Research Report

Analysis of resistance to alkaline salt stress in Arabidopsis thaliana with overexpression of OsiSAP1 gene  

Songmiao Hu , Jiali Liu , Yiteng Zhang , Haiyan Ma , Xiaoxu Dong , Qingjie Guan
Key Laboratory of Saline and Alkali vegetation Rehabilitation and Reconstruction in Northeast China ,School of Life Science ,Northeast Forestry University,Harbin 150040,China
Author    Correspondence author
Genomics and Applied Biology, 2020, Vol. 11, No. 2   
Received: 21 Apr., 2020    Accepted: 23 Apr., 2020    Published: 10 Jul., 2020
© 2020 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

The purpose of this study was to study the stress effects of rice ISAP transcription factor family containing zinc finger proteins of A20/AN1 domain and the mechanism of saline-alkali tolerance during rice growth and development. In this study, the ORF reading frame of OsiSAP1 (LOC_Os09g31200) gene 513bp was cloned from the leaves of rice Oryza sativa. L11, and the homology ratio NCBI 170 amino acids was as high as 71.51% with Panicum miliaceum L. The phylogenetic tree based on the nucleotide comparison of the open reading frame shows that it is on the same branch as Oryza officinalis. Through qRT-PCR detection in various tissues and organs of rice Oryza sativa. L11: root, stem, leaf and anther, it was found that the expression of mRNA in root was higher, and Gene gun-transformed onion epidermal cell method detected fluorescence signal of 35S-OsiSAP1-GFP fusion protein localized in the nucleus. The analysis of salt-alkali tolerance of rice overexpressing OsiSAP1 gene showed that the fresh weight and root length of transgenic lines were better than those of wild-type lines at germination stage and late germination stage under NaHCO3 treatment. It is speculated that OsiSAP1 transcription factors are involved in the regulation of saline-alkali tolerance in rice.

Keywords
Arabidopsis thaliana; Stress protein; Alkaline salt stress; Expression characteristics

Background

Plant growth and development are constantly challenged by changes in environmental conditions. in order to be able to effectively photosynthesis under stress, plants respond to stress through complex physiological and molecular changes. The stress response eventually induces signaling and regulation of a range of functional genes and their regulatory elements that initiate protein expression synthesis in their respective classes, including functional enzymes, transcription factors, molecular chaperones, ion channels and transporters, or stimulate changes in their activity (Mehrotra et al., 2014; Rajesh et al., 2014). At present, scholars have reported the transcription factors AP2/EREBP, bZIP, MYB/MYC (Martin and Paz-Ares, 1997; Naing and Kim, 2018), NAC and WRKY (Eulgem et al., 2000) under the drought and salt stress. Stress-related proteins (SAPs) are transcription factors expressed in response to abiotic stresses that contain A20/AN1 domains (Xu et al., 2008). Previous studies have reported that human SAPs proteins can play a negative role in regulating the immune function of NF-KB pathway induced by TNF regulation (Solanke et al., 2009; Gao et al., 2016). From the nature of induction, ISAPs gene family products may play a good role in the early stage of signal transduction pathway in stress response (Mukhopadhyay et al., 2004).

 

According to incomplete statistics, the rice genome (430 Mb) is the smallest of cereal crops, many of which are "housekeeping" genes expressed in all tissues, and are unique to its tissues and organs, as well as transcription induced by environmental induction Regulatory genes (Burr, 2002; Mukhopadhyay et al., 2004). Rice ISAPs polygenic family consists of 18 members (Ben-Saad et al., 2012), each involved in different biological pathways of rice physiology. Some progress has been made in studying the functional effects of OsiSAP1, OsiSAP8, OsiSAP9/ZFP177 and OsiSAP11 genes, which can improve the tolerance to abiotic stress (Dixit and Dhankher, 2011; Gimeno-Gilles et al., 2011; Kang et al., 2011). A study of the SAPs family is mostly based on the analysis of its genetic properties. The area of saline-alkali soil in Northeast China is as high as 6.2% (7.66 million hectares), and the sodas-alkali soil is close to a fifth of the cultivated land (Zhu et al., 2007), but OsiSAPs proteins involved in the regulation of plant alkaline salt resistance mechanism is not very clear, it is necessary to further study.

 

The protein OsiSAP1 genes related to stress were cloned from rice Oryza sativa. L11, and the expression of mRNA tissues and organs was detected by qRT-PCR technique; Further analysis of the induced expression characteristics of soda alkaline salt (NaHCO3) under stress; validation of its protein subcellular localization and functional location; By examining the comparative study between transgenic Arabidopsis thaliana and wild-type at the seed germination/seedling stage, it is stated that OsiSAP1 gene is involved in improving the tolerance of alkaline salts. In order to improve the resistance of rice no alkaline salt, it provides theoretical basis for the application of new rice lines.

 

1 Results and Analysis

1.1 Bioinformatics analysis

The sequencing results showed that the sequence length of the target gene was 510 bp, encoding 170 amino acids, and its structure was characterized by the inclusion of A20/AN1 domain, that is, the end of the N is the A20 structure, the end of the C is the AN1 structure (Figure 1A, Figure 1B), and the molecular weight of the protein was 18 KD, and the isoelectric point was 9.14. Clustal Omega analysis shows that Oryza officinalis is in the same evolutionary branch with 72.06% homology (Figure 1C).

 

 

Figure 1 Bioinformatics analysis of OsiSAP1 Gene

Note: A: Amino acid sequence homology alignment; B: Structure analysis; C: NJ method to construct phylogenetic tree

 

1.2 Expression of OsiSAP1 genes in different tissues and organs of rice

qRT-PCR detection of differences in the expression characteristics of OsiSAP1 genes in different tissues and organs of rice showed that they were expressed in the roots, stems, leaves, flowers, spikes, pelicans, spikes, flag leaves and other parts of rice (Figure 2). moreover, it can be seen that the expression of OsiSAP1 genes in the eight tissues of rice was not the same, the highest expression in spike was 15 times that in relative root, but lower in root and leaf.

 

 

Figure 2 Different tissues and organs expression analysis of OsiSAP1 gene

 

1.3 OsiSAP1 gene expression under stress

qRT-PCR techniques were used to detect the correlation between OsiSAP1 genes and plant resistance to abiotic stress and to analyze the expression characteristics of their mRNA under alkaline salt (NaHCO3) stress. The experiment showed that OsiSAP1 gene was obviously induced by alkaline salt stress, and the transcription level increased with the prolongation of NaHCO3 stress time. OsiSAP1 the expression in the leaves increased steadily and remained increasing at 48 h (Figure 3A), the expression in the root showed an overall growth trend, reaching the highest sharp increase at 12 h, about 16 times that of the control group, and decreased after 12 h, but the overall expression was still increasing, about 8 times higher than that in the control group (Figure 3B); The experimental results showed that OsiSAP1 expression was up-regulated by alkaline salt stress, Under NaHCO3 stress, the maximum expression in leaves was about 2 times higher than that in normal conditions and about 2 times higher in roots. It can be seen that OsiSAP1 is related to resistance to alkaline salt stress.

 

 

Figure 3 Real-time quantitative expression analysis of OsiSAP1 gene under stresses of salt (NaCl), alkali (NaHCO3)

 

1.4 OsiSAP1 protein subcellular localization

The onion epidermal cells were bombarded with a gene gun, and the plasmid was DNA pBS-MCS-GFP、pBS-OsiSAP1-GFP into the onion epidermal cells. after 24 h, the onion epidermal cells were torn off to make a tablet. GFP fluorescence was detected by microscope: the fusion protein of 35 S-OsiSAP1-GFP with OsiSAP1 gene showed green fluorescence in the nucleus. It was known that the OsiSAP1 plasmid was localized in the nucleus and speculated that the OsiSAP1 exercised its biological function in the nucleus (Figure 4).

 

 

Figure 4 OsiSAP1 located in onion epidermal cells

Note: a, b, c: Fluorescence, white light and overlapping field of view transiently express 35S-GFP onion epidermal cells as controls; d, e, f: Fluorescence, white light and overlapping field of view transiently express 35S-OsiSAP1-GFP onion epidermal cells

 

1.5 Analysis of alkaline salt resistance of transgenic Arabidopsis thaliana OsiSAP1

1.5.1 Molecular Detection of Transgenic OsiSAP1 Arabidopsis Plants

Detection of Hyg-resistant T2 Arabidopsis strains with specific primers(B11-R/pBI121JC-F) designed by pGWB11 vector sequence. The results showed that the amplified product size was 500 bp (T2#1,2,3,4,5,6), which was consistent with the positive control, while the wild-type Arabidopsis as a negative control (CK-) showed no target band (Figure 5), indicating that the OsiSAP1 genes had been successfully integrated into the chromosomes of the above plant genomes.

 

 

Figure 5 T2 generation of pGWB11-OsiSAP1-Flag transgenic Arabidopsis detected by PCR

Note: M: DM2000 Plus; CK+: Amplified product using pGWB11-OsiSAP1-Flag as template; CK-: Amplified product using wild-type genomic DNA as template; 1~6: Amplification product of T2 generation transgenic Arabidopsis 1 #, 2 #, 3 #, 4 #, 5 #, 6 # strain genomic DNA as template

 

1.5.2 Alkaline Resistance Analysis of Transgenic OsiSAP1 Arabidopsis

Wild-type (WT) and trans-OsiSAP1 Arabidopsis growth were not inhibited under the alkaline salt NaHCO3 stress control group (Figure 6). however, in the NaHCO3 stress treatment group (Figure 6), germination growth was inhibited, and plants are seriously injured under stress of greater than 6mM NaHCO3 and do not germinate. Fresh weight under alkaline salt stress (Figure 6) data indicate that the fresh weight of trans OsiSAP1 gene lines is greater than that of wild type. Resistance experiments during germination showed that the transgenic arabidopsis thaliana strain ratio WT showed a certain resistance to alkaline salt growth characteristics. It can be speculated that the OsiSAP1 gene reduces the damage of alkaline salts by regulating the expression of related genes and improves the tolerance of plants to alkaline salts.

 

 

Figure 6 Resistant analysis of transgenic Arabidopsis over-expressing OsiSAP1 germination

Note: A: Wild-type and overexpressed OsiSAP1 Arabidopsis thaliana grown on different stress NaHCO3 stress plates for 14 days; B: Fresh weight

 

1.5.3 Alkaline OsiSAP1 Growth in Arabidopsis thaliana Transgenic

In NaHCO3 treatment group, 0 mmol/L, 2 mmol/L, 4 mmol/L, 6 mmol/L, 8 mmol/L NaHCO3 Arabidopsis leaf growth was not significantly inhibited, under 10 mmol/L and 12 mmol/L NaHCO3 stress (Figure 7Af; Figure 7Ag), The leaves appear yellowed. Root length measurement results showed that under 2 mM and 4 mM NaHCO3 stress, the root growth of transgenic lines was significantly better than that of wild type, and the fresh weight of 4 mmol/L and 6 mmol/L NaHCO3 transgenic plants was significantly better than WT. The malondialdehyde content of transgenic Arabidopsis thaliana under 4 mmol/L, 6 mmol/L, 8 mmol/L, and 10 mmol/L treatments was significantly lower than that of wild type. The analysis of the alkaline salt stress experiment results in the late germination showed that the OsiSAP1 gene lines overexpressing wild-type Arabidopsis had increased resistance to alkaline salt stress, and it was speculated that the OsiSAP1 gene might be involved in the regulation of alkaline salt resistance.

 

 

Figure 7 Resistance of Arabidopsis overexpressing OsiSAP1 gene to NaHCO3 stress at the later stage of germination

Note: A/B-a,b,c,d,e,f,g: Wild-type and overexpressed OsiSAP1 Arabidopsis on 1/2 MS+0 mmol/L, 2 mmol/L, 4 mmol/L, 6 mmol/L, 8 mmol/L, 10 mmol/L, 12 mmol/L NaHCO3 plates Phenotype that grows for three weeks; C: Root length; D: Fresh weight; E: Malondialdehyde

 

2 Discussion and Conclusions

Plants have complex response stress systems through years of evolution, and a large number of genes are induced after various abiotic stresses (Seki et al., 2001). These genes function in a variety of ways, giving plants resistance to stress (Huang et al., 2009; Sharma et al., 2015), and the role of transcription factor regulation is important. The binding of transcription factors to specific sequences in the promoter of the target gene is involved in the regulation (Solanke et al., 2009; Aijia et al., 2015). Rice OsiSAP1 encodes a stress-related protein containing a single repetitive A20/AN1 zinc finger domain (Figure 1); the zinc finger structure is a tripeptide segment composed of a α- spiral and two β- folded sheets in parallel directions, shaped like a finger, and has the function of binding zinc ions. by domain comparison, it was found that the gene of Aegilops tauschii Coss. wheat coding stress related proteins on the same evolutionary branch was highly homologous. This result is consistent with that reported by Sreedharan et al. (2012). The distribution of stress-related protein family proteins in the nucleus and cytoplasm (Kang et al., 2011). This study observed that the fluorescence signal of the trans OsiSAP1-GFP fusion protein was localized in the nucleus, the same as the transcription factor AtSAP5 (Kang et al., 2013) located in the nucleus, and different from the OsiSAP8 (Kanneganti and Gupta, 2008) localization in the cytoplasm. The up-regulated expression of OsiSAP1 in response to NaHCO3 stress in rice leaves and roots was detected by fluorescence quantitative PCR (Figure 2), Southern blot analysis showed that OsiSAP1 was up-regulated by hormones, drought and salt NaCl, which was the same as Mukhopadhyay et al. (2004). infer that OsiSAP1 is involved in regulating the alkaline salt stress pathway. Transgenic technology has become an important means of scientific research, widely used in crop breeding and research plant stress related gene function (Ahmad et al., 2012; Nakashima et al., 2012), the ability of overexpressed OsiSAP1 Arabidopsis thaliana strains to resist alkaline salt (NaHCO3) stress in germination/seedling stage was higher than that in wild type (Figure 6, Figure 7), OsiSAP1 proteins play a positive role in responding to alkaline salt stress and improve resistance to alkaline salt stress. From this, it is speculated that OsiSAP1 may indirectly or directly regulate stress resistance-related genes, which provides experimental basis for further application of OsiSAP1 transcription factors to regulatory pathways that respond to alkaline salt stress to enhance plant resistance.

 

3 Materials and Methods

3.1 Material

3.1.1 Plant materials

Arabidopsis thaliana-0 (Colombian seed); Oryza sativa. L11 seeds were provided by the Northeast Institute of Geography and Agricultural Ecology, Chinese Academy of Sciences; Allium sativum L. were purchased from the market.

 

3.1.2 Strain and vector

DH5α competent cell (E. coli); EHA105 competent cell (Agrrobcrcterumtumefaciens) are preserved by the Key Laboratory of Saline and Alkali vegetation Rehabilitation and Reconstruction in Northeast China, School of Life Science, Northeast Forestry University.

 

The pMD18-T carrier was purchased from TaKaRa Company; the green fluorescent fusion protein localization expression vectors pBS-ΔMCS-GFP and pGWB11 were kept by our laboratory.

 

3.1.3 Experimental reagents and medicines

Gate way system carrier build kit is purchased from Invitrogen company; T4DNA-Ligase ligase, fast restriction endonuclease are purchased from Fermentas company; DNA Gel Extraction Kit, PurePlasmid Mini Kit are purchased from Beijing ComWin Biotech company; Trizol Reagent reagent is purchased from Invitrogen company; Ex-Taq and Primer star DNA polymerase, Ampicillin (Amp), Kanamycin (Kana) are purchased from TaKaRa Company; Reverse transcriptase kit are purchased from TOYOBO company; Other reagents used are domestic analytical reagents.

 

3.1.4 Experimental medium

(1) MS medium: MS (Murashige-skook)+0.8% Agar+3% sucrose, Adjust PH value to 5.8; 1/2 MS Medium: Halve the organic and mineral elements (iron removal) of the MS medium.

(2) LB medium: 0.5% yeast extract, 1% Tryptone, 1% NaCl.

(3) YEP medium: 1% yeast extract, 1% Tryptone, 0.5%NaCl; solid medium was added 1.5% respectively.

(4) Agrobacterium tumefaciens infection solution: sucrose, MES, added SilwetL-770.02%(v/v) and 6- BA (0.044μm, instead of BAP) before use.

 

3.1.5 Primers

Primers Composed by Comate Biosciences Co. Ltd. (Table 1).

 

 

Table 1 Primer Names and Sequences

 

3.2 Experimental methods

3.2.1 Rice OsiSAP1 gene cloning and bioinformatics analysis

The rice OsiSAP1 (LOC_Os09g31200) gene is a cDNA that is reverse transcribed from rice total RNA as a template, and a specific primer (OsiSAP1-RT-F/R) is designed based on the gene registered in GenBank, and the cDNA fragment of the known gene is cloned by PCR. The ORF region and amino acid analysis isoelectric point are deduced (https://www.expasy.org/), and the domain is analyzed by bioinformatics SMAT software (http://smart.embl-heidelberg.de/smart/set_mode.cgi?NORMAL=1), MAGA software analysis homology. (http://www.ebi.ac.uk/Tools/msa/clustalo/).

 

3.2.2 OsiSAP1 gene expression characteristics

Eight organs at different stages of Oryza sativa. L11 development were extracted: total RNA of roots, stems, leaves, flowers, spikes, barn, ear stems and flag leaves, was extracted by Trizol method, and cDNA was obtained by reverse transcription. SYBR Green qRT-PCR fluorescent dye method was used to determine the gene expression of OsiSAP1. Using rice Rubq1 as the internal reference gene (Rubq1-F/R), a specific primer (qRT-OsiSAP1-F/R) was designed to perform PCR reaction using 2×Brilliant III SYBR Green QPCR Master Mix (Agilent).

 

Oryza sativa. L11 was hydrotreated to the three-leaf stage and treated with 100 mM NaCl and 50 mM NaHCO3, respectively. Stress time was set to 0 h, 6 h, 12 h, 24 h, 48 h, sterile water was used to the control group, roots and leaves were frozen storage. Extract RNA from roots and leaves of different stress treatment groups, and reverse transcribe to get cDNA as a template, primers (qRT-PCR-F/R) were used to Real-Time PCR, the relative expression of OsiSAP1 genes was calculated by the system. the results were analyzed by data using Excel.

 

3.2.3 OsiSAP1 protein subcellular localization

Kpn1/Spe1 enzyme digestion sites were added to design primer (OsiSAP1-GFP-F/R) PCR amplification, and two kinds of enzyme digestion was used to construct PBS-OsiSAP1-GFP vector. PBS-35S-OsiSAP1-GFP and PBS-35S-GFP (positive control) were bombarded with gene gun to observe the green fluorescence expression of fusion protein under laser confocal microscope (Olympus).

 

3.3 Expression and resistance analysis of Rice OsiSAP1 gene in Arabidopsis thaliana

3.3.1 Construction of plant expression vector pGWB11-OsiSAP1-Flag and transformation of Arabidopsis thaliana

The primer (ChIPISAP1-F/R) was inserted into pENTR/D-TOPO Vector by PCR technology, and the pGWB11-OsiSAP1-Flag plant expression vector was constructed by LR reaction, and electroporation was introduced into Agrobacterium EHA105 to prepare the working solution to infect and transform Arabidopsis thaliana (Clough and Bent, 1998). T0 generation Arabidopsis thaliana seeds were sterilized and germinated on hygromycin (Hygromycin 35 mg/L) resistant plate, and hygromycin resistance was used to screen transgenic T1 generation plants. the next generation of Arabidopsis thaliana transgenic lines were screened by hygromycin. Genomic DNA of the leaves was extracted by CTAB method, and the primers (B11-R/PBI121-JCF) were used for PCR identification to obtain T3 generation seeds of transgenic lines.

 

3.3.2 Analysis of alkaline salt tolerance of transgenic Arabidopsis thaliana OsiSAP1

Transgenic Arabidopsis thaliana T3 generation and wild type were added to 1/2 MS solid medium with 2 mmol/L, 4 mmol/L, 6 mmol/L, 8 mmol/L, 10 mmol/L and 12 mmol/L NaHCO3 for screening analysis of transgenic Arabidopsis resistance, and the germination was observed after 2 weeks of cultivation. 1/2 MS medium is the control group, and the phenotype is examined after two weeks of cultivation; fresh weight, root length, and malondialdehyde content are measured.

 

The T3 generation plants and WT seeds were sterilized and sterilized and evenly sown on 1/2 MS medium. After vernalization at 4°C for 2 days, they were cultivated in an incubator. After 2 weeks of growth, seedlings of uniform growth were selected and inoculated to 1/2 MS+2 mmol/L, 4 mmol/L, 6 mmol/L, 8 mmol/L, 10 mmol/L, and 12 mmol/L NaHCO3 medium, the growth was investigated after 2 weeks, and plant physiological tests were conducted.

 

Authors contributions

Guan Q.J. conceived and designed the study. Hu S.M. and Liu J.L. performed the experiments and drafted the manuscript. Ma H.Y., and Dong X.X. contributed to the sample measurement and data analysis. Guan Q.J. Hu S.M. and Zhang Y.T draft revision. All authors read and approved the final manuscript.

 

Acknowledgements

Thank you for the Heilongjiang Science Fund Project (C2017009) and funded central university basic research business special fund project (2572019DF11).

 

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