Scientia Agricultura Sinica ›› 2021, Vol. 54 ›› Issue (21): 4500-4513.doi: 10.3864/j.issn.0578-1752.2021.21.002

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Over-expression of ZmIBH1-1 to Improve Drought Resistance in Maize Seedlings

ZHU FangFang(),DONG YaHui(),REN ZhenZhen,WANG ZhiYong,SU HuiHui,KU LiXia,CHEN YanHui()   

  1. College of Agronomy, Henan Agricultural University/National Key Laboratory of Wheat and Maize Crop Science, Zhengzhou 450046
  • Received:2021-04-25 Accepted:2021-06-16 Online:2021-11-01 Published:2021-11-09
  • Contact: YanHui CHEN E-mail:1261546452@qq.com;1018661461@qq.com;chy9890@163.com

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Abstract:

【Objective】Drought is an important factor that affects the growth and development of maize seriously. Through the mining of genes related to drought resistance in maize, transgene function verification and transcriptome analysis, analyzing the molecular regulation mechanism of key genes in response to drought stress, this paper provides the theoretical basis for drought resistance molecular breeding and genetic improvement. 【Method】In this study, the maize inbred line B104 (wild-type, WT) was used as the background to construct the ZmIBH1-1 overexpression (ZmIBH1-1-OE) transgenic line by Agrobacterium-mediated method. The transgenic plants and lines were identified via screening transgenic plants for glufosinate-ammonium resistance, PCR detection of marker gene and target gene and expression analysis of target gene by qRT-PCR. We used the ZmIBH1-1-OE and WT transgenic lines as materials. Through drought treatment (20% PEG6000), phenotype identification and drought tolerance physiological and biochemical index determination were carried out to verify the drought resistance function of ZmIBH1-1; RNA-Seq was used to identify differentially expressed genes (DEGs) under drought stress at the 4-leaf stage; Combined with DAP-seq (DNA affinity purification sequencing) analysis, it is preliminarily determined that ZmIBH1-1 protein directly regulates downstream target genes related to drought resistance, and IGV (Integrative Genomics Viewer) was used to analyze the position of the ZmIBH1-1 protein binding candidate target gene, and then the Dual-Luciferase assay was used to verify the regulatory relationship between ZmIBH1-1 protein and target genes. 【Result】12 transformation events were obtained by genetic transformation of maize. In the T3 generation, there were 458 plants in which the marker gene Bar and the target gene ZmIBH1-1 were simultaneously detected. The results of qRT-PCR showed that the expression level of ZmIBH1-1 in ZmIBH1-1-OE lines was significantly higher than that of WT and the expression levels of transformation events 3 and 8 were the highest, which were self-crossed to obtain T4 generation for subsequent experiments. Under drought stress, the survival rate, the relative water content, the chlorophyll content, soluble protein content and the physiological and biochemical indicators (superoxide dismutase, peroxidase, catalase activity) of ZmIBH1-1-OE were higher than those of WT significantly, which indicating that the overexpression of ZmIBH1-1 in maize confers higher drought tolerance. The RNA-Seq results showed that there were 1 214 DEGs between WT and ZmIBH1-1-OE lines. Gene Ontology (GO) analysis showed that DEGs were mainly involved in biological processes, cell components and molecular functions, such as photosynthesis, stress response, dehydration response, etc. in biological processes; KEGG enrichment analysis showed that DEGs were mainly involved in the signal transduction of plant hormones, the metabolism and other processes. Combining the significantly DEGs of RNA-Seq and the target genes of ZmIBH1-1 obtained from DAP-seq analysis, it is preliminarily identified 11 candidate target genes related to drought resistance that may be directly regulated by ZmIBH1-1, including 2 calcium signal related genes, 3 cysteine metabolism related genes, 1 bHLH transcription factor, 1 stress response protein, 1 glutathione transferase, 1 redox process protein and 2 ethylene response factor; Integrative genomics viewer showed that ZmIBH1-1 protein could bind to the promoters of the target genes; Subsequent Dual-Luciferase assay further showed that ZmIBH1-1 protein can directly act on 11 candidate target genes, of which, ZmIBH1-1 directly binds to the promoters of ZmCa-M, ZmSYCO, ZmbHLH54, ZmGlu-r1, ZmCLPB3 and ZmP450-99A2 to promote their expression, and directly binds to the promoters of ZmAGD12, ZmCYS, ZmCYSB, ZmERF-107 and ZmEIN3 to repress their expression. In addition, transcription factors such as NAC, WRKY and MYB also differentially expressed between WT and ZmIBH1-1-OE under drought stress. 【Conclusion】The overexpression of ZmIBH1-1 can enhance the drought tolerance of maize; ZmIBH1-1 improves the drought tolerance of maize by directly regulating the expression of genes ZmERF-107 and ZmEIN3 in the ethylene signaling pathway; ZmIBH1-1 enhances the drought tolerance of maize by directly regulating the calcium signal-related genes ZmCa-M and ZmAGD12; ZmIBH1-1 may indirectly regulate NAC, WRKY, MYB and other transcription factors in response to drought stress.

Key words: maize, drought stress, ZmIBH1-1, RNA-Seq, transcription factor, gene expression

Fig. 1

Schematic diagram of the T-DNA region of the ZmIBH1-1 overexpression recombinant plasmid LB: Left border repeat of T-DNA; Tnos: Terminator; Bar: Herbicide screening gene; PMAS: MAS promoter; P35S: 35S promoter; ETMV: TMV enhancer; RB: Right border repeat of T-DNA"

Table 1

Primers used in the study"

引物名称
Primer name		 引物序列
Primer sequence (5′-3′)
Bar-F CATCGAGACAAGCACGGTC
Bar-R AAACCCACGTCATGCCAGTT
ZmIBH-F CAATTACATTTACAATTACCATGGTCATGGCCAGGAAGAGGAC
ZmIBH-R CTCTCTAGACTCACCTAGGATCCTCATTGGGCGGAGAAG
qIBH-F AGGAACCACCGCCAAACC
qIBH-R GCHTCTCCGCAGCAGGAC
Tublin-F CCGCTATCTCCGTCGC
Tublin-R GTTCTTGGATGGCGGTCG

Fig. 2

Identification of some T3 transgenic maize plants A: Phenotypic identification of herbicide glyphosate sprayed or applied; B: PCR detection of Bar; C: PCR detection of IBH1-1. WT: Wild-type plant; T: Transgenic ZmIBH1-1-OE plant; 1: Positive control (plasmid DNA); 2: Blank; M: DL5000 DNA Marker; The rest represent transgenic plants"

Fig. 3

Expression of ZmIBH1-1 in 12 transformation events lines WT: Wild-type plant; 1-12: 12 transformation events of ZmIBH1-1-OE lines (n=3, ±SD, **P<0.01)"

Fig. 4

Phenotype and physiological changes of ZmIBH1-1-OE and wild type B104 lines under drought stress A: The phenotype of B104 and ZmIBH1-1-OE lines under PEG6000 stress; B: Mean survival rate of B104 and ZmIBH1-1-OE lines under PEG6000 stress (n=3, ±SD, **P<0.01, n.s not significant); C: Mean relative water contents (RWCs) of B104 and ZmIBH1-1-OE lines under PEG6000 stress (n=3, ±SD, **P<0.01, n.s not significant); D: Determination of POD, SOD and CAT enzyme activities of B104 and ZmIBH1-1-OE strains under PEG6000 stress (n=3, ±SD, **P< 0.01, n.s not significant); E: Determination of the contents of Cht, Car and SP of B104 and ZmIBH1-1-OE strains under PEG6000 stress (n=3, ±SD, **P<0.01, n.s not significant)"

Table 2

The summary of reads analysis from RNA-Seq data"

样品
Sample		 正常条件Normal 干旱胁迫Drought stress
原始reads
Raw reads		 过滤后的reads
Clean reads		 过滤后的
reads所占比
Reads keep rate (%)		 比对上的
reads
Mapped reads		 比对上的
reads占比
Mapped reads rate (%)		 原始reads
Raw reads		 过滤后的
reads
Clean reads		 过滤后的
reads所占比
Reads keep rate (%)		 比对上的reads
Mapped reads		 比对上的
reads占比
Mapped reads rate (%)
WT-1 5407756 5032404 93.05 4492503 89.27 3870308 3532833 91.28 3128759 88.56
WT-2 7232533 6586333 91.06 5987305 90.90 4119004 3813323 92.57 3482561 91.32
OE-1 8523635 7780152 91.27 6893250 88.60 6322179 5776743 91.37 5367210 92.91
OE-2 7647821 6977539 91.23 6289035 90.13 6994016 6490634 92.80 5901352 90.92

Fig. 5

RNA-Seq analysis of B104 and ZmIBH1-1-OE lines under normal and drought conditions A: PCA analysis of RNA-Seq. p represents PEG treatment, 0 h represents normal conditions, 1 and 2 represents two biological replicates respectively; B: Correlation analysis of RNA-Seq; C: The expression of ZmIBH1-1 in B104 and ZmIBH1-1-OE lines under normal/drought stress (n=2, ±SD, **P<0.01)"

Fig. 6

IGV showed that ZmIBH1-1 had peaks enrichment in the promoter region of some target genes A-D represents that ZmIBH1-1 can bind to the promoter region of target genes ZmEIN3, ZmERF-107, ZmCLPB3, and ZmAGD12, respectively. The red box represents the location of ZmIBH1-1 binding peaks"

Fig. 7

Regulation of target genes by ZmIBH1-1 A: The 35S: REN-Pro gene LUC reporter constructs were transiently expressed in N.benthamiana leaves together with control vector or 35S:ZmIBH1-1 effector, respectively. The expression level of REN was used an internal control; B-C: The LUC/REN ratio represents the relative activity of promoters. Data are values of three independent experiments. Significant differences from the corresponding control values (n=3, ±SD, **P<0.01). NC: Negative control"

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