PpERF3 positively regulates ABA biosynthesis by activating PpNCED2/3 transcription during fruit ripening in peach

Xiaobei Wang , Wenfang Zeng , Yifeng Ding , Yan Wang , Liang Niu , Jia-Long Yao , Lei Pan , Zhenhua Lu , Guochao Cui , Guohuai Li , Zhiqiang Wang

Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) : 19

PDF (1734KB)
Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) :19 DOI: 10.1038/s41438-018-0094-2
Article
research-article
PpERF3 positively regulates ABA biosynthesis by activating PpNCED2/3 transcription during fruit ripening in peach
Author information +
History +
PDF (1734KB)

Abstract

The plant hormone ethylene regulates ripening in climacteric fruits. The phytohormone abscisic acid (ABA) affects ethylene biosynthesis, but whether ethylene influences ABA biosynthesis is unknown. To explore this possibility, we investigated the interactions between the ABA biosynthesis genes PpNCED2/3 and the ethylene response transcription factor PpERF3 in peach fruit. The ABA content increased during fruit maturation and reached a peak at stage S4 III. The increase was greatly inhibited by the ethylene inhibitor 1-MCP, which also suppressed PpERF3 expression. PpERF3 shared a similar expression profile with PpNCED2/3, encoding a rate-limiting enzyme involved in ABA biosynthesis, during fruit ripening. A yeast one-hybrid assay suggested that the nuclear-localized PpERF3 might bind to the promoters of PpNCED2/3. PpERF3 increased the expression of PpNCED2/3 as shown by dual-luciferase reporters, promoter-GUS assays and transient expression analyses in peach fruit. Collectively, these results suggest that ethylene promotes ABA biosynthesis through PpERF3’s regulation of the expression of ABA biosynthesis genes PpNCED2/3.

Cite this article

Download citation ▾
Xiaobei Wang, Wenfang Zeng, Yifeng Ding, Yan Wang, Liang Niu, Jia-Long Yao, Lei Pan, Zhenhua Lu, Guochao Cui, Guohuai Li, Zhiqiang Wang. PpERF3 positively regulates ABA biosynthesis by activating PpNCED2/3 transcription during fruit ripening in peach. Horticulture Research, 2019, 6 (1) : 19 DOI:10.1038/s41438-018-0094-2

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Klee, H. J. & Giovannoni, J. J. Genetics and control of tomato fruit ripening and quality attributes. Annu. Rev. Genet. 45, 41-59 (2011).

[2]

Martel, C., Vrebalov, J., Tafelmeyer, P. & Giovannoni, J. J. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol. 157, 1568-1579 (2011).

[3]

Li, T. et al. Apple (Malus domestica) MdERF2 negatively affects ethylene biosynthesis during fruit ripening by suppressing MdACS1 transcription . Plant J. 88, 735-748 (2016).

[4]

Han, Y. et al. Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol. (2016). https://doi.org/10.1104/pp.16.00301.

[5]

McMurchie, E. J., McGlasson, W. B. & Eaks, I. L. Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature 237, 235 (1972).

[6]

Leng, P., Yuan, B. & Guo, Y. The role of abscisic acid in fruit ripening and responses to abiotic stress. J. Exp. Bot. 65, 4577-4588 (2014).

[7]

Wright, S. T. C. & Hiron, R. W. P. (+)-Abscisic acid, the growth inhibitor induced in detached wheat leaves by a period of wilting. Nature 224, 719 (1969).

[8]

Estrada-Melo, A. C., Reid, M. S. & Jiang, C. Z. Overexpression of an ABA biosynthesis gene using a stress-inducible promoter enhances drought resistance in petunia. Hortic. Res. 2, 15013 (2015).

[9]

Giribaldi, M., Gény, L., Delrot, S. & Schubert, A. Proteomic analysis of the effects of ABA treatments on ripening Vitis vinifera berries . J. Exp. Bot. 61, 2447-2458 (2010).

[10]

Sun, L. et al. Suppression of 9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiol. 158, 283-298 (2012).

[11]

Sun, L., Yuan, B., Zhang, M., Wang, L. & Cui, M. Fruit-specific RNAi-mediated suppression of SlNCED1 increases both lycopene and β-carotene contents in tomato fruit. J. Exp. Bot. 63, 3097-3108 (2012).

[12]

Mou, W. et al. Comprehensive analysis of ABA effects on ethylene biosynthesis and signaling during tomato fruit ripening. PLoS ONE 11, e0154072 (2016).

[13]

Soto, A., Ruiz, K. B., Ravaglia, D., Costa, G. & Torrigiani, P. ABA may promote or delay peach fruit ripening through modulation of ripening-and hormone-related gene expression depending on the developmental stage. Plant. Physiol. Biochem. 64, 11-24 (2013).

[14]

Shin, S., Lv, J., Fazio, G., Mazzola, M. & Zhu, Y. Transcriptional regulation of ethylene and jasmonate mediated defense response in apple (Malus domestica) root during Pythium ultimum infection . Hortic. Res. 1, 14053 (2014).

[15]

Xiao, Y. Y. et al. Banana ethylene response factors are involved in fruit ripening through their interactions with ethylene biosynthesis genes. J. Exp. Bot. 64, 2499-2510 (2013).

[16]

Kuang, J. F. et al. The transcriptional regulatory network mediated by banana (Musa acuminata) dehydration-responsive element binding (MaDREB) transcription factors in fruit ripening . New Phytol. 214, 762-781 (2017).

[17]

Yin, X. R., Allan, A. C., Chen, K. S. & Ferguson, I. B. Kiwifruit EIL and ERF genes involved in regulating fruit ripening. Plant Physiol. 153, 1280-1292 (2010).

[18]

Zhang, Z., Zhang, H., Quan, R., Wang, X. C. & Huang, R. Transcriptional regulation of the ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol. 150, 365-377 (2009).

[19]

Wang, X. et al. Genes involved in ethylene signal transduction in peach (Prunus persica) and their expression profiles during fruit maturation . Sci. Hortic. 224, 306-316 (2017).

[20]

Burbidge, A., Grieve, T. M., Jackson, A., Thompson, A. & McCarty, D. R. Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J. 17, 427-431 (1999).

[21]

Lara, I. & Vendrell, M. Changes in abscisic acid levels, ethylene biosynthesis, and protein patterns during fruit maturation of Granny Smith’ apples. J. Am. Soc. Hortic. Sci. 125, 183-189 (2000).

[22]

Sun, Y. et al. Transcriptional regulation of genes encoding key enzymes of abscisic acid metabolism during melon (Cucumis melo L.) fruit development and ripening . J. Plant. Growth Regul. 32, 233-244 (2013).

[23]

Rodrigo, M. J., Alquezar, B. & Zacarías, L. Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck) . J. Exp. Bot. 57, 633-643 (2006).

[24]

Wheeler, S., Loveys, B., Ford, C. & Davies, C. The relationship between the expression of abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid . Aust. J. Grape Wine Res. 15, 195-204 (2009).

[25]

Ji, K. et al. Non-climacteric ripening in strawberry fruit is linked to ABA, FaNCED2 and FaCYP707A1. Funct. Plant Biol. 39, 351-357 (2012).

[26]

Kumar, R., Khurana, A. & Sharma, A. K. Role of plant hormones and their interplay in development and ripening of fleshy fruits. J. Exp. Bot. 65, 4561-4575 (2014).

[27]

Lohani, S., Trivedi, P. K. & Nath, P. 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 (2004).

[28]

Tonutti, P., Bonghi, C., Ruperti, B., Tornielli, G. B. & Ramina, A. Ethylene evolution and 1-aminocyclopropane-1-carboxylate oxidase gene expression during early development and ripening of peach fruit. J. Am. Soc. Hortic. Sci. 122, 642-647 (1997).

[29]

He, Z. in Guidance to Experiment on Chemical Control in Crop Plants (ed He, Z. P.) 60-68 (Beijing Agricultural University Publishers, Beijing, 1993).

[30]

Weiler, E. W., Jourdan, P. S. & Conrad, W. Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 153, 561-571 (1981).

[31]

Tatsuki, M. et al. Increased levels of IAA are required for system 2 ethylene synthesis causing fruit softening in peach (Prunus persica L. Batsch) . J. Exp. Bot. 64, 1049-1059 (2013).

[32]

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method . Methods 25, 402-408 (2001).

[33]

Zhang, B. et al. Differential expression within the LOX gene family in ripening kiwifruit. J. Exp. Bot. 57, 3825-3836 (2006).

[34]

Lescot, M., Déhais, P., Thijs, G., Marchal, K. & Moreau, Y. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30, 325-327 (2002).

[35]

Liu, C., Zhao, A., Zhu, P., Li, J. & Han, L. Characterization and expression of genes involved in the ethylene biosynthesis and signal transduction during ripening of mulberry fruit. PLoS ONE 10, e0122081 (2015).

[36]

Wei, Q. et al. A wheat MYB transcriptional repressor TaMyb1D regulates phenylpropanoid metabolism and enhances tolerance to drought and oxidative stresses in transgenic tobacco plants. Plant Sci. 265, 112-123 (2017).

[37]

Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana . Plant J. 16, 735-743 (1998).

[38]

Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907 (1987).

[39]

Hellens, R. P. et al. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant. Methods 1, 13 (2005).

[40]

Liu, H. et al. UV-B irradiation differentially regulates terpene synthases and terpene content of peach. Plant Cell Environ. 40, 2261-2275 (2017).

PDF (1734KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/