Molecular characterization of banana NAC transcription factors and their interactions with ethylene signalling component EIL during fruit ripening

Journal of Experimental Botany

Volumn 63, Issue 14, 2012, Pages 5171-5187

  Shan, Wei ^a   Kuang, Jian Fei ^a   Chen, Lei ^a   Xie, Hui ^a   Peng, Huan Huan ^a   Xiao, Yun Yi ^a   Li, Xue Ping ^a   Chen, Wei Xin ^a   He, Quan Guang ^b   Chen, Jian Ye ^a   Lu, Wang Jin ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b NATIONAL ENGINEERING RESEARCH CENTER FOR NON FOOD BIOREFINERY   (China)

Author keywords

banana; EIL; fruit ripening; interaction; NAC; regulation

Indexed keywords

ETHYLENE; ETHYLENE DERIVATIVE; TRANSCRIPTION FACTOR; TRANSCRIPTOME; VEGETABLE PROTEIN;

ARTICLE; DNA SEQUENCE; DRUG EFFECT; FLUORESCENCE; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUSA; REAL TIME POLYMERASE CHAIN REACTION; TWO HYBRID SYSTEM;

ETHYLENES; FLUORESCENCE; FRUIT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MUSA; PLANT PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TWO-HYBRID SYSTEM TECHNIQUES;

CALYPTRONOMA;

EID: 84865798425     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers178     Document Type: Article

References (78)

1. Abel S, Theologis A. 1994. Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. The Plant Journal 5, 421-427.
2. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M. 1997. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. The Plant Cell 9, 841-857.
3. Al-Daoud F, Cameron RK. 2011. ANAC055 and ANAC092 contribute non-redundantly in an EIN2-dependent manner to age-related resistance in Arabidopsis. Physiological and Molecular Plant Pathology 76, 212-222.
4. Balazadeh S, Kwasneewski M, Caldana C, Mehrnia M, Zanor MI, Xue GP, Mueller-Roeber B. 2011. ORS1, an H2O2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Molecular Plant 4, 346-360.
5. Bapat VA, Trivedi PK, Ghosh A, Sane VA. 2010. Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnology Advances 28, 94-107.
6. Berger Y, Harpaz-Saad S, Brand A, Melnik H, Sirding N, Alvarez JP, Zinder M, Samach A, Eshed Y, Ori N. 2009. The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136, 823-832.
7. Bu Q, Jiang H, Li CB, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Li C. 2008. Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Research 18, 756-767.
8. Cara B, Giovannoni JJ. 2008. Molecular biology of ethylene during tomato fruit development and maturation. Plant Science 175, 106-113.
9. Chen JY, Liu DJ, Jiang YM, Zhao ML, Shan W, Kuang JF, Lu WJ. 2011. Molecular characterization of a strawberry FaASR in relation to fruit ripening. PloS ONE 6, 24649.
10. Chen L, Zhong HY, Kuang JF, Li JG, Lu WJ, Chen JY. 2011. Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234, 377-390.
11. Clendennen SK, Kipp PB, May GD. 1997. The role of ethylene in banana fruit ripening. In: Kanelis AK, ed. Biology and biotechnology of the plant hormone ethylene. Dordrecht: Kluwer Academic Publishers, 141-148.
12. Clendennen SK, May GD. 1997. Differential gene expression in ripening banana fruit. Plant Physiology 115, 463-469.
13. Delessert C, Kazan K, Wilson IW, Van Der Straeten D, Manners J, Dennis ES, Dolferus R. 2005. The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. The Plant Journal 43, 745-757.
14. Dominguez M, Vendrell M. 1993. Ethylene biosynthesis in banana fruit: evolution of EFE activity and ACC levels in peel and pulp during ripening. Journal of Horticultural Science 68, 63-70.
15. Duval M, Hsieh TF, Kim SY, Thomas TL. 2002. Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Molecular Biology 50, 237-248.
16. Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H. 2010. The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene. Journal of Experimental Botany 61, 1523-1535.
17. Ernst HA, Olsen AN, Skriver K, Larsen S, Leggio LL. 2004. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Reports 5, 297-303.
18. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LSP, Yamaguchi-Shinozaki K, Shinozaki K. 2004. A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. The Plant Journal 39, 863-876.
19. Gao F, Xiong AS, Peng RH, Jin XF, Xu J, Zhu B, Chen JM, Yao QH. 2010. OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants. Plant Cell Tissue and Organ Culture 100, 255-262.
20. Giovannoni JJ. 2004. Genetic regulation of fruit development and ripening. The Plant Cell 16, S170-S180.
21. Gong W, Shen YP, Ma LG, et al. 2004. Genome-wide ORFeome cloning and analysis of Arabidopsis transcription factor genes. Plant Physiology 135, 773-782.
22. Greve K, Cour TL, Jensen MK, Poulsen FM, Skriver K. 2003. Interactions between plant RING-H2 and plant-specific NAC (NAM/ATAF1/2/CUC2) proteins: RING-H2 molecular specificity and cellular localization. Biochemical Journal 371, 97-108.
23. Hao YJ, Song QX, Chen HW, Zou HF, Wei W, Kang XS, Ma B, Zhang WK, Zhang JS, Chen SY. 2010. Plant NAC-type transcription factor proteins contain a NARD domain for repression of transcriptional activation. Planta 232, 1033-1043.
24. Hao YJ, Wei W, Song QX, et al. 2011. Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. The Plant Journal 68, 302-313.
25. He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY. 2005. AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. The Plant Journal 44, 903-916.
26. Hegedus D, Yu M, Baldwin D, Margaret G, Sharpe A, Parkin I, Whitwill S, Lydiate D. 2003. Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Molecular Biology 53, 383-397.
27. Hershkovitz V, Friedman H, Goldschmidt EE, Feygenberg O, Pesis E. 2011. Effect of seed on ripening control components during avocado fruit development. Journal of Plant Physiology 168, 2177-2183.
28. Hibara K, Takada S, Tasaka M. 2003. CUC1 gene activates the expression of SAM-related genes to induce adventitious shoot formation. The Plant Journal 36, 687-696.
29. Jeong JS, Park YT, Jung H, Park SH, Kim JK. 2009. Rice NAC proteins act as homodimers and heterodimers. Plant Biotechnology Report 3, 127-134.
30. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG. 2009. Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323, 1053-1057.
31. Kim SG, Lee AK, Yoon HK, Park CM. 2008. A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. The Plant Journal 55, 77-88.
32. Kim SY, Kim SG, Kim YS, Seo PJ, Bae M, Yoon HK, Park CM. 2007. Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucleic Acids Research 35, 203-213.
33. Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM. 2006. A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. The Plant Cell 18, 3132-3144.
34. Klee HJ, Giovannoni JJ. 2011. Genetics and control of tomato fruit ripening and quality attributes. Annual Review of Genetics 45, 41-59.
35. Kleinow T, Himbert S, Krenz B, Jeske H, Koncz C. 2009. NAC domain transcription factor ATAF1 interacts with SNF1-related kinases and silencing of its subfamily causes severe developmental defects in Arabidopsis. Plant Science 177, 360-370.
36. Kumar R, Sharma MK, Kapoor S, Tyagi AK, Sharma AK. 2012. Transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes provides insight into LeMADS-RIN-regulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato. Molecular Genetics and Genomics 287, 189-203.
37. Larsson E, Sitbon F, Sundström J, von Arnold S. 2011. NAC regulation of embryo development in conifers. BMC Proceedings 5, 67.
38. Lee SH, Hannink M. 2003. Molecular mechanisms that regulate transcription factor localization suggest new targets for drug development. Advanced Drug Delivery Reviews 55, 717-731.
39. Lin R, Zhao W, Meng X, Wang M, Peng Y. 2007. Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea. Plant Science 172, 120-130.
40. Liu J, Xu B, Hu L, Li M, Su W, Wu J, Yang J, Jin Z. 2009. Involvement of a banana MADS-box transcription factor gene in ethylene-induced fruit ripening. Plant Cell Reports 28, 103-111.
41. Liu X, Shiomi S, Nakatsuka A, Kubo Y, Nakamura R, Inaba A, Liu XJ. 1999. Characterization of ethylene biosynthesis associated with ripening in banana fruit. Plant Physiology 121, 1257-1265.
42. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
43. Mao C, Ding W, Wu Y, Yu J, He X, Shou H, Wu P. 2007. Overexpression of a NAC-domain protein promotes shoot branching in rice. New Phytologist 176, 288-298.
44. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ. 2011. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiology 157, 1568-1579.
45. Mbéguié-A-Mbéguié D, Hubert O, Fils-Lycaon B, Chillet M, Baurens FC. 2008. EIN3-like gene expression during fruit ripening of Cavendish banana (Musa acuminata cv. Grande Naine). Physiologia Plantarum 133, 435-448.
46. Meng C, Cai C, Zhang T, Guo W. 2009. Characterization of six novel NAC genes and their responses to abiotic stresses in Gossypium hirsutum L. Plant Science 176, 352-359.
47. Morishita T, Kojima Y, Maruta T, Nishizawa-Yokoi A, Yabuta Y, Shigeoka S. 2009. Arabidopsis NAC transcription factor, ANAC078, regulates flavonoids biosynthesis under high-light. Plant and Cell, Physiology 50, 2210-2222.
48. Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2012. NAC transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta 1819, 97-103.
49. Oh SK, Lee S, Yu SH, Choi D. 2005. Expression of a novel NAC domain-containing transcription factor (CaNAC1) is preferentially associated with incompatible interactions between chili pepper and pathogens. Planta 222, 876-887.
50. Olsen AN, Ernst HA, Leggio LL, Skriver K. 2005. NAC transcription factors: structurally distinct, functionally diverse. Trends in Plant Science 10, 79-87.
51. Ooka H, Satoh K, Doi K, et al. 2003. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Research 10, 239-247.
52. Pinheiro GL, Marques CS, Costa MD, Reis PA, Alves MS, Carvalho CM, Fietto LG, Fontes EP. 2009. Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444, 10-23.
53. Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P. 2003. EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115, 679-689.
54. Qin G, Wang Y, Cao B, Wang W, Tian S. 2012. Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. The Plant Journal 70, 243-255.
55. Sablowski RW, Meyerowitz EM. 1998. A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92, 93-103.
56. Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM. 2010. Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. The Plant Journal 61, 661-671.
57. Seymour G, Ryder C, Cevik V, Hammond J, Popovich A, King G, Vrebalov J, Giovannoni JJ, Manning K. 2011. A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria × ananassa Duch.) fruit, a non-climacteric tissue. Journal of Experimental Botany 62, 1179-1188.
58. Souer E, Houwelingen AV, Kloos D, Mol J, Koes R. 1996. The no apical meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordial boundaries. Cell 85, 159-170.
59. Tieman DM, Ciardi JA, Taylor MG, Klee HJ. 2001. Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. The Plant Journal 26, 47-58.
60. Tisza V, Kovács L, Balogh A, Heszky L, Kiss E. 2010. Characterization of FaSPT, a SPATULA gene encoding a bHLH transcriptional factor from the non-climacteric strawberry fruit. Plant Physiology and Biochemistry 48, 822-826.
61. Tran LSP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2004. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. The Plant Cell 16, 2481-2498.
62. Verza NC, Figueira TRS, Sousa SM, Arruda P. 2011. Transcription factor profiling identifies an aleurone-preferred NAC family member involved in maize seed development. Annals of Applied Biology 158, 115-129.
63. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J. 2002. A MADS-box gene necessary for fruit ripening at the tomato Ripening-Inhibitor (Rin) locus. Science 296, 343-346.
64. Walter M, Chaban C, Schutze K, et al. 2004. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. The Plant Journal 40, 428-438.
65. Wang Y, Lu W, Jiang Y, Luo Y, Jiang W, Joyce D. 2006. Expression of ethylene-related expansin genes in cool-stored ripening banana fruit. Plant Science 170, 962-967.
66. Wan CY, Wilkins TA. 1994. A modified hot borate method significantly enhances the yield of high quality RNA from cotton (Gossypium hirsutum L.). Analytical Biochemistry 223, 7-12.
67. Waters BM, Uauy C, Dubcovsky J, Grusak MA. 2009. Wheat (Triticum aestivum) NAM proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain. Journal of Experimental Botany 60, 4263-4274.
68. Weir I, Lu J, Cook H, Causier B, Schwarz-Sommer Z, Davies B. 2004. CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum. Development 131, 915-922.
69. Xia N, Zhang G, Sun YF, et al. 2010. TaNAC8, a novel NAC transcription factor gene in wheat, responds to stripe rust pathogen infection and abiotic stresses. Physiological and Molecular Plant Pathology 74, 394-402.
70. Xie Q, Frugis G, Colgan D, Chua NH. 2000. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes & Development 14, 3024-3036.
71. Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M. 2005. Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Molecular Biology 59, 191-203.
72. Yamasaki K, Kigawa T, Inoue M, Watanabe S, Tateno M, Seki M, Shinozaki K, Yokoyama S. 2008. Structures and evolutionary origins of plant-specific transcription factor DNA-binding domains. Plant Physiology and Biochemistry 46, 394-401.
73. Yao J, Kvarnheden A, Morris B. 1999. Seven MADS-box genes in apple are expressed in different parts of the fruit. Journal of the American Society for Horticultural Science 124, 8-13.
74. Yin X, Allan AC, Chen K, Ferguson IB. 2010. Kiwifruit EIL and ERF genes involved in regulating fruit ripening. Plant Physiology 153, 1280-1292.
75. Yoshii M, Yamazaki M, Rakwal R, Kishi-Kaboshi M, Miyao A, Hirochika H. 2010. The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. The Plant Journal 61, 804-815.
76. Zhang K, Gan SS. 2012. An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiology 158, 961-969.
77. Zhao Q, Gallego-Giraldo L, Wang H, Zeng Y, Ding SY, Chen F, Dixon RA. 2010. NAC transcription factor orchestrates multiple features of cell wall development in Medicago Truncatula. The Plant Journal 63, 100-114.
78. Zhong R, Lee C, Ye ZH. 2010. Functional characterization of poplar wood-associated NAC domain transcription factors. Plant Physiology 152, 1044-1055.