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Acta Agronomica Sinica ›› 2025, Vol. 51 ›› Issue (9): 2318-2329.doi: 10.3724/SP.J.1006.2025.53011

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

Identification and functional analysis of low temperature responsive genes ZmNTL1 and ZmNTL5 in maize

GAO Yuan**(), WANG Yu-Qi**(), JIANG Jia-Ning, ZHAO Jian-Xiong, WANG Xue-He-Yuan, WANG Hao-Yu, ZHANG Rui-Jia, XU Jing-Yu, HE Lin*()   

  1. Heilongjiang Bayi Agricultural University, Daqing 163319, Heilongjiang, China
  • Received:2025-02-19 Accepted:2025-06-01 Online:2025-09-12 Published:2025-06-10
  • Contact: *E-mail: linlinhe65@sina.com E-mail:644909333@qq.com;3496668542@qq.com;linlinhe65@sina.com
  • About author:**Contributed equally to this work
  • Supported by:
    National Natural Science Foundation of China(31701328);Postdoctoral Research Foundation of Heilongjiang Province(LBH-Q21160)

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Abstract:

Low temperature is one of the major abiotic stresses limiting maize yield in Northeast China. Membrane-bound NAC transcription factors play important roles in plant stress responses. Investigating their function provides a theoretical basis for breeding maize with enhanced cold tolerance. In this study, the molecular characteristics of nine maize NTL genes were analyzed using bioinformatics approaches. Analysis of publicly available RNA-seq data revealed that six of these genes were significantly upregulated by low temperature stress in both roots and leaves. Among them, ZmNTL1 and ZmNTL5, which share 80.04% sequence homology, were selected for further study. A double knockout mutant (zmntl1zmntl5) was generated using gene-editing techniques. Under low temperature stress, the ion leakage rate in the leaves of zmntl1zmntl5 was significantly higher than in the wild-type B104. The fresh and dry weights of both aboveground and belowground tissues, as well as chlorophyll content, were significantly lower in zmntl1zmntl5 compared to B104. In contrast, zmntl1zmntl5 exhibited significantly higher levels of O2- and H2O2, while the activities of antioxidant enzymes GST, SOD, POD, and CAT were significantly reduced. Furthermore, the expression levels of ZmGST24, ZmNCED3, ZmDREB1.6, and ZmDREB2A were markedly decreased in zmntl1zmntl5 compared to B104 under cold stress. In summary, the absence of ZmNTL1 and ZmNTL5 compromises cold tolerance in maize, suggesting that both genes function as positive regulators in the cold stress response. This study provides a valuable theoretical foundation and genetic resources for the improvement of cold-tolerant maize varieties and the development of new cultivars.

Key words: maize, low temperature, RNA-seq, NTL, gene editing

Table 1

Primers used in this study"

引物名称
Primer name		 序列
Sequence (5′-3′)		 作用
Function
pCPB-Cas9-F GACGGCCAGTGCCAAGCTTGCTGTTTTTGTTAGCCCCATCG 载体构建 Vector construction
pCPB-Cas9-R CTAGCTCTAAAACAATCCTGGTGGCAGGTGCATAATTCGGTGCTTGC 载体构建 Vector construction
ZmNTL1-F CTTCTGCATTTCTAGGCATGATTG 测序 Sequencing
ZmNTL1-R CCGTCTATCTGCCTATGATTCTCAA 测序 Sequencing
ZmNTL5-F CTCGGGTGCTGTGTTTCTGTTTG 测序 Sequencing
ZmNTL5-R GAGGATACAGATTGACAGGCATCACTT 测序 Sequencing
ZmUbi-F TGGTTGTGGCTTCGTTGGTT 实时荧光定量PCR qRT-PCR
ZmUbi-R GCTGCAGAAGAGTTTTGGGTACA 实时荧光定量PCR qRT-PCR
ZmGST24-F CCGGAGTGCACCTGATAGC 实时荧光定量PCR qRT-PCR
ZmGST24-R TGACCCACGACTTGTACCTC 实时荧光定量PCR qRT-PCR
ZmNCED3-F CCGAGGAAAGCGGACGG 实时荧光定量PCR qRT-PCR
ZmNCED3-R CGTAGACCCCGTCGATGAAG 实时荧光定量PCR qRT-PCR
ZmDREB1.6-F TTGAGGTGGATGTGTTCGGC 实时荧光定量PCR qRT-PCR
ZmDREB1.6-R CCACAGCTCCATCTCACCAG 实时荧光定量PCR qRT-PCR
ZmDREB2A-F ATCACTCGGACATCGCATCC 实时荧光定量PCR qRT-PCR
ZmDREB2A-R AGATACCAGGGCTGTCCCAT 实时荧光定量PCR qRT-PCR

Table 2

Physicochemical properties of ZmNTLs genes"

基因名称
Gene name		 基因ID
Gene ID		 染色体位置
Chromosomal
location		 蛋白质长度
Protein length (aa)		 分子量
Molecular weight
(kD)		 理论等电点
Theoretical isoelectric point
ZmNTL1 GRMZM2G064541 3 517 57.50 5.49
ZmNTL2 GRMZM2G125777 4 665 71.82 4.53
ZmNTL3 GRMZM2G113950 4 657 71.98 4.62
ZmNTL4 GRMZM2G004531 7 709 77.98 4.67
ZmNTL5 GRMZM2G167492 8 518 57.33 5.52
ZmNTL6 GRMZM2G163914 9 612 66.81 5.58
ZmNTL7 GRMZM2G003715 10 664 73.61 4.81
ZmNTL8 GRMZM2G158204 8 313 34.83 9.62
ZmNTL9 AC196475.3_FG005 4 633 70.66 4.90
基因名称
Gene name		 不稳定指数
Instability index		 脂肪酸指数
Fatty acid index		 平均亲疏水性
Grand average of hydropathicity		 低温叶log2FC
log2FC of leaves under low temperature		 低温根log2FC
log2FC of roots under low temperature
ZmNTL1 49.37 70.60 -0.641 5.19 4.83
ZmNTL2 36.98 74.56 -0.365 -1.00 0.79
ZmNTL3 43.32 67.32 -0.530 2.19 1.47
ZmNTL4 46.98 68.27 -0.508 2.25 2.06
ZmNTL5 49.92 68.40 -0.607 3.32 2.56
ZmNTL6 49.88 79.07 -0.408 -1.21 0.62
ZmNTL7 47.62 67.12 -0.602 4.05 3.50
ZmNTL8 27.62 99.36 0.257 - -
ZmNTL9 56.17 65.94 -0.772 2.93 3.35

Fig. 1

Molecular characterization and expression patterns of ZmNTLs gene under low temperature stress A: gene structures of ZmNTLs. B: conservative motifs of ZmNTLs. C: prediction of ZmNTLs protein transmembrane domain. D: expression patterns of ZmNTLs under low temperature stress. E: phylogenetic relationship of NTLs. Green circles represent 7 NTLs from Arabidopsis thaliana, blue circles represent 5 NTLs from rice, yellow circles represent 9 NTLs from maize, red circle represents 1 NTL from wheat."

Fig. 2

Generation of zmntl1zmntl5 mutant materials A: protein sequence alignment of ZmNTL1 and ZmNTL5. B: schematic diagram of the pCPB-Cas9 recombinant vector. C: common target design of ZmNTL1 and ZmNTL5. D, E: alignment of mutant allele sequences in gene knockout materials."

Fig. 3

Effect of ZmNTL1 and ZmNTL5 knockouts on maize tolerance to low temperature A: phenotype of zmntl1zmntl5 mutant under low temperature stress. B-E: changes of aboveground fresh weight/dry weight and underground fresh weight/dry weight of zmntl1zmntl5 mutant under low temperature stress. F, G: changes of ion leakage rate and chlorophyll content of zmntl1zmntl5 mutant under low temperature stress. Scale bar: 10 cm. **, P < 0.01; ***, P < 0.001."

Fig. 4

Effects of ZmNTL1 and ZmNTL5 knockouts on the antioxidant defense system of maize under low temperature stress A-D: changes of GST, CAT, POD, and SOD activity of zmntl1zmntl5 mutant under low temperature stress. E, F: DAB and NBT staining of zmntl1zmntl5 mutants. G, H: changes of O2- and H2O2 contents in zmntl1zmntl5 mutant under low temperature stress. *, P < 0.05; **, P < 0.01."

Fig. 5

Effects of ZmNTL1 and ZmNTL5 knockouts on stress-related gene expression under low temperature stress A-D: relative expression levels of ZmGST24, ZmNCED3, ZmDREB1.6, and ZmDREB2A in the zmntl1zmntl5 mutant under low temperature stress. **, P < 0.01; ***, P < 0.001."

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