Deregulation of the OsmiR160 target gene OsARF18 causes growth and developmental defects with an alteration of auxin signaling in rice

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Huang, Jian ^a   Li, Zhiyong ^a   Zhao, Dazhong ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INDOLEACETIC ACID DERIVATIVE; MICRORNA; PLANT PROTEIN;

CELL DIFFERENTIATION; CELL DIVISION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; ORYZA; PHENOTYPE; PLANT LEAF; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

CELL DIFFERENTIATION; CELL DIVISION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; MICRORNAS; ORYZA; PHENOTYPE; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84979231470     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep29938     Document Type: Article

References (65)

1. Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
2. Carrington, J. C. & Ambros, V. Role of microRNAs in plant and animal development. Science 301, 336-338 (2003).
3. Jones-Rhoades, M. W., Bartel, D. P. & Bartel, B. MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19-53 (2006).
4. Voinnet, O. Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687 (2009).
5. Rogers, K. & Chen, X. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25, 2383-2399 (2013).
6. Liu, X. et al. The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in MicroRNA160a, in organogenesis and the mechanism regulating its expression. Plant J. 62, 416-428 (2010).
7. Todesco, M., Rubio-Somoza, I., Paz-Ares, J. & Weigel, D. A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. Plos Genet. 6, e1001031 (2010).
8. Yan, J. et al. Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24, 415-427 (2012).
9. Liu, B. et al. Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol. 139, 296-305 (2005).
10. Song, X. et al. Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. 69, 462-474 (2012).
11. Liu, B. et al. Oryza sativa dicer-like4 reveals a key role for small interfering RNA silencing in plant development. Plant Cell 19, 2705-2718 (2007).
12. Nonomura, K. I. et al. A germ cell-specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19, 2583-2594 (2007).
13. Abe, M. et al. WAVY LEAF1, an ortholog of Arabidopsis HEN1, regulates shoot development by maintaining MicroRNA and transacting small interfering RNA accumulation in rice. Plant Physiol. 154, 1335-1346 (2010).
14. Jiao, Y. et al. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nature Genet. 42, 541-544 (2010).
15. Wang, S. et al. Control of grain size, shape and quality by OsSPL16 in rice. Nature Genet. 44, 950-954 (2012).
16. Xie, K. et al. Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiol. 158, 1382-1394 (2012).
17. Zhu, Q. H., Upadhyaya, N. M., Gubler, F. & Helliwell, C. A. Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol. 9, 149 (2009).
18. Lee, D. Y. & An, G. Two AP2 family genes, supernumerary bract (SNB) and Osindeterminate spikelet 1 (OsIDS1), synergistically control inflorescence architecture and floral meristem establishment in rice. Plant J 69, 445-461 (2012).
19. Bian, H. et al. Distinctive expression patterns and roles of the miRNA393/TIR1 homolog module in regulating flag leaf inclination and primary and crown root growth in rice (Oryza sativa). New Phytol. 196, 149-161 (2012).
20. Sunkar, R., Girke, T., Jain, P. K. & Zhu, J. K. Cloning and characterization of microRNAs from rice. Plant Cell 17, 1397-1411 (2005).
21. Jeong, D. H. et al. Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23, 4185-4207 (2011).
22. Wang, J. W. et al. Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17, 2204-2216 (2005).
23. Mallory, A. C., Bartel, D. P. & Bartel, B. 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 (2005).
24. Liu, P. P. et al. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J. 52, 133-146 (2007).
25. Liu, X. et al. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc. Natl. Acad. Sci. USA 110, 15485-15490 (2013).
26. Hendelman, A., Buxdorf, K., Stav, R., Kravchik, M. & Arazi, T. Inhibition of lamina outgrowth following Solanum lycopersicum AUXIN RESPONSE FACTOR 10 (SlARF10) derepression. Plant Mol. Biol. 78, 561-576 (2012).
27. Damodharan, S., Zhao, D. & Arazi, T. A common miRNA160-based mechanism regulates ovary patterning, floral organ abscission and lamina outgrowth in tomato. Plant J. doi: 10.1111/tpj.13127 (2016).
28. Turner, M. et al. Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiol. 162, 2042-2055 (2013).
29. Axtell, M. J., Snyder, J. A. & Bartel, D. P. Common functions for diverse small RNAs of land plants. Plant Cell 19, 1750-1769 (2007).
30. Luo, Y., Guo, Z. & Li, L. Evolutionary conservation of microRNA regulatory programs in plant flower development. Dev. Biol. 380, 133-144 (2013).
31. Dai, X. & Zhao, P. X. psRNATarget: a plant small RNA target analysis server. Nucleic Acids. Res. 39, W155-159 (2011).
32. Li, Y. F. et al. Transcriptome-wide identification of microRNA targets in rice. Plant J. 62, 742-759 (2010).
33. Zhang, G. H., Xu, Q., Zhu, X. D., Qian, Q. & Xue, H. W. SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21, 719-735 (2009).
34. Wang, D. et al. Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394, 13-24 (2007).
35. Zhao, S. Q., Xiang, J. J. & Xue, H. W. Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control. Mol. Plant 6, 174-187 (2013).
36. Chhun, T. et al. Saturated humidity accelerates lateral root development in rice (Oryza sativa L.) seedlings by increasing phloembased auxin transport. J. Exp. Bot. 58, 1695-1704 (2007).
37. Li, G. et al. Rice actin-binding protein RMD is a key link in the auxin-actin regulatory loop that controls cell growth. Proc. Natl. Acad. Sci. USA 111, 10377-10382 (2014).
38. Yamamoto, Y., Kamiya, N., Morinaka, Y., Matsuoka, M. & Sazuka, T. Auxin biosynthesis by the YUCCA genes in rice. Plant Physiol. 143, 1362-1371 (2007).
39. Vanneste, S. & Friml, J. Auxin: a trigger for change in plant development. Cell 136, 1005-1016 (2009).
40. Woo, Y. M. et al. Constitutively wilted 1, a member of the rice YUCCA gene family, is required for maintaining water homeostasis and an appropriate root to shoot ratio. Plant Mol. Biol. 65, 125-136 (2007).
41. Fujino, K. et al. NARROW LEAF 7 controls leaf shape mediated by auxin in rice. Mol Genet. Genomics 279, 499-507 (2008).
42. Baker, C. C., Sieber, P., Wellmer, F. & Meyerowitz, E. M. The early extra petals1 mutant uncovers a role for MicroRNA miR164c in regulating petal number in Arabidopsis. Curr. Biol. 15, 303-315 (2005).
43. Koyama, T., Furutani, M., Tasaka, M. & Ohme-Takagi, M. TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. Plant Cell 19, 473-484 (2007).
44. Chen, X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 2022-2025 (2004).
45. Liu, H. et al. OsmiR396d-regulated OsGRFs function in floral organogenesis in rice through binding to their targets OsJMJ706 and OsCR4. Plant Physiol. 165, 160-174 (2014).
46. Itoh, J., Hibara, K., Sato, Y. & Nagato, Y. Developmental role and auxin responsiveness of Class III homeodomain leucine zipper gene family members in rice. Plant Physiol. 147, 1960-1975 (2008).
47. Williams, L., Carles, C. C., Osmont, K. S. & Fletcher, J. C. A database analysis method identifies an endogenous trans-acting shortinterfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc. Natl. Acad. Sci. USA 102, 9703-9708 (2005).
48. Fahlgren, N. et al. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr. Biol. 16, 939-944 (2006).
49. Chitwood, D. H. et al. Pattern formation via small RNA mobility. Genes Dev. 23, 549-554 (2009).
50. Marin, E. et al. miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22, 1104-1117 (2010).
51. Wu, M. F., Tian, Q. & Reed, J. W. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211-4218 (2006).
52. Guilfoyle, T. J. & Hagen, G. Auxin response factors. Curr. Opin. Plant Biol. 10, 453-460 (2007).
53. Shen, C. et al. Functional analysis of the structural domain of ARF proteins in rice (Oryza sativa L.). J. Exp. Bot. 61, 3971-3981 (2010).
54. Nagasaki, H. et al. The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc. Natl. Acad. Sci. USA 104, 14867-14871 (2007).
55. Dharmasiri, N., Dharmasiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445 (2005).
56. Tan, X. et al. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640-645 (2007).
57. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. Activation and repression of transcription by auxin-response factors. Proc. Natl. Acad. Sci. USA 96, 5844-5849 (1999).
58. Wang, S., Tiwari, S. B., Hagen, G. & Guilfoyle, T. J. AUXIN RESPONSE FACTOR7 restores the expression of auxin-responsive genes in mutant Arabidopsis leaf mesophyll protoplasts. Plant Cell 17, 1979-1993 (2005).
59. Boer, D. R. et al. Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 156, 577-589 (2014).
60. Gutierrez, L. et al. Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21, 3119-3132 (2009).
61. Zhang, B. MicroRNA: a new target for improving plant tolerance to abiotic stress. J. Exp. Bot. 66, 1749-1761 (2015).
62. Zhou, M. & Luo, H. MicroRNA-mediated gene regulation: potential applications for plant genetic engineering. Plant Mol. Biol. 83, 59-75 (2013).
63. Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271-282 (1994).
64. Jia, G., Liu, X., Owen, H. A. & Zhao, D. Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc. Natl. Acad. Sci. USA 105, 2220-2225 (2008).
65. Zhao, D. Z., Wang, G. F., Speal, B. & Ma, H. The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16, 2021-2031 (2002).