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Ectopic over-expression of HaFT-1, a 14-3-3 protein from Haloxylon ammodendron, enhances acquired thermotolerance in transgenic Arabidopsis

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Abstract

Haloxylon ammodendron, an important shrub utilized for afforestation in desert areas, can withstand harsh ecological conditions such as drought, high salt and extreme heat. A better understanding of the stress adaptation mechanisms of H. ammodendron is vital for ecological improvement in desert areas. In this study, the role of the H. ammodendron 14-3-3 protein HaFT-1 in thermotolerance was investigated. qRT-PCR analysis showed that heat stress (HS) priming (the first HS) enhanced the expression of HaFT-1 during the second HS and subsequent recovery phase. The subcellular localization of YFP-HaFT-1 fusion protein was mainly detected in cytoplasm. HaFT-1 overexpression increased the germination rate of transgenic Arabidopsis seeds, and the survival rate of HaFT-1 overexpression seedlings was higher than that of wild-type (WT) Arabidopsis after priming-and-triggering and non-primed control treatments. Cell death staining showed that HaFT-1 overexpression lines exhibited significantly reduced cell death during HS compared to WT. Transcriptome analysis showed that genes associated with energy generation, protein metabolism, proline metabolism, autophagy, chlorophyll metabolism and reactive oxygen species (ROS) scavenging were important to the thermotolerance of HS-primed HaFT-1 transgenic plants. Growth physiology analysis indicated that priming-and-triggering treatment of Arabidopsis seedlings overexpressing HaFT-1 increased proline content and strengthened ROS scavenging activity. These results demonstrated that overexpression of HaFT-1 increased not only HS priming but also tolerance to the second HS of transgenic Arabidopsis, suggesting that HaFT-1 is a positive regulator in acquired thermotolerance.

Key message

Over-expression of HaFT-1 enhances heat stress priming and tolerance to the second HS in transgenic Arabidopsis, suggesting HaFT-1 as a positive regulator in acquired thermotolerance.

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Data availability

The raw RNA-Seq data from this study have been deposited at the NCBI Sequence Read Archive (SRA) and can be accessed with BioProject accession No. PRJNA849331. The SRA accessions, BioProject accession and design description are listed in Supplementary Table 8.

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Acknowledgements

We thank National Natural Science Foundation of China for funding (Grant numbers: 31760070 and 32060070). We would like to thank A&L Scientific Editing (www.alpublish.com) for its linguistic assistance during the preparation of this manuscript.

Funding

This work was supported by National Natural Science Foundation of China (Grant numbers: 31760070 and 32060070).

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Contributions

BW conceived the study, designed the experiments, and wrote the manuscript. RP designed and performed all the experiments, and wrote the first draft of the manuscript, which was further expanded by XD and BW. XD and HZ participated in designing the experiments. WR performed some of the physiological assays and gene expression assays. SL constructed the plant expression vector of HaFT-1 and performed transgenic Arabidopsis screening of T1 to T2 generations. All authors read and approved the manuscript.

Corresponding author

Correspondence to Bo Wang.

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The authors declare that they have no competing interests. The authors have no relevant financial or non-financial interests to disclose.

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Pan, R., Ren, W., Liu, S. et al. Ectopic over-expression of HaFT-1, a 14-3-3 protein from Haloxylon ammodendron, enhances acquired thermotolerance in transgenic Arabidopsis. Plant Mol Biol 112, 261–277 (2023). https://doi.org/10.1007/s11103-023-01361-5

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  • DOI: https://doi.org/10.1007/s11103-023-01361-5

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