IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress

Plant Cell

Volumn 24, Issue 9, 2012, Pages 3590-3602

  Kinoshita, Natsuko ^a,b   Wang, Huan ^a   Kasahara, Hiroyuki ^c   Liu, Jun ^a   MacPherson, Cameron ^a,d   Machida, Yasunori ^b   Kamiya, Yuji ^c   Hannah, Matthew A ^e   Chuaa, Nam Hai ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b NAGOYA UNIVERSITY   (Japan)

^c RIKEN Center for Sustainable Resource Science   (Japan)

^d KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^e Bayer sa nv Belgium   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84868116999     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.097006     Document Type: Article

References (84)

1. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Arenas-Huertero, C., Pérez, B., Rabanal, F., Blanco-Melo, D., De la Rosa, C., Estrada-Navarrete, G., Sanchez, F., Covarrubias, A.A., and Reyes, J.L. (2009). Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol. Biol. 70: 385-401.
3. Aukerman, M.J., and Sakai, H. (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15: 2730-2741.
4. Bartel, D.P. (2004). MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
5. Belin, C., Megies, C., Hauserová, E., and Lopez-Molina, L. (2009). Abscisic acid represses growth of the Arabidopsis embryonic axis after germination by enhancing auxin signaling. Plant Cell 21: 2253-2268.
6. Benková, E., Ivanchenko, M.G., Friml, J., Shishkova, S., and Dubrovsky, J.G. (2009). A morphogenetic trigger: Is there an emerging concept in plant developmental biology? Trends Plant Sci. 14: 189-193.
7. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G., and Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602.
8. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palme, K., and Scheres, B. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44.
9. Bolstad, B.M., Irizarry, R.A., Astrand, M., and Speed, T.P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
10. 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.
11. Campanella, J.J., Larko, D., and Smalley, J. (2003). A molecular phylogenomic analysis of the ILR1-like family of IAA amidohydrolase genes. Comp. Funct. Genomics 4: 584-600.
12. Carrington, J.C., and Ambros, V. (2003). Role of microRNAs in plant and animal development. Science 301: 336-338.
13. Catala, R., Ouyang, J., Abreu, I.A., Hu, Y., Seo, H., Zhang, X., and Chua, N.H. (2007). The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. Plant Cell 19: 2952-2966.
14. Chapman, E.J., and Carrington, J.C. (2007). Specialization and evolution of endogenous small RNA pathways. Nat. Rev. Genet. 8: 884-896.
15. Chen, X. (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303: 2022-2025.
16. Chen, X. (2009). Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25: 21-44.
17. Clayton, D., and Kaldor, J. (1987). Empirical Bayes estimates of agestandardized relative risks for use in disease mapping. Biometrics 43: 671-681.
18. Covarrubias, A.A., and Reyes, J.L. (2010). Post-transcriptional gene regulation of salinity and drought responses by plant microRNAs. Plant Cell Environ. 33: 481-489.
19. Davies, R.T., Goetz, D.H., Lasswell, J., Anderson, M.N., and Bartel, B. (1999). IAR3 encodes an auxin conjugate hydrolase from Arabidopsis. Plant Cell 11: 365-376.
20. De Smet, I., Vanneste, S., Inzé, D., and Beeckman, T. (2006). Lateral root initiation or the birth of a new meristem. Plant Mol. Biol. 60: 871-887.
21. Dharmasiri, N., Dharmasiri, S., and Estelle, M. (2005). The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
22. Dharmasiri, S., and Estelle, M. (2002). The role of regulated protein degradation in auxin response. Plant Mol. Biol. 49: 401-409.
23. Ding, Z., and Friml, J. (2010). Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc. Natl. Acad. Sci. USA 107: 12046-12051.
24. Dubrovsky, J.G., Doerner, P.W., Colón-Carmona, A., and Rost, T.L. (2000). Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiol. 124: 1648-1657.
25. Franco-Zorrilla, J.M., Valli, A., Todesco, M., Mateos, I., Puga, M.I., Rubio-Somoza, I., Leyva, A., Weigel, D., García, J.A., and Paz-Ares, J. (2007). Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39: 1033-1037.
26. Friml, J., Wi-sniewska, J., Benková, E., Mendgen, K., and Palme, K. (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806-809.
27. Fujiwara, T., Hirai, M.Y., Chino, M., Komeda, Y., and Naito, S. (1992). Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia. Plant Physiol. 99: 263-268.
28. Gifford, M.L., Dean, A., Gutierrez, R.A., Coruzzi, G.M., and Birnbaum, K.D. (2008). Cell-specific nitrogen responses mediate developmental plasticity. Proc. Natl. Acad. Sci. USA 105: 803-808.
29. Golden, T.A., Schauer, S.E., Lang, J.D., Pien, S., Mushegian, A.R., Grossniklaus, U., Meinke, D.W., and Ray, A. (2002). SHORT INTEGUMENTS1/SUSPENSOR1/CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol. 130: 808-822.
30. Gonzalez, E., Gordon, A., James, C., and Arreseigor, C. (1995). The role of sucrose synthase in the response of soybean nodules to drought. J. Exp. Bot. 46: 1515-1523.
31. Gálvez, L., González, E.M., and Arrese-Igor, C. (2005). Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J. Exp. Bot. 56: 2551-2561.
32. Han, M.H., Goud, S., Song, L., and Fedoroff, N. (2004). The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc. Natl. Acad. Sci. USA 101: 1093-1098.
33. Hardtke, C.S. (2006). Root development-Branching into novel spheres. Curr. Opin. Plant Biol. 9: 66-71.
34. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., and Speed, T.P. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
35. Jacobsen, S.E., Running, M.P., and Meyerowitz, E.M. (1999). Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126: 5231-5243.
36. Keuskamp, D.H., Pollmann, S., Voesenek, L.A., Peeters, A.J., and Pierik, R. (2010). Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proc. Natl. Acad. Sci. USA 107: 22740-22744.
37. Khan, G.A., Declerck, M., Sorin, C., Hartmann, C., Crespi, M., and Lelandais-Brière, C. (2011). MicroRNAs as regulators of root development and architecture. Plant Mol. Biol. 77: 47-58.
38. Kinoshita, N., Berr, A., Belin, C., Chappuis, R., Nishizawa, N.K., and Lopez-Molina, L. (2010). Identification of growth insensitive to ABA3 (gia3), a recessive mutation affecting ABA signaling for the control of early post-germination growth in Arabidopsis thaliana. Plant Cell Physiol. 51: 239-251.
39. Kutter, C., Schöb, H., Stadler, M., and Meins, F. Jr., and Si-Ammour, A. (2007). MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell 19: 2417-2429.
40. Lafforgue, G., Martínez, F., Sardanyés, J., de la Iglesia, F., Niu, Q.W., Lin, S.S., Solé, R.V., Chua, N.H., Daròs, J.A., and Elena, S.F. (2011). Tempo and mode of plant RNA virus escape from RNA interference-mediated resistance. J. Virol. 85: 9686-9695.
41. LeClere, S., Tellez, R., Rampey, R.A., Matsuda, S.P., and Bartel, B. (2002). Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J. Biol. Chem. 277: 20446-20452.
42. Li, W.X., Oono, Y., Zhu, J., He, X.J., Wu, J.M., Iida, K., Lu, X.Y., Cui, X., Jin, H., and Zhu, J.K. (2008). The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20: 2238-2251.
43. Lin, S.I., Chiang, S.F., Lin, W.Y., Chen, J.W., Tseng, C.Y., Wu, P.C., and Chiou, T.J. (2008). Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol. 147: 732-746.
44. Lin, S.S., Wu, H.W., Elena, S.F., Chen, K.C., Niu, Q.W., Yeh, S.D., Chen, C.C., and Chua, N.H. (2009). Molecular evolution of a viral non-coding sequence under the selective pressure of amiRNAmediated silencing. PLoS Pathog. 5: e1000312.
45. Liu, H.H., Tian, X., Li, Y.J., Wu, C.A., and Zheng, C.C. (2008).Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14: 836-843.
46. Liu, Q., Katou, K., and Okamoto, H. (1992). Effects of exogenous auxin on the regulation of elongation growth of excised segments of vigna hypocotyls under osmotic-stress. Plant Cell Physiol. 33: 915-919.
47. Llave, C., Xie, Z., Kasschau, K.D., and Carrington, J.C. (2002). Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297: 2053-2056.
48. Lobbes, D., Rallapalli, G., Schmidt, D.D., Martin, C., and Clarke, J. (2006). SERRATE: A new player on the plant microRNA scene. EMBO Rep. 7: 1052-1058.
49. Lu, C., and Fedoroff, N. (2000). A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12: 2351-2366.
50. Lynn, K., Fernandez, A., Aida, M., Sedbrook, J., Tasaka, M., Masson, P., and Barton, M.K. (1999). The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126: 469-481.
51. Martin, R.C., Liu, P.P., Goloviznina, N.A., and Nonogaki, H. (2010). microRNA, seeds, and Darwin?: Diverse function of miRNA in seed biology and plant responses to stress. J. Exp. Bot. 61: 2229-2234.
52. Moldovan, D., Spriggs, A., Yang, J., Pogson, B.J., Dennis, E.S., and Wilson, I.W. (2010). Hypoxia-responsive microRNAs and transacting small interfering RNAs in Arabidopsis. J. Exp. Bot. 61: 165-177.
53. Møller, S.G., Kunkel, T., and Chua, N.H. (2001). A plastidic ABC protein involved in intercompartmental communication of light signaling. Genes Dev. 15: 90-103.
54. Montgomery, T.A., and Carrington, J.C. (2008). Splicing and dicing with a SERRATEd edge. Proc. Natl. Acad. Sci. USA 105: 8489-8490.
55. Nag, A., and Jack, T. (2010). Sculpting the flower; the role of microRNAs in flower development. Curr. Top. Dev. Biol. 91: 349-378.
56. Nagpal, P., Ellis, C.M., Weber, H., Ploense, S.E., Barkawi, L.S., Guilfoyle, T.J., Hagen, G., Alonso, J.M., Cohen, J.D., Farmer, E.E., Ecker, J.R., and Reed, J.W. (2005). Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132: 4107-4118.
57. Nonogaki, H. (2010). MicroRNA gene regulation cascades during early stages of plant development. Plant Cell Physiol. 51: 1840-1846.
58. Pant, B.D., Buhtz, A., Kehr, J., and Scheible, W.R. (2008). Micro-RNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 53: 731-738.
59. Parizot, B., et al. (2008). Diarch symmetry of the vascular bundle in Arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation. Plant Physiol. 146: 140-148.
60. Park, W., Li, J., Song, R., Messing, J., and Chen, X. (2002). CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12: 1484-1495.
61. Petricka, J.J., and Benfey, P.N. (2008). Root layers: Complex regulation of developmental patterning. Curr. Opin. Genet. Dev. 18: 354-361.
62. Poethig, R.S. (2009). Small RNAs and developmental timing in plants. Curr. Opin. Genet. Dev. 19: 374-378.
63. Rampey, R.A., LeClere, S., Kowalczyk, M., Ljung, K., Sandberg, G., and Bartel, B. (2004). A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol. 135: 978-988.
64. Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., and Bartel, D.P. (2002). MicroRNAs in plants. Genes Dev. 16: 1616-1626.
65. Reyes, J.L., and Chua, N.H. (2007). ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J. 49: 592-606.
66. Schauer, S.E., Jacobsen, S.E., Meinke, D.W., and Ray, A. (2002). DICER-LIKE1: Blind men and elephants in Arabidopsis development. Trends Plant Sci. 7: 487-491.
67. Shibasaki, K., Uemura, M., Tsurumi, S., and Rahman, A. (2009). Auxin response in Arabidopsis under cold stress: Underlying molecular mechanisms. Plant Cell 21: 3823-3838.
68. Smyth, G.K. (2005). Limma: Linear models for microarray data. In Bioinformatics and Computational Biology Solutions Using R and Bioconductor, C.V.R. Gentleman, S. Dudoit, R. Irizarry, and W. Huber, eds (New York: Springer), pp. 397-420.
69. Sugawara, S., Hishiyama, S., Jikumaru, Y., Hanada, A., Nishimura, T., Koshiba, T., Zhao, Y., Kamiya, Y., and Kasahara, H. (2009). Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc. Natl. Acad. Sci. USA 106: 5430-5435.
70. Sultan, S.E. (2000). Phenotypic plasticity for plant development, function and life history. Trends Plant Sci. 5: 537-542.
71. Sunkar, R., Chinnusamy, V., Zhu, J., and Zhu, J.K. (2007). Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 12: 301-309.
72. Sunkar, R., and Zhu, J.K. (2004). Novel and stress-regulated micro-RNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001-2019.
73. Taniguchi, M., Kiba, T., Sakakibara, H., Ueguchi, C., Mizuno, T., and Sugiyama, T. (1998). Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett. 429: 259-262.
74. Tukey, J.W. (1977). Some thoughts on clinical trials, especially problems of multiplicity. Science 198: 679-684.
75. Vaucheret, H., Vazquez, F., Crété, P., and Bartel, D.P. (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.
76. Vazquez, F., Gasciolli, V., Crété, P., and Vaucheret, H. (2004). The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr. Biol. 14: 346-351.
77. Wang, J.W., Czech, B., and Weigel, D. (2009). miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738-749.
78. Wang, J.W., Park, M.Y., Wang, L.J., Koo, Y., Chen, X.Y., Weigel, D., and Poethig, R.S. (2011). miRNA control of vegetative phase change in trees. PLoS Genet. 7: e1002012.
79. Wang, X.J., Reyes, J.L., Chua, N.H., and Gaasterland, T. (2004). Prediction and identification of Arabidopsis thaliana microRNAs and their mRNA targets. Genome Biol. 5: R65.
80. Wu, G., Park, M.Y., Conway, S.R., Wang, J.W., Weigel, D., and Poethig, R.S. (2009). The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138: 750-759.
81. Wu, M.F., Tian, Q., and Reed, J.W. (2006). Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133: 4211-4218.
82. Yang, L., Liu, Z., Lu, F., Dong, A., and Huang, H. (2006). SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J. 47: 841-850.
83. Zhao, B., Liang, R., Ge, L., Li, W., Xiao, H., Lin, H., Ruan, K., and Jin, Y. (2007). Identification of drought-induced microRNAs in rice. Biochem. Biophys. Res. Commun. 354: 585-590.
84. Zuo, J., Niu, Q.W., and Chua, N.H. (2000). Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24: 265-273.