FTSH (filamentation temperature-sensitive H) is a cytoplasmic membrane protein endopeptidase and belongs to the AAA (ATPase associated with diverse cellular activities) protease family (Ogura and Wilkinson, 2001). The family has an N-terminal transmembrane domain, ATP and Zn²⁺ binding sites, forms complexes with regulatory factor HflK or HflC oligomers in the form of cyclic homohexamer, and relies on ATP to degrade short-lived proteins and misassembled membrane proteins, so as to regulate the normal growth and development of organisms (Kihara et al., 1997; Kihara and Ito, 1998; Ito and Akiyama, 2005). FTSH is necessary for the growth of many organisms. The decrease of gene expression or gene mutation of this family will lead to serious growth defects and even death of Bacillus subtilis and Escherichia coli (Deuerling et al., 1997; Jayasekera et al., 2000). FTSH gene was first independently discovered by 4 different research groups when screening different phenotypes in Escherichia coli (Schumann, 1999). So far, it has been found and studied in a variety of organisms such as Bacillus subtilis (Deuerling et al., 1995), Lactococcus lactis (Duwat et al., 1995), Arabidopsis thaliana (Lindahl et al., 1996), Nicotiana tabacum (Seo et al., 2000), Medicago sativa (Ivashuta et al., 2002), Citrullus lanatus (Akashi et al., 2004), Synechocystis sp (Kamata et al., 2005), Solanum lycopersicum (Sun et al., 2006a), Zea mays (Andjelkovic and Thompson 2006), Spinacia oleracea (Yoshioka et al., 2006), Brassica juncea (Knight et al., 2006), Solanum tuberosum (Fan et al., 2007), Xerophyta viscose (Ingle et al., 2007), Oryza sativa (Zhang and Sun, 2009), Glycine max (Yin et al., 2011), Lactobacillus plantarum (Bove et al., 2012), Arachis hypogaea (Zheng et al., 2016, Jiangsu Agricultural Sciences, 44(12): 74-77) and Acidovorax citrulli (Ji et al., 2019).

FTSH was involved in the response of organisms to a variety of stress. Heat stress or light stress increased the expression of FTSH gene in Synechocystis sp cells (Kamata et al., 2005). Lactobacillus plantarum mutants lacking FTSH protease showed significant sensitivity to the increase of heat and salt concentration, while FTSH overexpression led to the increase of heat and salt stress tolerance (Bove et al., 2012). The growth ability of the FTSH gene deletion mutant of Acidovorax citrulli was significantly reduced under heat stress and high salt stress (Ji et al., 2019). It was also found that FTSH was involved in resisting stress responses such as cold stress, heat stress, drought stress and salt stress. Stress could increase the expression of FTSH gene. For example, cold stress increased the expression of MsFTSH gene in Medicago sativa (Ivashuta et al., 2002); Heat stress increased the expression of AtFTSH11 gene in Arabidopsis thaliana (Chen et al., 2006) and LeFTSH6 gene in Solanum lycopersicum (Sun et al., 2006b); Drought stress significantly increased the expression of SoFTSH4-like gene in leaves and roots of Solanum tuberosum (Fan et al., 2007); Salt stress up-regulated the expression of 9 FTSH gene in Arachis hypogaea, including one FTSH6-like gene (Zheng et al., 2016). FTSH gene can improve the tolerance of plants to stress. Overexpression of AtFTSH11 in Arabidopsis thaliana contributed to the overall tolerance to heat stress (Chen et al., 2006); FTSHi5 can inhibit the expression of aging related genes and maintain cell redox balance (Wang et al., 2018b; Havé et al., 2018). However, there was no report on the application of FTSH gene in wheat.

Wheat is an important food crop in the world. In different regions of the world, wheat is often subjected to drought and heat stress throughout its growth period, and its yield and quality are seriously affected. Therefore, improving the drought and heat resistance of wheat is of great significance to the high and stable yield and high quality of wheat. In order to study the characteristics and functions of wheat FTSH genes, TaFTSH6 was cloned from wheat ‘Bobwhite’, and its expression changes under drought and heat stress were analyzed by bioinformatics to provide a theoretical basis for wheat drought and heat resistance and provide a new idea for wheat breeding for drought and heat stress tolerance.

1 Results and Analysis

1.1 TaFTSH6 gene cloning and evolutionary tree analysis of amino acid sequence

Using wheat leaf cDNA as template, TaFTSH6F and TaFTSH6R were used for PCR amplification. The amplification products were detected by 1% agarose gel electrophoresis. The gene fragment larger than 2000 bp was observed (Figure 1), which was consistent with the expectation. The target fragment was recovered, purified and connected with pMD19-T vector to transform E. coil DH5α competent cells, the transformed products were screened by colony PCR for positive clones, and the plasmids were extracted and sent to BGI for sequencing. The sequence has an ORF of 2 049 bp and encodes 683 amino acids. The gene sequence was compared on the wheat gene bank URGI, and it was found that the gene was located on the chr7D chromosome, so it was named TaFTSH6-7D.

Figure 1 Amplification products of TaFTSH6-7D PCR Note: M: DL 2000 Marker; 1: PCR product of TaFTSH6-7D ORF

The evolutionary tree analysis of FTSH amino acid sequences of different species showed that TaFTSH6 sequence was highly similar to FTSH6 of other species, and FTSH6 sequence also showed obvious differences between monocotyledons and dicotyledons (Figure 2). TaFTSH6-7D had the highest homology with its diploid ancestor Aegilops auschii, up to 99%, and was slightly different from TaFTSH6-7A and TaFTSH6-7B. Moreover, TaFTSH6-7D was closely related to Hordeum vulgare, Brachypodium distachyon, Oryza sativa, Sorghum bicolor and Zea mays, and far from FTSH6 of other species.

1.2 Structural analysis of TaFTSH6 protein

By comparing the TaFTSH6 protein sequence of wheat with that of Oryza sativa, Hordeum vulgare and Zea mays, it was found that the FTSH6 sequence was highly conserved and had the typical characteristics of FTSH family, especially between 90~670 aa. It showed a conserved N-terminal transmembrane domain at 164~182. There were typical ATP binding sites at 260~268, 315~320 and 360~366. The conserved WalkerA domain GXXGXGK (S/T) was located at 260~268, and the conserved WalkerB domain VFIDE was located at 315~320. Behind the ATP binding site, there was a typical LLRXGRX arginine ring structure (at 375~381) (Figure 3).

1.3 Cis-elements analysis of TaFTSH6 promoters

The promoter sequence in the region about 2 kb upstream of the start codon of TaFTSH6-7D gene coding region was analyzed. The results showed that CAACTG drought response site was found at 56 bp, 339 bp, 1 101 bp and 1 833 bp upstream of ATG, and GACnnCTCnnGAA heat shock transcription factor binding site was found at 234 bp upstream of ATG. In addition, there were many cis-acting regulatory elements involved in growth and development, cis-acting regulatory elements involved in hormone signal transduction pathway and cis-acting regulatory elements involved in abiotic stress response in the promoter region of TaFTSH6-7D gene (Table 1).

Table 1 Cis-elements analysis of TaFTSH6-7D promoters

1.4 The expression analysis of TaFTSH6-7D gene under drought and heat stress

In order to study the response of TaFTSH6-7D gene to drought and heat stress, the expression of TaFTSH6 gene in leaves and roots of wheat at seedling stage was analyzed by RT-PCR. The results showed that under drought stress, the expression of TaFTSH6-7D gene in leaves and roots of wheat increased, especially after 12 hours of treatment, the expression of TaFTSH6-7D gene increased significantly and extremely significantly in leaves and roots, respectively. Under heat stress, the expression of TaFTSH6-7D gene in leaves and roots of wheat also increased. At 6 h, 2 d (6 h/d) and 3 d (6 h/d), the expression of TaFTSH6-7D gene increased significantly in leaves and roots. The above results showed that TaFTSH6-7D gene was induced by drought and heat stress (Figure 4).

2 Discussion

Plants face a variety of abiotic and biotic stresses throughout their life cycle, and protein degradation in vivo is one of the important ways for plants to respond to environmental stress and coordinate the relationship between growth and stress response (Chen et al., 2020). Organisms degrade end-of-life proteins and misassembled membrane proteins to regulate the normal growth and their response to the environment (Wang et al., 2018a). There are mainly ATP-independent lysosomal pathway and ATP-dependent ubiquitin proteasome pathway for protein degradation in organisms. Recent studies have also found the caspase pathway, the La protease pathway of mitochondria, the Kex2 hydrolase pathway in the Golgi body, and the hydrolase pathway on the cell membrane surface (Ling et al., 2019). Protein degradation by FTSH protease depends on ATP to provide energy. In Escherichia coli, FTSH forms complexes with the regulator Hf1KC oligomer in the form of cyclic homo-hexamer, and its activity is modified by phosphorylation (Kato and Sakamoto, 2019), and it degrade short-lived proteins and misassembled proteins (Nishimura et al., 2016). Its special feature is that it is membrane anchored, which can degrade wrong proteins and maintain membrane stability under stress conditions (Kato and Sakamoto, 2018). It is a hydrolase on the surface of cell membrane. Therefore, the FTSH protease family has an N-terminal transmembrane domain and a C-terminal region extending into the matrix. The C-terminal region contains ATPase and protease domain. ATPase domain plays the function of unfolding enzyme and transfers the substrate to the protease domain degradation chamber through a narrow pore. This study found that the FTSH6 protein sequences of different species were highly conserved in the N-terminal transmembrane domain, the C-terminal ATP binding site and the arginine ring.

At present, the mechanism of FTSH protease is still poorly understood. FTSH protease can extract and degrade the intact membrane protein from the membrane (Kato and Sakamoto, 2018). There are 12 FTSH coding genes in Arabidopsis thaliana, and 9 of them are located on the thylakoid membrane of the chloroplasts, 3 are located on the mitochondrial membrane (Sakamoto et al., 2003). FTSH is involved in the formation of thylakoid membrane during the early development of chloroplasts. The FTSH mutation in Nicotiana tabacum caused the collapse of thylakoid membrane in the later stages of leaf development (Kato et al., 2012). In addition, FTSH is also involved in the degradation and assembly of D1 protein in photosystem II repair cycle and several protein complexes in photosynthetic electron transport pathway. In Arabidopsis thaliana mutants lacking FTSH, light-damaged D1 protein accumulated, ROS (reactive oxygen species) signals were not effectively transmitted, and showed higher sensitivity to strong light stress (Zaltsman et al., 2005; Dogra et al., 2017; Wang et al., 2018a). However, the regulation mode of protease activity of FTSH, the pattern of FTSH and its complex recognizing damaged proteins, and the specific function and function mode of FTSH need to be further studied.

FTSH has been reported to be involved in the response to drought and heat stress. Under drought conditions, the increase of FTSH gene expression or a large amount of FTSH protein synthesis were found in plants such as Xerophyta viscose (Ingle et al., 2007), Citrullus lanatus originated from African desert (Akashi et al., 2004), Zea mays (Andjelkovic and Thompson, 2006), Brassica juncea (Knight et al., 2006) and Solanum tuberosum (Fan min et al., 2007). The increase of FTSH gene expression in the roots of Oryza sativa can enhance drought stress tolerance (Zhang and sun, 2009). Heat stress can increase the expression of LeFTSH6 gene in Solanum lycopersicum (Sun et al., 2006a; 2006b). Overexpression of FTSH11 in Arabidopsis thaliana contributed to the overall tolerance to heat stress (Chen et al., 2006). In wheat, it was found that the expression of FTSH2 in heat-resistant varieties was significantly higher than that in heat sensitive varieties under heat stress (Wang et al., 2015). In this study, it was found that the expression of TaFTSH6-7D gene in wheat increased significantly under PEG simulated drought or 36℃ heat treatment at seedling stage, which was consistent with the reports about other plants. The results of this study showed that TaFTSH6-7D gene was induced by drought and heat stress. The further study on the function and regulation mode of TaFTSH6 gene will provide a theoretical guidance to wheat molecular breeding for drought and heat stress tolerance.

3 Materials and Methods

3.1 Plant materials and treatment

In the light incubator, the seeds of wheat (Triticum aestivum L.) variety ‘Bobwhite’ were cultured in the medium at 4℃ for 5 d, 12℃ for 5 d and 25℃ for 2 d, and then transferred to 1/2MS medium and cultured until three leaf stage under the conditions of 25℃ (16 h)/20℃ (8 h) (day/night) and 75% relative humidity. The seedlings were subjected to simulated drought (15% PEG, 6 h, 12 h, 24 h and 48 h), heat (36℃, 3 h, 6 h, 2 d (6 h/d) and 3 d (6 h/d)) stress, and compared with normal growing seedlings. The samples were frozen in liquid nitrogen and stored at -80℃.

3.2 RNA extraction and cDNA synthesis

The total RNA was extracted from wheat leaves and roots by Trizol method, and the plants extracted RNA were seedlings and in good growth condition. After removing DNA from RNA samples, cDNA was synthesized according to the instructions of one-step reverse transcription kit from Tiangen Company and stored at -20℃.

3.3 Primer design and PCR amplification

The primers used in this experiment were showed in the table (Table 2). TaFTSH6F and TaFTSH6R were used for gene cloning. The PCR reaction procedure was as follows: pre-denaturation at 94℃ for 5 min, denaturation at 94℃ for 45 s, annealing at 60℃ for 45 s, extension at 72℃ for 120 s, as to the first five cycles, the annealing temperature of each cycle was 1℃ lower than that of the previous one, and after reducing to 55℃, 30 cycles need to be performed, and then extended at 72℃ for 10 min, and finally kept at 12℃. The ABI Stepone plus quantitative PCR instrument was used for fluorescence quantitative PCR, and the operation was carried out according to the instructions of SYBR Green PCR Master Mix (Applied biosystems) kit. In order to ensure the specificity of primers, the 3’- end primers were designed in untranslated sequences, the specificity of primers was checked on the Wheat Gene Index database (http://blast.jcvi.org/euk-blast/index.cgi?project=tae1) website, and the melting curve presented a single peak. The expression of housekeeping gene TaRP15 did not change under drought and heat stress. Three replicates were set up.

Table 2 Primers sequences listed

3.4 Bioinformatics analysis

the URGI (https://urgi.versailles.inra.fr/blaST/?dbgroup=wheat_all&program=blaSTn) was used for obtaining the physical location of TaFTSH6 gene based on the known sequence of wheat. According to the obtained positioning, cDNA sequences were obtained from (http://202.194.139.32/). The intron exon analysis of TaFTSH6 gene was performed in FGENESH HMM based Gene Structure prediction of Softberry. The FTSH6 sequences of other species were searched through BLASTX (http://www.ncbi. nlm.nih.gov/) on NCBI website. In MEGA10.0, ClustalW method was used for multi sequence alignment analysis, and then neighbor-joining method (bootstrap=1000) was used to construct evolutionary tree. The transmembrane domain analysis was performed on (http://www.cbs.dtu.dk/services/TMHMM-2.0/). The analysis of cis-acting elements of promoter was performed on (http://bioinformatics.psb.ugent.be/webtools/plantcare/html).

Authors’ contributions

LY was the executor of this study, completing data analysis and writing the first draft of the manuscript; JHJ participated in designing the experiments and analyzing the results; LJ and LYG were the conceivers of the project. HXJ directed the experimental design, data analysis, manuscript writing and revision. All authors read and approved the final manuscript.

Acknowledgments

This study was jointly funded by Public Welfare Projects of Key Research and Development in Shandong Province (No.2017NC210010) and National Key Research and Development Projects in China (No.2017YFD0301003).

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