–24 nucleotides; sRNAs) were demonstrated to play vital roles in facilitating gene silencing. In plants, the generation of these sRNAs mainly depends on some proteins encoded by respective Dicer-like (DCL), Argonaute (AGO) and RNA-dependent RNA polymerases (RDR) gene families. Here, we analyzed the DCL, AGO and RDR gene families in maize, including gene structure, phylogenetic relationships, protein conserved motifs and genomic localization among gene family members. A total of 5 Zmdcl, 18 Zmago and 5 Zmrdr genes were identified in maize. Phylogenetic analyses clustered each of these genes families into four subfamilies. In addition, gene chromosomal localization revealed that five pairs of Zmago genes resulted from tandem or segmental duplication, respectively. EST expression data mining revealed that these newly identified genes had temporal and spatial expression pattern. Furthermore, the transcripts of these genes were detected in the leaves by two different abiotic stress treatments using semi-quantitative RT-PCR. The data demonstrated that these genes exhibited different expression levels in stress treatments. The results of this study provided basic genomic information for these gene families and insights into the probable roles of these genes in plant growth and development. This will further provide a solid foundation for future functional genomics studies of Dicer-like, Argonaute and RDR gene families in maize.
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References
Astier-Manifacier S, Cornuet P (1971) RNA-dependent RNA polymerase in Chinese cabbage. Biochim Biophys Acta 232:484–493
Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3:21–29
Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits mRNAs and siRNAs. Proc Natl Acad Sci USA 102:11928–11933
Bernstein E, Caudy AA, Hammond SM, Harmon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409(6818):363–366
Carmell MA, Xuan Z, Zhang M, Hannon GJ (2002) The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev 16:2733–2742
Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338
Chan SWL, Zilberman D, **e Z, Johansen LK, Carrington JC, Jacobsen SE (2004) RNA silencing genes control de novo DNA methylation. Science 303:1336
Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896
Cogoni C, Macino G (1999) Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399:166–169
Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe DC (2000) An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543–553
Deleris A, Gallego-Bartolome J, Bao J, Kasschau KD, Carrington JC, Voinnet O (2006) Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:68–71
Djupedal I, Ekwall K (2009) Epigenetics: heterochromatin meets RNAi. Cell Res 19:282–295
Dorweiler JE, Carey CC, Kubo KM, Hollick JB, Kermicle JL, Chandler VL (2000) Mediator of paramutation1 is required for establishment and maintenance of paramutation at multiple maize loci. Plant Cell 12:2101–2118
Eddy SR (2008) A probabilistic model of local sequence alignment that simplifies statistical significance estimation. PloS Comput Bio l4(5):e1000069
Fagard M, Boutet S, Morel J-B, Bellini C, Vaucheret H (2000) AG01, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc Natl Acad Sci USA 97:11650–11654
Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944
Finnegan EJ, Matzke MA (2003) The small RNA world. J Cell Sci 116:4689–4693
Girard A, Sachidanandam R, Hannon GJ, Carmell MA (2006) A germline specific class of small RNAs binds mammalian Piwi proteins. Nature 442(7099):199–202
Großhans H, Filipowicz W (2008) The expanding world of small RNAs. Nature 451:414–416
Gu Z, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of drosophila, nematode, and yeast. Mol Biol Evol 19:256–262
Hammond SM, Boettcher S, Caudy AA, Kobayashi R, Hannon GJ (2001) Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293:1146–1150
Henderson IR, Zhang X, Lu C, Johnson L, Meyers BC, Green PJ, Jacobsen SE (2006) Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat Genet 38(6):721–725
Höck J, Meister G (2008) The Argonaute protein family. Genome Biol 210(9):1–8
Hunter C, Sun H, Poethig RS (2003) The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr Biol 13:1734–1739
Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9:22–32
Iyer LM, Koonin EV, Aravind L (2003) Evolutionary connection between the catalytic subunits of DNA-dependent RNA polymerases and eukaryotic RNA-dependent RNA polymerases and the origin of RNA polymerases. BMC Struct Biol 3(1):1
Jia Y, Lisch DR, Ohtsu K, Scanlon MJ, Nettleton D, Schnable PS (2009) Loss of RNA-dependent RNA polymerase 2 (RDR2) function causes widespread and unexpected changes in the expression of transposons, genes, and 24-nt small RNAs. PLoS Genet 5(11):e1000737
Jovel J, Walker M, Sanfacon H (2007) Recovery of Nicotiana benthamiana plants from a necrotic response induced by a nepovirus is associated with RNA silencing but not with reduced virus titer. J Virol 81:12285–12297
Kapoor M, Arora R, Lama T, Nijhawan A, Khurana JP, Tyagi AK, Kapoor S (2008) Genome-wide identification, organization and phylogenetic analysis of dicer-like, argonaute and RNA-dependent RNA polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genomics 451(9):1471–2164
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Lai EC (2003) microRNAs: Runts of the genome assert themselves. Curr Biol 13:925–936
Lisch D, Carey CC, Dorweiler JE, Chandler VL (2002) A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing. Proc Natl Acad Sci USA 99:6130–6135
Liu B, Li P, Li X, Liu C, Cao S, Chu C, Cao X (2005) Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol 139:296–305
Luo Z, Chen Z (2007) Improperly terminated, unpolyadenylated mRNA of sense transgenes is targeted by RDR6-mediated RNA silencing in Arabidopsis. Plant Cell 19(3):943–958
Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlap** functions with the ARGONAUTE1 gene. Development (UK) 126:469–481
MacRae IJ, Doudna JA (2007) Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Curr Opin Struct Biol 17:138–145
Margis R, Fusaro AF, Smith NA, Curtin SJ, Watson JM, Finnegan EJ, Waterhouse PM (2006) The evolution and diversification of dicers in plants. FEBS Lett 580(10):2442–2450
Matzke M, Kanno T, Huettel B, Daxinger L, Matzke AJ (2007) Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10:512–519
McGinnis KM, Springer C, Lin Y, Carey CC, Chandler V (2006) Transcriptionally silenced transgenes in maize are activated by three mutations defective in paramutation. Genetics 173:1637–1647
Millar AA, Waterhouse PM (2005) Plant and animal microRNAs: similarities and differences. Funct Integr Genomics 5:129–135
Moazed D (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457:413–420
Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel J-B, Jouette D, Lacombe AM, Nikic S, Picault N (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101(5):533–542
Moussian B, Schoof H, Haecker A, Jurgens G, Laux T (1998) Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J 17:1799–1809
Nicholson AW (2003) The ribonuclease III family: forms and functions in RNA maturation, decay, and gene silencing. In: Hannon GJ (ed) RNAi: a guide to gene silencing, vol 8. Cold Spring Harbor Laboratory Press, New York, pp 149–174
Peters L, Meister G (2007) Argonaute proteins: mediators of RNA silencing. Mol Cell 26(8):611–623
Rivas FV, Tolia NH, Song JJ, Aragon JP, Liu J, Hannon GJ, Joshua-Tor L (2005) Purified Argonaute2 and an siRNA form recombinant human RISC. Nat Struct Mol Biol 12(4):340–349
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: Blind men and elephants in Arabidopsis development. Trends Plant Sci 7:487–491
Schmitz RJ, Hong L, Fitzpatrick KE, Amasino RM (2007) DICER-LIKE 1 and DICER-LIKE 3 redundantly act to promote flowering via repression of FLOWERING LOCUS C in Arabidopsis thaliana. Genetics 176:1359–1362
Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115
Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S, Timmons L, Plasterk RH, Fire A (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107(4):465–476
Smardon A, Spoerke JM, Stacey SC, Klein ME, Mackin N, Maine EM (2000) EGO-1 is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans. Curr Biol 10:169–178
Thompson J, Higgins D, Gibson T (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Vaucheret H, Vazquez F, Crete P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18:1187–1197
Wassenegger M, Heimes S, Riedel L, Sanger HL (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell 76(3):567–576
**e Z, Fan B, Chen C, Chen Z (2001) An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc Natl Acad Sci USA 98:6516–6521
**e Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2(5):E104
Yang S, Zhang X, Yue J, Tian D, Chen J (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 280:187–198
Yigit E, Batista PJ, Bei Y, Pang KM, Chen CC, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ, Mello CC (2006) Analysis of the C. elegans Argonaute family reveals that distinct argonautes act sequentially during RNAi. Cell 127(4):747–757
Yu D, Fan B, MacFarlane SA, Chen Z (2003) Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol Plant Microb Interact 16:206–216
Zaratiegui M, Irvine DV, Martienssen RA (2007) Noncoding RNAs and gene silencing. Cell 128:763–776
Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W (2004) Single processing center models for human dicer and bacterial RNase III. Cell 118:57–68
Zilberman D, Cao X, Jacobsen SE (2003) Argonaute 4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:716–719
Zilberman D, Cao X, Johansen LK, **e Z, Carrington JC, Jacobsen SE (2004) Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr Biol 14:1214–1220
Acknowledgments
This study was supported by grants from the National High-Tech Research and Development Program (863 Program) (No. 2008AA10Z408) and the National Natural Science Foundation of China (No. 11075001 and No. 30771309). We wish to thank the two anonymous reviewers for their helpful comments on this manuscript. We also acknowledge Professor Beijiu Cheng for critical reading of the manuscript.
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Communicated by B. Li.
Y. Qian and Y. Cheng contributed equally to this work.
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Qian, Y., Cheng, Y., Cheng, X. et al. Identification and characterization of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in maize. Plant Cell Rep 30, 1347–1363 (2011). https://doi.org/10.1007/s00299-011-1046-6
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DOI: https://doi.org/10.1007/s00299-011-1046-6