Genome-wide identification and expression analysis of auxin response factor gene family in Medicago truncatula

Frontiers in Plant Science

Volumn 6, Issue FEB, 2015, Pages

  Shen, Chenjia ^a   Yue, Runqing ^b   Sun, Tao ^a   Zhang, Lei ^c   Xu, Luqin ^a   Tie, Shuanggui ^b   Wang, Huizhong ^a   Yang, Yanjun ^a  

^a HANGZHOU NORMAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Auxin; Auxin response factor (ARF); Auxin signaling; Nodule formation; Sinorhizobium meliloti infection

Indexed keywords

MEDICAGO TRUNCATULA; SINORHIZOBIUM MELILOTI;

EID: 84925152896     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00073     Document Type: Article

References (54)

1. Aya, K., Hobo, T., Sato-Izawa, K., Ueguchi-Tanaka, M., Kitano, H., and Matsuoka, M. (2014). A novel AP2-type transcription factor, SMALL ORGAN SIZE1, controls organ size downstream of an auxin signaling pathway. Plant Cell Physiol. 55, 897-912. doi: 10.1093/pcp/pcu023
2. Bazin, J., Bustos-Sanmamed, P., Hartmann, C., Lelandais-Briere, C., and Crespi, M. (2012). Complexity of miRNA-dependent regulation in root symbiosis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1570-1579. doi: 10.1098/rstb.2011.0228
3. Berendzen, K. W., Weiste, C., Wanke, D., Kilian, J., Harter, K., and Droge-Laser, W. (2012). Bioinformatic cis-element analyses performed in Arabidopsis and rice disclose bZIP- and MYB-related binding sites as potential AuxRE-coupling elements in auxin-mediated transcription. BMC Plant Biol. 12:125. doi: 10.1186/1471-2229-12-125
4. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., et al. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39-44. doi: 10.1038/nature03184
5. Bowers, J. E., Chapman, B. A., Rong, J., and Paterson, A. H. (2003). Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422, 433-438. doi: 10.1038/nature01521
6. Chapman, E. J., Greenham, K., Castillejo, C., Sartor, R., Bialy, A., Sun, T. P., et al. (2012). Hypocotyl transcriptome reveals auxin regulation of growth-promoting genes through GA-dependent and -independent pathways. PLoS ONE7:e36210. doi: 10.1371/journal.pone.0036210
7. Chen, C., Ane, J. M., and Zhu, H. (2008). OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice. New Phytol. 180, 311-315. doi: 10.1111/j.1469-8137.2008.02612.x
8. Cho, H., Ryu, H., Rho, S., Hill, K., Smith, S., Audenaert, D., et al. (2014). A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nat. Cell Biol. 16, 66-76. doi: 10.1038/ncb2893
9. Chung, Y., Maharjan, P. M., Lee, O., Fujioka, S., Jang, S., Kim, B., et al. (2011). Auxin stimulates DWARF4expression and brassinosteroid biosynthesis in Arabidopsis. Plant J. 66, 564-578. doi: 10.1111/j.1365-313X.2011.04513.x
10. Engstrom, M., Ehrhardt, W., Mitra, M., and Long, R. (2002). Pharmacological analysis of nod factor-induced calcium spiking in Medicago truncatula. Evidence for the requirement of type IIA calcium pumps and phosphoinositide signaling. Plant Physiol. 128, 1390-1401. doi: 10.1104/pp.010691
11. Fang, Y., You, J., Xie, K., Xie, W., and Xiong, L. (2008). Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol. Genet. Genomics 280, 547-563. doi: 10.1007/s00438-008-0386-6
12. Godiard, L., Niebel, A., Micheli, F., Gouzy, J., Ott, T., and Gamas, P. (2007). Identification of new potential regulators of the Medicago truncatula-Sinorhizobium meliloti symbiosis using a large-scale suppression subtractive hybridization approach. Mol. Plant Microbe Interact. 20, 321-332. doi: 10.1094/MPMI-20-3-0321
13. Goetz, M., Vivian-Smith, A., Johnson, S. D., and Koltunow, A. M. (2006). AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 18, 1873-1886. doi: 10.1105/tpc.105.037192
14. Guilfoyle, T. J., and Hagen, G. (2007). Auxin response factors. Curr. Opin. Plant Biol. 10, 453-460. doi: 10.1016/j.pbi.2007.08.014
15. Hardtke, C. S., and Berleth, T. (1998). The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405-1411. doi: 10.1093/emboj/17.5.1405
16. Harper, R. M., Stowe-Evans, E. L., Luesse, D. R., Muto, H., Tatematsu, K., Watahiki, M. K., et al. (2000). The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsistissue. Plant Cell 12, 757-770. doi: 10.1105/tpc.12.5.757
17. Hayashi, K. (2012). The interaction and integration of auxin signaling components. Plant Cell Physiol. 53, 965-975. doi: 10.1093/pcp/pcs035
18. Kalluri, U. C., Difazio, S. P., Brunner, A. M., and Tuskan, G. A. (2007). Genome-wide analysis of Aux/IAA and ARFgene families in Populus trichocarpa. BMC Plant Biol. 7:59. doi: 10.1186/1471-2229-7-59
19. Kondorosi, E., Redondo-Nieto, M., and Kondorosi, A. (2005). Ubiquitin-mediated proteolysis. To be in the right place at the right moment during nodule development. Plant Physiol. 137, 1197-1204. doi: 10.1104/pp.105.060004
20. Li, H., Johnson, P., Stepanova, A., Alonso, J. M., and Ecker, J. R. (2004), Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev. Cell 7, 193-204. doi: 10.1016/j.devcel.2004.07.002
21. Li, X., Lei, M., Yan, Z., Wang, Q., Chen, A., Sun, J., et al. (2013). The REL3-mediated TAS3 ta-siRNA pathway integrates auxin and ethylene signaling to regulate nodulation in Lotus japonicus. New Phytol. 201, 531-544. doi: 10.1111/nph.12550
22. Liu, P. P., Montgomery, T. A., Fahlgren, N., Kasschau, K. D., Nonogaki, H., and Carrington, J. C. (2007). Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages.Plant J. 52, 133-146. doi: 10.1111/j.1365-313X.2007.03218.x
23. Madsen, L. H., Tirichine, L., Jurkiewicz, A., Sullivan, J. T., Heckmann, A. B., Bek, A. S., et al. (2010). The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Commun. 1, 10. doi: 10.1038/ncomms1009
24. Mathesius, U., Schlaman, H. R., Spaink, H. P., Of Sautter, C., Rolfe, B. G., and Djordjevic, M. A. (1998). Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J. 14, 23-34. doi: 10.1046/j.1365-313X.1998.00090.x
25. Messinese, E., Mun, J. H., Yeun, L. H., Jayaraman, D., Rouge, P., Barre, A., et al. (2007). A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol. Plant Microbe Interact. 20, 912-921. doi: 10.1094/MPMI-20-8-0912
26. Molesini, B., Cecconi, D., Pii, Y., and Pandolfini, T. (2014). Local and systemic proteomic changes in Medicago truncatula at an early phase of Sinorhizobium meliloti infection. J. Proteome Res. 13, 408-421. doi: 10.1021/pr4009942
27. Mun, J. H., Yu, H. J., Shin, J. Y., Oh, M., Hwang, H. J., and Chung, H. (2012). Auxin response factor gene family inBrassica rapa: genomic organization, divergence, expression, and evolution. Mol. Genet. Genomics 287, 765-784. doi: 10.1007/s00438-012-0718-4
28. Nallu, S., Silverstein, K. A., Samac, D. A., Bucciarelli, B., Vance, C. P., and VandenBosch, K. A. (2013). Regulatory patterns of a large family of defensin-like genes expressed in nodules of Medicago truncatula. PLoS ONE 8:e60355. doi: 10.1371/journal.pone.0060355
29. Narise, T., Kobayashi, K., Baba, S., Shimojima, M., Masuda, S., Fukaki, H., et al. (2010). Involvement of auxin signaling mediated by IAA14 and ARF7/19 in membrane lipid remodeling during phosphate starvation. Plant Mol. Biol. 72, 533-544. doi: 10.1007/s11103-009-9589-4
30. Nishimura, T., Wada, T., Yamamoto, K. T., and Okada, K. (2005). The Arabidopsis STV1 protein, responsible for translation reinitiation, is required for auxin-mediated gynoecium patterning. Plant Cell 17, 2940-2953. doi: 10.1105/tpc.105.036533
31. Ortu, G., Balestrini, R., Pereira, A., Becker, D., Kuster, H., and Bonfante, P. (2012). Plant genes related to gibberellin biosynthesis and signaling are differentially regulated during the early stages of AM fungal interactions. Mol. Plant5, 951-954. doi: 10.1093/mp/sss027
32. Pacios-Bras, C., Schlaman, H. R., Boot, K., Admiraal, P., Langerak, J. M., Stougaard, J., et al. (2003). Auxin distribution in Lotus japonicus during root nodule development. Plant Mol. Biol. 52, 1169-1180. doi: 10.1023/B:PLAN.0000004308.78057.f5
33. Parry, G., Delbarre, A., Marchant, A., Swarup, R., Napier, R., Perrot-Rechenmann, C., et al. (2001). Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. Plant J. 25, 399-406. doi: 10.1046/j.1365-313x.2001.00970.x
34. Plet, J., Wasson, A., Ariel, F., Le Signor, C., Baker, D., Mathesius, U., et al. (2011). MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J. 65, 622-633. doi: 10.1111/j.1365-313X.2010.04447.x
35. Qi, Y., Wang, S., Shen, C., Zhang, S., Chen, Y., Xu, Y., et al. (2012). OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytol. 193, 109-120. doi: 10.1111/j.1469-8137.2011.03910.x
36. Rightmyer, A. P., and Long, S. R. (2011). Pseudonodule formation by wild-type and symbiotic mutant Medicago truncatula in response to auxin transport inhibitors. Mol. Plant Microbe Interact. 24, 1372-1384. doi: 10.1094/MPMI-04-11-0103
37. Roudier, F., Fedorova, E., Lebris, M., Lecomte, P., Gyorgyey, J., Vaubert, D., et al. (2003). The Medicago species A2-type cyclin is auxin regulated and involved in meristem formation but dispensable for endoreduplication-associated developmental programs. Plant Physiol. 131, 1091-1103. doi: 10.1104/pp.102.011122
38. Sakamoto, T., Morinaka, Y., Inukai, Y., Kitano, H., and Fujioka, S. (2013). Auxin signal transcription factor regulates expression of the brassinosteroid receptor gene in rice. Plant J. 73, 676-688. doi: 10.1111/tpj.12071
39. Shen, C., Wang, S., Bai, Y., Wu, Y., Zhang, S., Chen, M., et al. (2010). Functional analysis of the structural domain of ARF proteins in rice (Oryza sativa L.). J. Exp. Bot. 61, 3971-3981. doi: 10.1093/jxb/erq208
40. Shen, C., Wang, S., Zhang, S., Xu, Y., Qian, Q., Qi, Y., et al. (2013). OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryza sativa L.). Plant Cell Environ. 36, 607-620. doi: 10.1111/pce.12001
41. Tan, X., Calderon-Villalobos, L. I., Sharon, M., Zheng, C., Robinson, C. V., Estelle, M., et al. (2007). Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640-645. doi: 10.1038/nature05731
42. Tiwari, S. B., Hagen, G., and Guilfoyle, T. (2003). The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15, 533-543. doi: 10.1105/tpc.008417
43. Turner, M., Nizampatnam, N. R., Baron, M., Coppin, S., Damodaran, S., Adhikari, S., et al. (2013). Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiol. 162, 2042-2055. doi: 10.1104/pp.113.220699
44. Ulmasov, T., Hagen, G., and Guilfoyle, T. J. (1997). ARF1, a transcription factor that binds to auxin response elements. Science 276, 1865-1868. doi: 10.1126/science.276.5320.1865
45. van Noorden, G. E., Kerim, T., Goffard, N., Wiblin, R., Pellerone, F. I., Rolfe, B. G., et al. (2007). Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol. 144, 1115-1131. doi: 10.1104/pp.107.099978
46. van Noorden, G. E., Ross, J. J., Reid, J. B., Rolfe, B. G., and Mathesius, U. (2006). Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiol. 140, 1494-1506. doi: 10.1104/pp.105.075879
47. Wang, D., Pei, K., Fu, Y., Sun, Z., Li, S., Liu, H., et al. (2007). Genome-wide analysis of the auxin response factors(ARF) gene family in rice (Oryza sativa). Gene 394, 13-24. doi: 10.1016/j.gene.2007.01.006
48. Wang, Y., Deng, D., Shi, Y., Miao, N., Bian, Y., and Yin, Z. (2012). Diversification, phylogeny and evolution of auxin response factor (ARF) family: insights gained from analyzing maize ARF genes. Mol. Biol. Rep. 39, 2401-2415. doi: 10.1007/s11033-011-0991-z
49. Wasson, A. P., Pellerone, F. I., and Mathesius, U. (2006). Silencing the flavonoid pathway in Medicago truncatulainhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell 18, 1617-1629. doi: 10.1105/tpc.105.038232
50. Wu, M. F., Tian, Q., and Reed, J. W. (2006). Arabidopsis microRNA167 controls patterns of ARF6 and ARF8expression, and regulates both female and male reproduction. Development 133, 4211-4218. doi: 10.1242/dev.02602
51. Yang, J. H., Han, S. J., Yoon, E. K., and Lee, W. S. (2006). Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res. 34, 1892-1899. doi: 10.1093/nar/gkl118
52. Young, N. D., Debelle, F., Oldroyd, G. E., Geurts, R., Cannon, S. B., Udvardi, M. K., et al. (2011). The Medicagogenome provides insight into the evolution of rhizobial symbioses. Nature 480, 520-524. doi: 10.1038/nature10625
53. Zhang, G., Chen, M., Chen, X., Xu, Z., Guan, S., Li, L. C., et al. (2008). Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J. Exp. Bot. 59, 4095-4107. doi: 10.1093/jxb/ern248
54. Zouine, M., Fu, Y., Chateigner-Boutin, A. L., Mila, I., Frasse, P., Wang, H., et al. (2014). Characterization of the tomato ARF gene family uncovers a multi-levels post-transcriptional regulation including alternative splicing.PLoS ONE 9:e84203. doi: 10.1371/journal.pone.0084203