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Acta Agronomica Sinica ›› 2023, Vol. 49 ›› Issue (9): 2331-2343.doi: 10.3724/SP.J.1006.2023.23069

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

Identification of ZmC2s gene family and functional analysis of ZmC2-15 under heat tolerance in maize

HUANG Yu-Jie(), ZHANG Xiao-Tian, CHEN Hui-Li, WANG Hong-Wei(), DING Shuang-Cheng()   

  1. Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River, Ministry of Agricultural and Rural Affairs (Co-construction by Ministry and Province), College of Agriculture, Yangtze University, Jingzhou 434025, Hubei, China
  • Received:2022-10-11 Accepted:2023-02-10 Online:2023-09-12 Published:2023-02-22
  • Supported by:
    National Natural Science Foundation of China(31701439)

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Abstract:

The objective of this study is to identify the members of maize ZmC2s gene family, to analyze the association between their genetic variations and heat tolerance, and to lay a foundation for clarifying its function and molecular mechanism in maize heat tolerance. Using the C2 protein domain PF00168, hmmsearch was applied to search for the members of the ZmC2s gene family from maize B73 genome. The protein isoelectric point, molecular weight, phylogenetic evolution, and gene family replication were analyzed. Using the method of candidate gene association analysis, the association between the natural variations of ZmC2s and the heat tolerance of maize seedlings was conducted, and the important heat-tolerant candidate genes of maize ZmC2s gene family were found. The relative gene expression level of the heat-tolerant candidate gene under stress was identified by Real time fluorescent quantitative PCR (RT-qPCR). The subcellular expression sites of heat-tolerant candidate gene were identified by transforming maize protoplasts. A total of 95 maize ZmC2s genes were identified from the reference genome B73 in maize. According to the order of their physical coordinates, 95 maize ZmC2s genes were named from ZmC2-1 to ZmC2-95, respectively. The length of the 95 proteins was 130-2141, the isoelectric point was 4.1-10.8, and the molecular weight was 14.1-230.1. The evolution tree of C2 gene in maize, rice, and sorghum genomes was constructed. We found that C2 genes can be divided into three major cluster branches, and each cluster branch can be subdivided into two small cluster branches. Analyzing the whole genome collinearity data of maize, rice, and sorghum, 59 ZmC2s genes were detected to have corresponding replication genes in rice and sorghum genomes. A candidate-gene based on the association analysis of ZmC2s showed that ZmC2-15/60/91 were important candidate genes for heat tolerance in maize (P ≤ 0.001, MLM), among which ZmC2-15 was the most significantly associated to heat tolerance at seedling stage (P ≤ 0.000,01, MLM), and the relative expression level of ZmC2-15 was up-regulated under various stress treatments. Subcellular localization indicated that ZmC2-15 was localized in the cytoplasm, nuclear membrane, and endoplasmic reticulum. The overexpression of ZmC2-15 improved plant heat tolerance. ZmC2-15 can be used as an important candidate gene for regulating heat tolerance in maize.

Key words: maize, heat tolerance, C2 gene family, association analysis of candidate genes, subcellular localization

Fig. 1

Identification of ZmC2s gene family member and protein physicochemical properties analysis The number of introns (A), the exon number (B), protein molecular weight (C), protein isoelectric point (D), protein length (E), gene name (F), gene physical coordinates (G), and genBank accession number (H) for ZmC2 gene family members."

Fig. 2

Phylogenetic tree of C2 domain genes in maize, rice, and sorghum The phylogenetic tree was generated by comparing the amino acid sequences of the C2 domain in MEGA 7. All genes were divided into three groups, I, II, and III, using the neighbor joining method."

Fig. 3

Analysis of gene replication in maize C2 domain and rice and sorghum The gene duplication analysis of ZmC2s located on chromosomes 1, 2 (A), 3, 4 (B), 5, 6 (C), 7, 8, 9, and 10 (D) of rice and sorghum genome; E: the type and number of C2 gene replication in maize, rice, and sorghum genomes."

Fig. 4

Association analysis between genetic variation of ZmC2s with heat tolerance at seedlings stage in maize A: the number of genetic polymorphism markers in ZmC2s. The significant associated ZmC2s and the number of significant associated markers under (GLM, P ≤ 0.01). B: MLM, P ≤ 0.01; C: MLM, P ≤ 0.001; D: MLM, P ≤ 0.000,01; E: the number of genes and markers with significant associations among them; F: the coordinate of ZmC2s; G: ZmC2s gene names; H: QQplot of association analysis of genetic variation of ZmC2 gene with heat tolerance; association analysis of genetic variations in ZmC2-15 (I), ZmC2-60 (J), and ZmC2-91 (K) genes with heat tolerance in maize seedlings."

Fig. 5

Relative expression pattern of ZmC2-15 genes under high temperature (A), drought (B), low temperature (C), ethephon (D), sodium chloride (E), hydrogen peroxide (F), gibberellin (G), ABA (H), and salicylic acid (I) Bar shows mean ± SD. *: P ≤ 0.05; **: P ≤ 0.01; t-test."

Fig. 6

Localization of ZmC2-15-GFP in maize protoplast A: the subcellular localization of GFP protein in maize protoplast; B: the subcellular localization of ZmC2-15-GFP in maize protoplasts after adding nuclear fuel. ZmC2-15-GFP refers to pGreenII-35SΩ-ZmC2-15-GFP, 35S:GFP refers to pGreenII-35SΩ-GFP."

Fig. 7

Subcellular co-localization of ZmC2-15-GFP with ERD2-mCherry (A), ST-mCherry (B), VHA-A1-mCherry (C), and HDEL- mCherryL (D) in maize protoplasts HDEL-mCherry, ERD2-mCherry, ST-mCherry, and VHA-A1-mCherry are used as the protein localization markers for endoplasmic reticulum, cis golgi, golgi, and reverse golgi, respectively."

Fig. 8

Heat stress tolerance of ZmC2-15 transformed Arabidopsis A: before heat treatment; B: after heat treatment; C: primer locations and semi quantitative analysis; D: the histogram of survival rate of VC and transgenic Arabidopsis. VC represents empty-vector pGreenII-35SΩ transformation of Arabidopsis. Bar shows mean ± SD. The values were calculated from three biological replicates, and the total number of individual plants is 30 for each one of VC, OE1, and OE2. *: P ≤ 0.05; **: P ≤ 0.01; t-test."

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