The Auxin response factor gene family in banana: Genome-wide identification and expression analyses during development, ripening, and Abiotic stress

Frontiers in Plant Science

Volumn 6, Issue September, 2015, Pages

  Hu, Wei ^a   Zuo, Jiao ^a   Hou, Xiaowan ^a   Yan, Yan ^a   Wei, Yunxie ^a   Liu, Juhua ^a   Li, Meiying ^a   Xu, Biyu ^a   Jin, Zhiqiang ^a  

^a INSTITUTE OF TROPICAL BIOSCIENCE AND BIOTECHNOLOGY   (China)

Author keywords

Abiotic stresses; Auxin response factors (ARF) transcription factor; Banana; Development; Expression analysis; Ripening

Indexed keywords

EID: 84942886526     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00742     Document Type: Article

References (66)

1. Asif, M. H., Lakhwani, D., Pathak, S., Bhambhani, S., Bag, S. K., and Trivedi, P. K. (2014). Genome-wide identification and expression analysis of the mitogen-activated protein kinase gene family from banana suggest involvement of specific members in different stages of fruit ripening. Funct. Integr. Genomics 14, 161-175. doi: 10.1007/s10142-013-0349-9
2. Backiyarani, S., Uma, S., Nithya, S., Chandrasekar, A., Saraswathi, M. S., Thangavelu, R., et al. (2015). Genome-wide analysis and differential expression of chitinases in banana against root lesion nematode (Pratylenchus coffeae) and eumusa leaf spot (Mycosphaerella eumusae) pathogens. Appl. Biochem. Biotechnol. 175, 3585-3598. doi: 10.1007/s12010-015-1528-z
3. Bananuka, J. A., Rubaihayo, P. R., and Tenywa, M. M. (1999). Reactions of Musa genotypes to drought stress. Afr. CropSci. J. 7, 333-339.
4. Bapat, V. A., Trivedi, P. K., Ghosh, A., Sane, V. A., Ganapathi, T. R., and Nath, P. (2010). Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnol. Adv. 28, 94-107. doi: 10.1016/j.biotechadv.2009.10.002
5. Chen, L., Ren, F., Zhong, H., Feng, Y., Jiang, W., and Li, X. (2010). Identification and expression analysis of genes in response to high-salinity and drought stresses in Brassica napus. Acta Biochim. Biophys. Sin. 42, 154-164. doi: 10.1093/abbs/gmp113
6. D'Hont, A., Denoeud, F., Aury, J. M., Baurens, F. C., Carreel, F., Garsmeur, O., et al. (2012). The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488, 213-217. doi: 10.1038/nature11241
7. Davey, M. W., Gudimella, R., Harikrishna, J. A., Sin, L. W., Khalid, N., and Keulemans, J. (2013). A draft Musa balbisiana genome sequence for molecular genetics in polyploid, inter- and intra-specific Musa hybrids. BMC Genomics 14:683. doi: 10.1186/1471-2164-14-683
8. Davies, P. J. (1995). Plant Hormones, Physiology, Biochemistry and Molecular Biology, 2ndEdn. Dordrecht: Kluwer.
9. de Jong, M., Wolters-Arts, M., Feron, R., Mariani, C., and Vriezen, W. H. (2009). The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J. 57, 160-170. doi: 10.1111/j.1365-313X.2008.03671.x
10. de Jong, M., Wolters-Arts, M., Garcia-Martinez, J. L., Mariani, C., and Vriezen, W. H. (2011). The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signalling during tomato fruit set and development. J. Exp. Bot. 62, 617-626. doi: 10.1093/jxb/erq293
11. Du, H., Wu, N., Fu, J., Wang, S., Li, X., Xiao, J., et al. (2012). A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J. Exp. Bot. 63, 6467-6480. doi: 10.1093/jxb/ers300
12. Ellis, C. M., Negpal, P., Young, J. C., Hagen, G., Guilfoyle, T. J., and Reed, J. W. (2005). AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132, 4563-4574. doi: 10.1242/dev.02012
13. Finn,R. D., Clements, J., and Eddy, S. R. (2011). HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39, 29-37. doi: 10.1093/nar/gkr367
14. 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
15. 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
16. Ha, C. V., Le, D. T., Nishiyama, R., Watanabe, Y., Sulieman, S., Tran, U. T., et al. (2013). The auxin response factor transcription factor family in soybean: genome-wide identification and expression analyses during development and water stress. DNA Res. 20, 511-524. doi: 10.1093/dnares/dst027
17. Hagen, G., and Guilfoyle, T. (2002). Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol. 49, 373-385. doi: 10.1023/A:1015207114117
18. Hardtke, C. S., and Berleth, T. (1998). The Arabidopsis gene MONOPTEROUS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405-1411. doi: 10.1093/emboj/17.5.1405
19. Hayashi, K. (2012). The interaction and integration ofauxin signaling components. Plant Cell Physiol. 53, 965-975. doi: 10.1093/pcp/pcs035
20. Hill, S. A., and Rees, T. (1995a). The effect of glucose on the control of carbohydrate metabolism in ripening bananas. Planta 196, 335-343. doi: 10.1007/BF00201393
21. Hill, S. A., and Rees, T. (1995b). The effect of hypoxia on the control of carbohydrate metabolism in ripening bananas. Planta 197, 313-323. doi: 10.1007/BF00202653
22. Hirayama, T., and Shinozaki, K. (2010). Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J. 61, 1041-1052. doi: 10.1111/j.1365-313X.2010.04124.x
23. Hu, W., Liu, J. H., Yang, X. Y., Zhang, J. B., Jia, C. H., Li, M. Y., et al. (2014). Identification of a gene encoding glutamate decarboxylase involved in the postharvest fruit ripening process in banana. HortScience 49, 1056-1060.
24. Huang, J. C., Xiao, Y., and Zhao, C. X. (1999). Some physiological responses of banana to water stress. J. Zhongkai Agrotech. Coll. 12, 40-42.
25. Jacob-Wilk, D., Holland, D., Goldschmidt, E. E., Riov, J., and Eyal, Y. (1999). Chlorophyll breakdown by chlorophyllase: isolation and functional expression of the chlase1 gene from ethylene-treated citrus fruit and its regulation during development. Plant J. 20, 653-661. doi: 10.1046/j.1365-313X.1999.00637.x
26. Jain, M., and Khurana, J. P. (2009). Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J. 276, 3148-3162. doi: 10.1111/j.1742-4658.2009.07033.x
27. Kalluri, U. C., Difazio, S. P., Brunner, A. M., and Tuskan, G. A. (2007). Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol. 7:59. doi: 10.1186/1471-2229-7-59
28. Kumar, R., Tyagi, A. K., and Sharma, A. K. (2011). Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol. Genet. Genomics 285, 245-260. doi: 10.1007/s00438-011-0602-7
29. Lee, M., Jung, J. H., Han, D. Y., Seo, P. J., Park, W. J., and Park, C. M. (2012). Activation of a flavin monooxygenase gene YUCCA7 enhances drought resistance in Arabidopsis. Planta 235, 923-938. doi: 10.1007/s00425-011-1552-3
30. Li, J., Dai, X., and Zhao, Y. (2006). A role for auxin response factor 19 in auxin and ethylene signaling in Arabidopsis. Plant Physiol. 140, 899-908. doi: 10.1104/pp.105.070987
31. Li, S. B., OuYang, W. Z., Hou, X. J., Xie, L. L., Hu, C. G., and Zhang, J. Z. (2015). Genome-wide identification, isolation and expression analysis of auxin response factor (ARF) gene familyin sweet orange (Citrus sinensis). Front. Plant Sci. 6:119. doi: 10.3389/fpls.2015.00119
32. Lim, P. O., Lee, I. C., Kim, J., Kim, H. J., Ryu, J. S., Woo, H. R., et al. (2010). Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J. Exp. Bot. 61, 1419-1430. doi: 10.1093/jxb/erq010
33. Lohani, S., Trivedi, P. K., and Nath, P. (2004). Changes in activities of cell wall hydrolases during ethylene-induced ripening in banana: effect of 1-MCP, ABA and IAA. Postharvest Biol. Technol. 31, 119-126. doi: 10.1016/j.postharvbio.2003.08.001
34. Matsui, A., Mizunashi, K., Tanaka, M., Kaminuma, E., Nguyen, A. H., Nakajima, M., et al. (2014). tasiRNA-ARF pathway moderates floral architecture in arabidopsis plants subjected to drought stress. Biomed Res. Int. 2014:303451. doi: 10.1155/2014/303451
35. Mun, J. H., Yu, H. J., Shin, J. Y., Oh, M., Hwang, H. J., and Chung, H. (2012). Auxin response factor gene family in Brassica rapa: genomic organization, divergence, expression, and evolution. Mol. Genet. Genomics 287, 765-784. doi: 10.1007/s00438-012-0718-4
36. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., et al. (2006). A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439. doi: 10.1126/science.1126088
37. Okushima, Y., Overvoorde, P. J., Arima, K., Alonso, J. M., Chan, A., Chang, C., et al. (2005). Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17, 444-463. doi: 10.1105/tpc.104.028316
38. Park, J. E., Park, J. Y., Kim, Y. S., Staswick, P. E., Jeon, J., Yun, J., et al. (2007). GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 282, 10036-10046. doi: 10.1074/jbc.M610524200
39. Paterson, A. H., Bowers, J. E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., et al. (2009). The Sorghum bicolor genome and the diversification ofgrasses. Nature 457, 551-556. doi: 10.1038/nature07723
40. Perez-Rodriguez, P., Riano-Pachón, D. M., Correa, L. G., Rensing, S. A., Kersten, B., and Mueller-Roeber, B. (2010). PlnTFDB: updated content and newfeatures of the plant transcription factor database. Nucleic Acids Res. 38, D822-D827. doi: 10.1093/nar/gkp805
41. Pua, E. C., Chandramouli, S., Han, P., and Liu, P. (2003). Malate synthase gene expression during fruit ripening of Cavendish banana (Musa acuminata cv. Williams). J. Exp. Bot. 54, 309-316. doi: 10.1093/jxb/erg030
42. Sagar, M., Chervin, C., Mila, I., Hao, Y., Roustan, J. P., Benichou, M., et al. (2013). SlARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit development. Plant Physiol. 161, 1362-1374. doi: 10.1104/pp.113.213843
43. Schruff, M. C., Spielman, M., Tiwari, S., Adams, S., Fenby, N., and Scott, R. J. (2005). The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signaling, cell division, and size of seeds and other organs. Development 133, 251-261. doi: 10.1242/dev.02194
44. Sekhwal, M. K., Swami, A. K., Sharma, V., and Sarin, R. (2015). Identification of drought-induced transcription factors in Sorghum bicolor using GO term semantic similarity. Cell. Mol. Biol. Lett. 20, 1-23. doi: 10.2478/s11658-014-0223-3
45. Serrani, J. C., Ruiz-Rivero, O., Fos, M., and Garcia-Martinez, J. L. (2008). Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant J. 56, 922-934. doi: 10.1111/j.1365-313X.2008.03654.x
46. 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
47. Shen, C., Yue, R., Sun, T., Zhang, L., Xu, L., Tie, S., et al. (2015). Genome-wide identification and expression analysis of auxin response factor gene family in Medicago truncatula. Front. Plant Sci. 6:73. doi: 10.3389/fpls.2015.00073
48. 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. doi: 10.1105/tpc.109.069906
49. Sreedharan, S., Shekhawat, U. K., and Ganapathi, T. R. (2013). Transgenic banana plants overexpressing a native plasma membrane aquaporin MusaPIP1; 2 display high tolerance levels to different abiotic stresses. Plant Biotechnol. J. 11, 942-952. doi: 10.1111/pbi.12086
50. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739. doi: 10.1093/molbev/msr121
51. Thomas, P., and Janave, M. T. (1992). Effect of temperature on chlorophyllase activity, chlorophyll degradation, and carotenoids of Cavendish bananas during ripening. Int. J. Food Sci. Technol. 27, 57-63. doi: 10.1111/j.1365-2621.1992.tb01178.x
52. 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
53. Tohge, T., and Fernie, A. R. (2010). Combining genetic diversity, informatics and metabolomics to facilitate annotation of plant gene function. Nat. Protoc. 5, 1210-1227. doi: 10.1038/nprot.2010.82
54. Ulmasov, T., Hagen, G., and Guilfoyle, T. J. (1999). Dimerization and DNA binding of auxin response factors. Plant J. 19, 309-319. doi: 10.1046/j.1365-313X.1999.00538.x
55. Ulmasov, T., Murfett, J., Hagen, G., and Guilfoyle, T. J. (1997). Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell. 9, 1963-1971. doi: 10.1105/tpc.9.11.1963
56. van Asten, P. J. A., Fermont, A. M., and Taulya, G. (2011). Drought is a major yield loss factor for rainfed East African highland banana. Agric. Water Manage. 98, 541-552. doi: 10.1016/j.agwat.2010.10.005
57. Wan, S., Li, W., Zhu, Y., Liu, Z., Huang, W., and Zhan, J. (2014). Genome-wide identification, characterization and expression analysis of the auxin response factor gene familyin Vitis vinifera. Plant Cell Rep. 33, 1365-1375. doi: 10.1007/s00299-014-1622-7
58. Wang, D., Pei, K., Fu, Y., Sun, Z., Li, S., Liu, H., et al. (2007). Genome-wide analysis ofthe auxin response factors (ARF) gene familyin rice (Oryza sativa). Gene 394, 13-24. doi: 10.1016/j.gene.2007.01.006
59. Wang, S., Bai, Y., Shen, C., Wu, Y., Zhang, S., Jiang, D., et al. (2010). Auxin-related gene families in abiotic stress response in Sorghum bicolor. Funct. Integr. Genomics 10, 533-546. doi: 10.1007/s10142-010-0174-3
60. Wu, J., Wang, F., Cheng, L., Kong, F., Peng, Z., Liu, S., et al. (2011). Identification, isolation and expression analysis of auxin response factor (ARF) genes in Solanum lycopersicum. Plant Cell Rep. 30, 2059-2073. doi: 10.1007/s00299-011-1113-z
61. Xing, H., Pudake, R. N., Guo, G., Xing, G., Hu, Z., Zhang, Y., et al. (2011). Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genomics 12:178. doi: 10.1186/1471-216412-178
62. Yu, H., Soler, M., Mila, I., Clemente, H. S., Savelli, B., Dunand, C., et al. (2014). Genome-wide characterization and expression profiling of the AUXIN RESPONSE FACTOR (ARF) gene family in Eucalyptus grandis. PLoS ONE 30:e108906. doi: 10.1371/journal.pone.0108906
63. Zahir, Z. A., Shah, M. K., Naveed, M., and Akhter, M. J. (2010). Substrate- dependent auxin production by Rhizobium phaseoli improves the growth and yield of Vigna radiate L. under salt stress conditions. J. Microbiol. Biotechnol. 20, 1288-1294. doi: 10.4014/jmb.1002.02010
64. Zhang, H., Jin, J., Tang, L., Zhao, Y., Gu, X., Gao, G., et al. (2011). PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res. 39, D1114-D1117. doi: 10.1093/nar/gkq1141
65. Zhang, S. W., Li, C. H., Cao, J., Zhang, Y. C., Zhang, S. Q., Xia, Y. F., et al. (2009). Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol. 151, 1889-1901. doi: 10.1104/pp.109.146803
66. 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