Multi-gene silencing in Arabidopsis: A collection of artificial microRNAs targeting groups of paralogs encoding transcription factors

Plant Journal

Volumn 80, Issue 1, 2014, Pages 149-160

  Jover Gil, Sara ^a   Paz Ares, Javier ^b   Micol, José Luis ^a   Ponce, María Rosa ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b CSIC   (Spain)

Author keywords

Arabidopsis; Artificial microRNAs; Functional genomics tools; Functional redundancy; Gene redundancy; Tandem paralogs

Indexed keywords

ENCODING (SYMBOLS); PLANTS (BOTANY); REDUNDANCY; RNA; SIGNAL ENCODING; TRANSCRIPTION FACTORS;

ARABIDOPSIS; FUNCTIONAL GENOMICS; FUNCTIONAL REDUNDANCY; MICRORNAS; PARALOGS;

TRANSCRIPTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; MICRORNA; TRANSCRIPTION FACTOR;

ARABIDOPSIS; FLOWER; GENE SILENCING; GENETICS; GENOMICS; METABOLISM; PHENOTYPE; PLANT LEAF; SEEDLING; TRANSGENE; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; GENE SILENCING; GENOMICS; MICRORNAS; PHENOTYPE; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; SEEDLING; TRANSCRIPTION FACTORS; TRANSGENES;

EID: 84924756195     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12609     Document Type: Article

References (57)

1. Alvarez, J.P., Pekker, I., Goldshmidt, A., Blum, E., Amsellem, Z. and Eshed, Y. (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell, 18, 1134-1151.
2. Berna, G., Robles, P. and Micol, J.L. (1999) A mutational analysis of leaf morphogenesis in Arabidopsis thaliana. Genetics, 152, 729-742.
3. Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M. and Benning, C. (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17, 170-180.
4. Bolle, C., Huep, G., Kleinbolting, N., Haberer, G., Mayer, K., Leister, D. and Weisshaar, B. (2013) GABI-DUPLO: a collection of double mutants to overcome genetic redundancy in Arabidopsis thaliana. Plant J. 75, 157-171.
5. Bowman, J.L., Smyth, D.R. and Meyerowitz, E.M. (1989) Genes directing flower development in Arabidopsis. Plant Cell, 1, 37-52.
6. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y.Y., Sieburth, L. and Voinnet, O. (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science, 320, 1185-1190.
7. Cheng, X.F. and Wang, Z.Y. (2005) Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J. 43, 758-768.
8. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
9. Cnops, G., Jover-Gil, S., Peters, J.L., Neyt, P., De Block, S., Robles, P., Ponce, M.R., Gerats, T., Micol, J.L. and Van Lijsebettens, M. (2004) The rotunda2 mutants identify a role for the LEUNIG gene in vegetative leaf morphogenesis. J. Exp. Bot. 55, 1529-1539.
10. Curtis, M.D. and Grossniklaus, U. (2003) A Gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
11. Dai, X. and Zhao, P.X. (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res. 39, W155-W159.
12. Davuluri, R.V., Sun, H., Palaniswamy, S.K., Matthews, N., Molina, C., Kurtz, M. and Grotewold, E. (2003) AGRIS: Arabidopsis gene regulatory information server, an information resource of Arabidopsis cis-regulatory elements and transcription factors. BMC Bioinformatics, 4, 25.
13. Dorca-Fornell, C., Gregis, V., Grandi, V., Coupland, G., Colombo, L. and Kater, M.M. (2011) The Arabidopsis SOC1-like genes AGL42, AGL71 and AGL72 promote flowering in the shoot apical and axillary meristems. Plant J. 67, 1006-1017.
14. Dugas, D.V. and Bartel, B. (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol. Biol. 67, 403-417.
15. Eriksson, M.E., Hanano, S., Southern, M.M., Hall, A. and Millar, A.J. (2003) Response regulator homologues have complementary, light-dependent functions in the Arabidopsis circadian clock. Planta, 218, 159-162.
16. Fernandez, A.I., Viron, N., Alhagdow, M. et al. (2009) Flexible tools for gene expression and silencing in tomato. Plant Physiol. 151, 1729-1740.
17. Ferrandez-Ayela, A., Alonso-Peral, M.M., Sanchez-Garcia, A.B., Micol-Ponce, R., Perez-Perez, J.M., Micol, J.L. and Ponce, M.R. (2013a) Arabidopsis TRANSCURVATA1 encodes NUP58, a component of the nucleopore central channel. PLoS One, 8, e67661.
18. Ferrandez-Ayela, A., Micol-Ponce, R., Sanchez-Garcia, A.B., Alonso-Peral, M.M., Micol, J.L. and Ponce, M.R. (2013b) Mutation of an Arabidopsis NatB N-a-terminal acetylation complex component causes pleiotropic developmental defects. PLoS One, 8, e80697.
19. Ferrandiz, C., Liljegren, S.J. and Yanofsky, M.F. (2000) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science, 289, 436-438.
20. Guo, A., He, K., Liu, D., Bai, S., Gu, X., Wei, L. and Luo, J. (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics, 21, 2568-2569.
21. Hauser, F., Chen, W., Deinlein, U., Chang, K., Ossowski, S., Fitz, J., Hannon, G.J. and Schroeder, J.I. (2013) A genomic-scale artificial microRNA library as a tool to investigate the functionally redundant gene space in Arabidopsis. Plant Cell, 25, 2848-2863.
22. Horiguchi, G., Molla-Morales, A., Perez-Perez, J.M., Kojima, K., Robles, P., Ponce, M.R., Micol, J.L. and Tsukaya, H. (2011) Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. Plant J. 65, 724-736.
23. Hulskamp, M., Misra, S. and Jurgens, G. (1994) Genetic dissection of trichome cell development in Arabidopsis. Cell, 76, 555-566.
24. Iida, K., Seki, M., Sakurai, T., Satou, M., Akiyama, K., Toyoda, T., Konagaya, A. and Shinozaki, K. (2005) RARTF: database and tools for complete sets of Arabidopsis transcription factors. DNA Res. 12, 247-256.
25. Ito, S., Matsushika, A., Yamada, H., Sato, S., Kato, T., Tabata, S., Yamashino, T. and Mizuno, T. (2003) Characterization of the APRR9 pseudo-response regulator belonging to the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol. 44, 1237-1245.
26. Jover-Gil, S., Candela, H., Robles, P., Aguilera, V., Barrero, J.M., Micol, J.L. and Ponce, M.R. (2012) The microRNA pathway genes AGO1, HEN1 and HYL1 participate in leaf proximal-distal, venation and stomatal patterning in Arabidopsis. Plant Cell Physiol. 53, 1322-1333.
27. Kumimoto, R.W., Zhang, Y., Siefers, N. and Holt, B.F. 3rd (2010) NF-YC3, NF-YC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. Plant J. 63, 379-391.
28. Lanet, E., Delannoy, E., Sormani, R., Floris, M., Brodersen, P., Crete, P., Voinnet, O. and Robaglia, C. (2009) Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell, 21, 1762-1768.
29. Lechner, E., Leonhardt, N., Eisler, H., Parmentier, Y., Alioua, M., Jacquet, H., Leung, J. and Genschik, P. (2011) MATH/BTB CRL3 receptors target the homeodomain-leucine zipper ATHB6 to modulate abscisic acid signaling. Dev. Cell, 21, 1116-1128.
30. Li, Y., Zheng, L., Corke, F., Smith, C. and Bevan, M.W. (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev. 22, 1331-1336.
31. Lloyd, J. and Meinke, D. (2012) A comprehensive dataset of genes with a loss-of-function mutant phenotype in Arabidopsis. Plant Physiol. 158, 1115-1129.
32. Martienssen, R. and Irish, V. (1999) Copying out our ABCs: the role of gene redundancy in interpreting genetic hierarchies. Trends Genet. 15, 435-437.
33. Michael, T.P., Salome, P.A., Yu, H.J., Spencer, T.R., Sharp, E.L., McPeek, M.A., Alonso, J.M., Ecker, J.R. and McClung, C.R. (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science, 302, 1049-1053.
34. Micol, J.L. (2009) Leaf development: time to turn over a new leaf? Curr. Opin. Plant Biol. 12, 9-16.
35. Monfared, M.M., Simon, M.K., Meister, R.J., Roig-Villanova, I., Kooiker, M., Colombo, L., Fletcher, J.C. and Gasser, C.S. (2011) Overlapping and antagonistic activities of BASIC PENTACYSTEINE genes affect a range of developmental processes in Arabidopsis. Plant J. 66, 1020-1031.
36. Nakamichi, N., Kita, M., Ito, S., Sato, E., Yamashino, T. and Mizuno, T. (2005) The Arabidopsis pseudo-response regulators, PRR5 and PRR7, coordinately play essential roles for circadian clock function. Plant Cell Physiol. 46, 609-619.
37. Nakamichi, N., Kiba, T., Henriques, R., Mizuno, T., Chua, N.H. and Sakakibara, H. (2010) PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell, 22, 594-605.
38. Ochando, I., Jover-Gil, S., Ripoll, J.J., Candela, H., Vera, A., Ponce, M.R., Martinez-Laborda, A. and Micol, J.L. (2006) Mutations in the microRNA complementarity site of the INCURVATA4 gene perturb meristem function and adaxialize lateral organs in Arabidopsis. Plant Physiol. 141, 607-619.
39. Ossowski, S., Schwab, R. and Weigel, D. (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 53, 674-690.
40. Palatnik, J.F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J.C. and Weigel, D. (2003) Control of leaf morphogenesis by microRNAs. Nature, 425, 257-263.
41. Parenicova, L., de Folter, S., Kieffer, M. et al. (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell, 15, 1538-1551.
42. Perez-Perez, J.M., Ponce, M.R. and Micol, J.L. (2002) The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis. Dev. Biol. 242, 161-173.
43. Perez-Perez, J.M., Ponce, M.R. and Micol, J.L. (2004) The ULTRACURVATA2 gene of Arabidopsis encodes an FK506-binding protein involved in auxin and brassinosteroid signaling. Plant Physiol. 134, 101-117.
44. Perez-Perez, J.M., Candela, H. and Micol, J.L. (2009) Understanding synergy in genetic interactions. Trends Genet. 25, 368-376.
45. Pomeranz, M.C., Hah, C., Lin, P.C., Kang, S.G., Finer, J.J., Blackshear, P.J. and Jang, J.C. (2010) The Arabidopsis tandem zinc finger protein AtTZF1 traffics between the nucleus and cytoplasmic foci and binds both DNA and RNA. Plant Physiol. 152, 151-165.
46. Ponce, M.R., Quesada, V. and Micol, J.L. (1998) Rapid discrimination of sequences flanking and within T-DNA insertions in the Arabidopsis genome. Plant J. 14, 497-501.
47. Quesada, V., Ponce, M.R. and Micol, J.L. (1999) OTC and AUL1, two convergent and overlapping genes in the nuclear genome of Arabidopsis thaliana. FEBS Lett. 461, 101-106.
48. Riano-Pachon, D.M., Ruzicic, S., Dreyer, I. and Mueller-Roeber, B. (2007) PlnTFDB: an integrative plant transcription factor database. BMC Bioinformatics, 8, 42.
49. Schmittgen, T.D. and Livak, K.J. (2008) Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101-1108.
50. Schwab, R., Palatnik, J.F., Riester, M., Schommer, C., Schmid, M. and Weigel, D. (2005) Specific effects of microRNAs on the plant transcriptome. Dev. Cell, 8, 517-527.
51. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. and Weigel, D. (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell, 18, 1121-1133.
52. Serrano-Cartagena, J., Candela, H., Robles, P., Ponce, M.R., Perez-Perez, J.M., Piqueras, P. and Micol, J.L. (2000) Genetic analysis of incurvata mutants reveals three independent genetic operations at work in Arabidopsis leaf morphogenesis. Genetics, 156, 1363-1377.
53. Stracke, R., Werber, M. and Weisshaar, B. (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4, 447-456.
54. Tang, H., Bowers, J.E., Wang, X., Ming, R., Alam, M. and Paterson, A.H. (2008) Synteny and collinearity in plant genomes. Science, 320, 486-488.
55. Teng, S., Keurentjes, J., Bentsink, L., Koornneef, M. and Smeekens, S. (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol. 139, 1840-1852.
56. White, D.W. (2006) PEAPOD regulates lamina size and curvature in Arabidopsis. Proc. Natl Acad. Sci. USA, 103, 13238-13243.
57. Zhang, Y. (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res. 33, W701-W704.