Abstract
MicroRNAs (miRNAs) are small RNA molecules recognized as important regulators of gene expression. Although plant miRNAs have been extensively studied in model systems, less is known in other plants with limited genome sequence data. We are interested in the identification of miRNAs in Phaseolus vulgaris (common bean) to uncover different plant strategies to cope with adverse conditions and because of its relevance as a crop in develo** countries. Here we present the identification of conserved and candidate novel miRNAs in P. vulgaris present in different organs and growth conditions, including drought, abscisic acid treatment, and Rhizobium infection. We also identified cDNA sequences in public databases that represent the corresponding miRNA precursors. In addition, we predicted and validated target mRNAs amongst reported EST and cDNAs for P. vulgaris. We propose that the novel miRNAs present in common bean and other legumes, are involved in regulation of legume-specific processes including adaptation to diverse external cues.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen E, **e 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. doi:10.1038/ng1478
Allen E, **e Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221. doi:10.1016/j.cell.2005.04.004
Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17:1658–1673. doi:10.1105/tpc.105.032185
Barakat A, Wall K, Leebens-Mack J, Wang YJ, Carlson JE, Depamphilis CW (2007) Large-scale identification of microRNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. Plant J 51:991–1003. doi:10.1111/j.1365-313X.2007.03197.x
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. doi:10.1016/S0092-8674(04)00045-5
Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6–24. doi:10.1104/pp.108.120725
Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T, Moreau S, Niebel A, Frickey T, Weiller G, He J, Dai X, Zhao PX, Tang Y, Udvardi MK (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55:504–513
Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54:876–887. doi:10.1111/j.1365-313X.2008.03448.x
Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54. doi:10.1016/S1360-1385(97)82562-9
Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190. doi:10.1126/science.1159151
Colmenero-Flores JM, Campos F, Garciarrubio A, Covarrubias AA (1997) Characterization of Phaseolus vulgaris cDNA clones responsive to water deficit: identification of a novel late embryogenesis abundant-like protein. Plant Mol Biol 35:393–405. doi:10.1023/A:1005802505731
Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernie T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20:3084–3088. doi:10.1101/gad.402806
Dezulian T, Palatnik JF, Huson DH, Weigel D (2005) Conservation and divergence of microRNA families in plants. Genome Biol 6:13. doi:10.1186/gb-2005-6-11-p13
Elbashir SM, Lendeckel W, Tuschl T (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15:188–200. doi:10.1101/gad.862301
Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2:e219. doi:10.1371/journal.pone.0000219
Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043. doi:10.1016/j.cub.2005.10.016
Gresshoff PM (2003) Post-genomic insights into plant nodulation symbioses. Genome Biol 4:201. doi:10.1186/gb-2003-4-1-201
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. doi:10.1093/nar/gkj112
Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351. doi:10.1016/j.tplants.2007.06.013
John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS (2004) Human microRNA targets. PLoS Biol 2:e363. doi:10.1371/journal.pbio.0020363
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799. doi:10.1016/j.molcel.2004.05.027
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53. doi:10.1146/annurev.arplant.57.032905.105218
Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC (2004) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88. doi:10.1038/nature02363
Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, ** H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251. doi:10.1105/tpc.108.059444
Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619. doi:10.1105/tpc.003210
Lu C, Meyers BC, Green PJ (2007a) Construction of small RNA cDNA libraries for deep sequencing. Methods 43:110–117. doi:10.1016/j.ymeth.2007.05.002
Lu S, Sun YH, Amerson H, Chiang VL (2007b) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J 51:1077–1098. doi:10.1111/j.1365-313X.2007.03208.x
Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55:131–151
Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK (2008) Criteria for annotation of plant microRNAs. Plant Cell 20:3186–3190
Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447:1126–1129. doi:10.1038/nature05903
Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141. doi:10.1016/j.cell.2008.02.033
Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217. doi:10.1006/jmbi.2000.4042
Okamura K, Phillips MD, Tyler DM, Duan H, Chou YT, Lai EC (2008) The regulatory activity of microRNA* species has substantial influence on microRNA and 3′ UTR evolution. Nat Struct Mol Biol 15:354–363. doi:10.1038/nsmb.1409
Pandey SP, Shahi P, Gase K, Baldwin IT (2008) Herbivory-induced changes in the small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata. Proc Natl Acad Sci USA 105:4559–4564. doi:10.1073/pnas.0711363105
Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425. doi:10.1101/gad.1476406
Ramanjulu S, Bartels D (2002) Drought- and desiccation-induced modulation of gene expression in plants. Plant Cell Environ 25:141–151. doi:10.1046/j.0016-8025.2001.00764.x
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. doi:10.1111/j.1365-313X.2006.02980.x
Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520. doi:10.1016/S0092-8674(02)00863-2
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009. doi:10.1006/bbrc.2001.6299
Sanchez DH, Lippold F, Redestig H, Hannah MA, Erban A, Kramer U, Kopka J, Udvardi MK (2008) Integrative functional genomics of salt acclimatization in the model legume Lotus japonicus. Plant J 53:973–987. doi:10.1111/j.1365-313X.2007.03381.x
Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Annu Rev Genet 32:33–57. doi:10.1146/annurev.genet.32.1.33
Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527. doi:10.1016/j.devcel.2005.01.018
Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109–112. doi:10.1126/science.1077937
Subramanian S, Fu Y, Sunkar R, Barbazuk WB, Zhu JK, Yu O (2008) Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 9:160. doi:10.1186/1471-2164-9-160
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019. doi:10.1105/tpc.104.022830
Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25. doi:10.1186/1471-2229-8-25
Szittya G, Moxon S, Santos DM, **g R, Fevereiro MP, Moulton V, Dalmay T (2008) High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 9:593. doi:10.1186/1471-2164-9-593
Valdes-Lopez O, Arenas-Huertero C, Ramirez M, Girard L, Sanchez F, Vance CP, Reyes JL, Hernandez G (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus deficiency signaling in common bean roots. Plant Cell Environ 31:1834–1843
Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771. doi:10.1101/gad.1410506
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. doi:10.1242/dev.02602
**ong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165–S183. doi:10.1105/tpc.010278
Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94. doi:10.1016/j.tplants.2004.12.012
Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8:R96. doi:10.1186/gb-2007-8-6-r96
Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46:243–259. doi:10.1111/j.1365-313X.2006.02697.x
Zhao B, Liang R, Ge L, Li W, **ao H, Lin H, Ruan K, ** Y (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590. doi:10.1016/j.bbrc.2007.01.022
Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W (2008a) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1779:780–788
Zhou ZS, Huang SQ, Yang ZM (2008b) Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochem Biophys Res Commun 374:538–542. doi:10.1016/j.bbrc.2008.07.083
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415. doi:10.1093/nar/gkg595
Acknowledgments
We thank the help of Jerome Verleyen and Roberto Rodríguez during the early phases of sequence analysis. This work was supported by grants from CONACyT, Mexico (J48740) and DGAPA-UNAM (IN-227706) to JLR, and JLR and AAC, respectively.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Arenas-Huertero, C., Pérez, B., Rabanal, F. et al. Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70, 385–401 (2009). https://doi.org/10.1007/s11103-009-9480-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-009-9480-3