Ectopic Over-expression of HaFT-1, a 14-3-3 Protein from Haloxylon Ammodendron, Enhances Acquired Thermotolerance in Transgenic Arabidopsis

Overview

Journal Plant Mol Biol

Date 2023 Jun 21

PMID 37341869

Authors

Rong Pan

Wenjing Ren

Shuanshuan Liu

Hua Zhang

Xin Deng

Bo Wang

Affiliations

Soon will be listed here.

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.

Citing Articles

The 14-3-3 protein nt GF14e interacts with CIPK2 and increases low potassium stress in tobacco.

Xu L, Lu Y, Jiang J, Chen Q, Xu Y, Mi Q Plant Signal Behav. 2024; 19(1):2359257.

PMID: 38825861 PMC: 11152103. DOI: 10.1080/15592324.2024.2359257.

References

Altuntas C, Demiralay M, Sezgin Muslu A, Terzi R . Proline-stimulated signaling primarily targets the chlorophyll degradation pathway and photosynthesis associated processes to cope with short-term water deficit in maize. Photosynth Res. 2020; 144(1):35-48. DOI: 10.1007/s11120-020-00727-w. View

Avramova Z . Transcriptional 'memory' of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J. 2015; 83(1):149-59. DOI: 10.1111/tpj.12832. View

Avramova Z . Defence-related priming and responses to recurring drought: Two manifestations of plant transcriptional memory mediated by the ABA and JA signalling pathways. Plant Cell Environ. 2018; 42(3):983-997. DOI: 10.1111/pce.13458. View

Brandwein D, Wang Z . Interaction between Rho GTPases and 14-3-3 Proteins. Int J Mol Sci. 2017; 18(10). PMC: 5666830. DOI: 10.3390/ijms18102148. View

Charng Y, Liu H, Liu N, Chi W, Wang C, Chang S . A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol. 2006; 143(1):251-62. PMC: 1761974. DOI: 10.1104/pp.106.091322. View

Chen C, Chen H, Zhang Y, Thomas H, Frank M, He Y . TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol Plant. 2020; 13(8):1194-1202. DOI: 10.1016/j.molp.2020.06.009. View

Chi C, Xu X, Wang M, Zhang H, Fang P, Zhou J . Strigolactones positively regulate abscisic acid-dependent heat and cold tolerance in tomato. Hortic Res. 2021; 8(1):237. PMC: 8558334. DOI: 10.1038/s41438-021-00668-y. View

Costa M, Farrant J, Oliver M, Ligterink W, Buitink J, Hilhorst H . Key genes involved in desiccation tolerance and dormancy across life forms. Plant Sci. 2016; 251:162-168. DOI: 10.1016/j.plantsci.2016.02.001. View

Dobra J, Cerny M, Storchova H, Dobrev P, Skalak J, Jedelsky P . The impact of heat stress targeting on the hormonal and transcriptomic response in Arabidopsis. Plant Sci. 2015; 231:52-61. DOI: 10.1016/j.plantsci.2014.11.005. View

10.

Dong Q, Duan D, Zheng W, Huang D, Wang Q, Li X . MdVQ37 overexpression reduces basal thermotolerance in transgenic apple by affecting transcription factor activity and salicylic acid homeostasis. Hortic Res. 2021; 8(1):220. PMC: 8484266. DOI: 10.1038/s41438-021-00655-3. View

11.

Friedrich T, Oberkofler V, Trindade I, Altmann S, Brzezinka K, Lamke J . Heteromeric HSFA2/HSFA3 complexes drive transcriptional memory after heat stress in Arabidopsis. Nat Commun. 2021; 12(1):3426. PMC: 8187452. DOI: 10.1038/s41467-021-23786-6. View

12.

Garwe D, Thomson J, Mundree S . XVSAP1 from Xerophyta viscosa improves osmotic-, salinity- and high-temperature-stress tolerance in Arabidopsis. Biotechnol J. 2006; 1(10):1137-46. DOI: 10.1002/biot.200600136. View

13.

Gokirmak T, Denison F, Laughner B, Paul A, Ferl R . Phosphomimetic mutation of a conserved serine residue in Arabidopsis thaliana 14-3-3ω suggests a regulatory role of phosphorylation in dimerization and target interactions. Plant Physiol Biochem. 2015; 97:296-303. DOI: 10.1016/j.plaphy.2015.10.022. View

14.

Grinevich D, Desai J, Stroup K, Duan J, Slabaugh E, Doherty C . Novel transcriptional responses to heat revealed by turning up the heat at night. Plant Mol Biol. 2019; 101(1-2):1-19. PMC: 6695350. DOI: 10.1007/s11103-019-00873-3. View

15.

He Y, Wu J, Lv B, Li J, Gao Z, Xu W . Involvement of 14-3-3 protein GRF9 in root growth and response under polyethylene glycol-induced water stress. J Exp Bot. 2015; 66(8):2271-81. PMC: 4986726. DOI: 10.1093/jxb/erv149. View

16.

Hilker M, Schwachtje J, Baier M, Balazadeh S, Baurle I, Geiselhardt S . Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev Camb Philos Soc. 2015; 91(4):1118-1133. DOI: 10.1111/brv.12215. View

17.

Huang Y, Niu C, Yang C, Jinn T . The Heat Stress Factor HSFA6b Connects ABA Signaling and ABA-Mediated Heat Responses. Plant Physiol. 2016; 172(2):1182-1199. PMC: 5047099. DOI: 10.1104/pp.16.00860. View

18.

Kawai-Yamada M, Ohori Y, Uchimiya H . Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell. 2003; 16(1):21-32. PMC: 301392. DOI: 10.1105/tpc.014613. View

19.

Kinoshita T, Seki M . Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol. 2014; 55(11):1859-63. DOI: 10.1093/pcp/pcu125. View

20.

Kosugi S, Hasebe M, Tomita M, Yanagawa H . Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci U S A. 2009; 106(25):10171-6. PMC: 2695404. DOI: 10.1073/pnas.0900604106. View