Wheat Elongator Subunit 4 Negatively Regulates Freezing Tolerance by Regulating Ethylene Accumulation

Wang, Kai; Zhai, Mingjuan; Han, Ran; Wang, Xiaolu; Xu, Wenjing; Zeng, Xiaoxue; Qi, Guang; Komatsuda, Takao; Liu, Cheng

doi:10.3390/ijms23147634

Open AccessArticle

Wheat Elongator Subunit 4 Negatively Regulates Freezing Tolerance by Regulating Ethylene Accumulation

by

Kai Wang

^1,†

,

Mingjuan Zhai

^2,†,

Ran Han

¹,

Xiaolu Wang

¹,

Wenjing Xu

¹,

Xiaoxue Zeng

¹,

Guang Qi

¹,

Takao Komatsuda

¹ and

Cheng Liu

^1,*

¹

Crop Research Institute, Shandong Academy of Agricultural Sciences/National Engineering Research Center of Wheat and Maize/Shandong Technology Innovation Center of Wheat, Jinan 252100, China

²

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China

^*

Author to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Int. J. Mol. Sci. 2022, 23(14), 7634; https://doi.org/10.3390/ijms23147634

Submission received: 13 June 2022 / Revised: 7 July 2022 / Accepted: 8 July 2022 / Published: 11 July 2022

(This article belongs to the Special Issue Environmental Stress and Plants 2.0)

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Abstract

Freezing stress is a major factor limiting production and geographical distribution of temperate crops. Elongator is a six subunit complex with histone acetyl-transferase activity and is involved in plant development and defense responses in Arabidopsis thaliana. However, it is unknown whether and how an elongator responds to freezing stress in plants. In this study, we found that wheat elongator subunit 4 (TaELP4) negatively regulates freezing tolerance through ethylene signaling. TaELP4 promoter contained cold response elements and was up-regulated in freezing stress. Subcellular localization showed that TaELP4 and AtELP4 localized in the cytoplasm and nucleus. Silencing of TaELP4 in wheat with BSMV-mediated VIGS approach significantly elevated tiller survival rate compared to control under freezing stress, but ectopic expression of TaELP4 in Arabidopsis increased leaf damage and survival rate compared with Col-0. Further results showed that TaELP4 positively regulated ACS2 and ACS6 transcripts, two main limiting enzymes in ethylene biosynthesis. The determination of ethylene content showed that TaELP4 overexpression resulted in more ethylene accumulated than Col-0 under freezing stress. Epigenetic research showed that histone H3K9/14ac levels significantly increased in coding/promoter regions of AtACS2 and AtACS6 in Arabidopsis. RT-qPCR assays showed that the EIN2/EIN3/EIL1-CBFs-COR pathway was regulated by TaELP4 under freezing stress. Taken together, our results suggest that TaELP4 negatively regulated plant responses to freezing stress via heightening histone acetylation levels of ACS2 and ACS6 and increasing their transcription and ethylene accumulation.

Keywords: Elongator complex; freezing stress; histone acetylation; ethylene; Triticum aestivum

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MDPI and ACS Style

Wang, K.; Zhai, M.; Han, R.; Wang, X.; Xu, W.; Zeng, X.; Qi, G.; Komatsuda, T.; Liu, C. Wheat Elongator Subunit 4 Negatively Regulates Freezing Tolerance by Regulating Ethylene Accumulation. Int. J. Mol. Sci. 2022, 23, 7634. https://doi.org/10.3390/ijms23147634

AMA Style

Wang K, Zhai M, Han R, Wang X, Xu W, Zeng X, Qi G, Komatsuda T, Liu C. Wheat Elongator Subunit 4 Negatively Regulates Freezing Tolerance by Regulating Ethylene Accumulation. International Journal of Molecular Sciences. 2022; 23(14):7634. https://doi.org/10.3390/ijms23147634

Chicago/Turabian Style

Wang, Kai, Mingjuan Zhai, Ran Han, Xiaolu Wang, Wenjing Xu, Xiaoxue Zeng, Guang Qi, Takao Komatsuda, and Cheng Liu. 2022. "Wheat Elongator Subunit 4 Negatively Regulates Freezing Tolerance by Regulating Ethylene Accumulation" International Journal of Molecular Sciences 23, no. 14: 7634. https://doi.org/10.3390/ijms23147634

APA Style

Wang, K., Zhai, M., Han, R., Wang, X., Xu, W., Zeng, X., Qi, G., Komatsuda, T., & Liu, C. (2022). Wheat Elongator Subunit 4 Negatively Regulates Freezing Tolerance by Regulating Ethylene Accumulation. International Journal of Molecular Sciences, 23(14), 7634. https://doi.org/10.3390/ijms23147634

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Wheat Elongator Subunit 4 Negatively Regulates Freezing Tolerance by Regulating Ethylene Accumulation

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