NAC transcription factors play an important role in ethylene biosynthesis, reception and signaling of tomato fruit ripening

Molecular Genetics and Genomics

Volumn 291, Issue 3, 2016, Pages 1205-1217

  Kou, Xiaohong ^a   Liu, Chen ^a   Han, Lihua ^a   Wang, Shuang ^a   Xue, Zhaohui ^a  

^a TIANJIN UNIVERSITY   (China)

Author keywords

Ethylene; Fruit ripening; NAC transcription; Tomato; VIGS

Indexed keywords

ETHYLENE; MESSENGER RNA; PHYTOHORMONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAC4; TRANSCRIPTION FACTOR SNAC9; UNCLASSIFIED DRUG; ETHYLENE DERIVATIVE; PLANT PROTEIN;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DOWN REGULATION; FRUIT RIPENING; GENE; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; LEACO1 GENE; LEACS2 GENE; LEACS4 GENE; LEERF2 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SENESCENCE; SIGNAL TRANSDUCTION; SNAC4 GENE; SNAC9 GENE; TOMATO; CHEMISTRY; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR MODEL; PROMOTER REGION; SYNTHESIS;

ETHYLENES; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; LYCOPERSICON ESCULENTUM; MODELS, MOLECULAR; PLANT GROWTH REGULATORS; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84957544544     PISSN: 16174615     EISSN: 16174623     Source Type: Journal    
DOI: 10.1007/s00438-016-1177-0     Document Type: Article

References (46)

1. Cara B, Giovannoni JJ (2008) Molecular biology of ethylene during tomato fruit development and maturation. Plant Sci 175:106–113
2. Choudhury SR, Roy S, Sengupta DN (2008) Characterization of transcriptional profiles of MA-ACS1 and MA-ACO1 genes in response to ethylene, auxin, wounding, cold and different photoperiods during ripening in banana fruit. J Plant Physiol 165:1865–1878
3. Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Boil 10:283–289
4. Hamilton A, Lycett G, Grierson D (1990) Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature 346:284–287
5. 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. Plant J 44:903–916
6. Huang JC, Piater LA, Dubery IA (2006) The NAC transcription factor gene ANAC072 is differentially expressed in Arabidopsis thaliana in response to microbe-associated molecular pattern (MAMP) molecules. Physiol Mol Plant P 80:19–27
7. Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, Kasumi T (2008) DNA-binding specificity, transcriptional activation potential, and therin mutation effect for the tomato fruit-ripening regulator RIN. Plant J. 55:212–223
8. Kevany B, Tieman DM, Taylor M, Dal Cin V, Klee H (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J. 51:458–567
9. Kieber J, Rothenberg M, Roman G, Feldmann A, Ecker J (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis encodes a member of the Raf family of protein kinases. Cell 72:427–441
10. Klee HJ (2004) Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiol 135:660–667
11. Kou XH, Watkins CB, Gan SS (2012) Arabidopsis AtNAP regulates fruit senescence. J Exp Bot 63:6139–6147
12. Kou XH, Wang S, Wu MS, Guo RZ, Xue ZH, Meng N, Tao XM, Chen MM, Zhang YF (2014) Molecular characterization and expression analysis of NAC family transcription factors in tomato. Plant Mol Biol Rep 32:501–516
13. Lashbrook CC, Tieman DM, Klee HJ (1998) Differential regulation of the tomato ETR gene family throughout plant development. Plant J. 15:243–252
14. Leclercq J, Adams-Phillips LC, Zegzouti H, Jones B, Latche A, Giovannoni JJ, Pech JC, Bouzayen M (2002) LeCTR1, a tomato CTR1-Like gene, demonstrates ethylene signaling ability in Arabidopsis and novel expression patterns in tomato. Plant Physiol 130:1132–1142
15. Li L, Zhu BZ, Fu DQ, Luo YB (2011) RIN transcription factor plays an important role in ethylene biosynthesis of tomato fruit ripening. J Sci Food Agric 13:2308–2314
16. Lincoln JE, Campbell AD, Oetiker J, Rottmann WH, Oeller PW, Shen NF, Theologis A (1993) LE-ACS4, a fruit ripening and wound-induced 1-aminocyclopropane-1-carboxylate synthase gene of tomato (Lycopersicon esculentum). J Biol Chem 268:19422–19430
17. Lindemose S, Jensen MK, Van de Velde J, O’Shea C, Heyndrickx KS, Workman CT, Vandepoele K, Skriver K, De Masi F (2014) A DNA-binding-site landscape and regulatory network analysis for NAC transcription factors in Arabidopsis thaliana. Nucleic Acids Res 42:7681–7693
18. −△△CT method. Methods 25:402–408
19. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96
20. Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118:1295–1305
21. Oeller PW, Wong LM, Taylor LP, Pike DA, Theologis A (1991) Reversible inhibition of tomato fruit senescence by antisense l-aminocy-clopropane-1-carboxylate synthase. Science 254:427–439
22. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005a) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87
23. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005b) DNA-binding specificity and molecular functions of NAC transcription factors. Plant Sci 169:785–797
24. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247
25. Peng H, Cheng HY, Yu XW, Shi QH, Zhang H, Li JG, Ma Hao (2009a) Characterization of a chickpea (Cicer arietinum L.) NAC family gene, CarNAC5, which is both developmentally- and stress-regulated. Plant Physiol Bioch. 47:1037–1045
26. Peng H, Cheng HY, Chen C, Yu XW, Yang JN, Gao WR, Shi QH, Zhang H, Li JG, Ma H (2009b) A NAC transcription factor gene of Chickpea (Cicer arietinum), CarNAC3, is involved in drought stress response and various developmental processes. J Plant Physiol 166:1934–1945
27. Pirrello J, Jaimes-Miranda F, Sanchez-Ballesta MT, Tournier B, Ahmad QK, Regad F, Latche A, Pech JC, Bouzayen M (2006) Sl-ERF2, a tomato ethylene response factor involved in ethylene response and seed germination. Plant Cell Physiol 47:1195–1205
28. Shan W, Kuang JF, Chen L, Xie H, Peng HH, Xiao YY, Li XP, Chen WX, He QG, Chen JY, Lu WJ (2012) Molecular characterization of banana NAC transcription factors and their interactions with ethylene signalling component EIL during fruit ripening. J Exp Bot 63:5171–5187
29. Soto A, Ruiz KB, Ziosi V, Costa G, Torrigiani P (2012) Ethylene and auxin biosynthesis and signaling are impaired by methyl jasmonate leading to a transient slowing down of ripening in peach fruit. J Plant Physiol 169:1858–1865
30. Thompson AJ, Tor M, Barry CS, Vrebalov J, Orfila C, Jarvis MC, Giovannoni JJ, Grierson D, Seymour GB (1999) Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant. Plant Physiol 120:383–389
31. Tieman DE, Taylor MG, Ciardi JA, Klee H (2000) The tomato ethylene receptors NR and LeETR4 are negative regulators of ethylene response and exhibit functional compensation within a multigene family. Proc Natl Acad Sci 97:5663–5668
32. 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. Plant J. 26:47–58
33. Tigchelaar E (1978) Tomato ripening mutants. HortScience 13:502
34. Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latche A, Pech JC, Bouzayen M (2003) New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Lett 550:149–154
35. Wilmowicz E, Kesy J, Kopcewicz J (2008) Ethylene and ABA interactions in the regulation of flower induction in Pharbitis nil. J Plant Physiol 165:1917–1928
36. Xia N, Zhang G, Sun YF, Zhu L, Xu LS, Chen XM, Liu B, Yu YT, Wang XJ, Huang LL, Kang ZS (2010) TaNAC8, a novel NAC transcription factor gene in wheat, responds to stripe rust pathogen infection and abiotic stresses. Physiol Mol Plant P 74:394–402
37. Xu Q, Wang WQ, Zeng JK, Zhang J, Grierson D, Li X, Yin XR, Chen KS (2015) A NAC transcription factor, EjNAC1, affects lignification of loquat fruit by regulating lignin. Postharvest Biol Tec 102:25–31
38. Yang RC, Deng CT, Ouyang B, Ye ZB (2011) Molecular analysis of two salt-responsive NAC-family genes and their expression analysis in tomato. Mol Biol Rep 38:857–863
39. Yang XT, Song J, Campbell-Palmer L, Fillmore S, Zhang ZQ (2013) Effect of ethylene and 1-MCP on expression of genes involved in ethylene biosynthesis and perception during ripening of apple fruit. Postharvest Biol Tec 78:55–66
40. Yang X, Hu YX, Li XL, Yu XD, Li QL (2014) Molecular characterization and function analysis of SlNAC2 in Suaeda liaotungensis K. Gene 543:190–197
41. Yokotani N, Tamura S, Nakano R, Inaba A, Kubo Y (2003) Characterization of a novel tomato EIN3-like gene (LeEIL4). J Exp Bot 54:2775–2776
42. Zhang ZK, Huber DJ, Hurr BM, Rao JP (2009) Delay of tomato fruit ripening in response to 1-methylcyclopropene is influenced by internal ethylene levels. Postharvest Biol. Tec. 54:1–8
43. Zhu H, Zhu B, Shao Y, Wang X, Lin X, Xie Y, Li Y, Gao H, Luo Y (2006) Tomato fruit development and ripening are altered by the silencing of LeEIN2 gene. J Integr Plant Biol 48:1478–1485
44. Zhu HL, Zhu BZ, Li YC, Shao Y, Wang XG, Xie YH, Chen AJ, Luo JJ, Jia XY, Luo YB (2008) Expression and DNAbinding activity of the tomato transcription factor RIN (ripening inhibitor). Biosci Biotechnol Biochem 72:250–252
45. Zhu ZG, Shi JL, Xu WR, Li H, He MY, Xu Y, Xu TF, Yang YZ, Cao JL, Wang YJ (2013) Three ERF transcription factors from Chinese wild grapevine Vitis pseudoreticulata participate in different biotic and abiotic stress-responsive pathways. J Plant Physiol 170:923–933
46. Zhu M, Chen G, Zhou S, Tu Y, Wang Y, Dong T, Hu Z (2014) A new tomato NAC (NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol 55:119–135