Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (12): 2265-2281.doi: 10.3864/j.issn.0578-1752.2024.12.001

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

Analysis of Maize Phenylalanine Ammonia-Lyase (PAL) Family Genes and Functional Study of ZmPAL5

CAO LiRu1(), YE FeiYu1(), KU LiXia2, MA ChenChen1, PANG YunYun1, LIANG XiaoHan1, ZHANG Xin1(), LU XiaoMin1()   

  1. 1 Grain Crop Research Institute, Henan Academy of Agricultural Sciences/The Shennong Laboratory, Zhengzhou 450002
    2 College of Agronomy, Henan Agricultural University, Zhengzhou 450046
  • Received:2023-11-15 Accepted:2024-01-12 Online:2024-06-16 Published:2024-06-25
  • Contact: ZHANG Xin, LU XiaoMin

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Abstract:

【Objective】 Mining the key drought-resistant genes of maize, revealing its drought-resistant molecular mechanism, and providing genetic resources and theoretical guidance for the cultivation of new drought-resistant maize varieties.【Method】Transcriptome data combined with weighted gene co-expression network (WGCNA) and screening methods for physiological and biochemical indicators of drought resistance were used to identify ZmPAL genes associated with drought resistance and rewatering. Genome-wide analysis of the genes encoding PAL was performed using bioinformatics methods. Quantitative real-time fluorescence PCR (qRT-PCR) was used to detect the expression of ZmPAL genes under drought treatment conditions, as well as the expression characteristics of ZmPAL5 among different inbred lines and the expression patterns in different tissues. Finally, genetic transformation was used to analyze the drought resistance function of ZmPAL5 in maize, and the deletion-type Arabidopsis mutant was analyzed for drought resistance with the help of CRISPR/Cas9 technology for the PAL5 homologous gene.【Result】Nineteen maize ZmPAL genes were identified, six of which were clustered on chromosome 5 and encoded proteins that were mostly hydrophilic acidic proteins and relatively evolutionarily conserved in the PAL family of genes. The promoter region of ZmPAL genes contained a large number of cis-acting elements associated with hormonal and abiotic stress responses. Six core genes were identified, four of which were significantly up-regulated for expression after drought treatment. In particular, ZmPAL5 showed an 8.57-fold increase in expression after drought stress. The expression level of ZmPAL5 was found to be significantly higher in the drought-resistant inbred line Zheng 8713 than in the drought-sensitive inbred line B73 under both drought stress and rewatering treatments. Meanwhile, ZmPAL5, a constitutively expressed gene, showed a high level of expression in young stems. Overexpressed ZmPAL5 maize grew well under drought stress, and its relative water content, lignin, chlorophyll, soluble protein, proline content, and activities of superoxide dismutase, peroxidase, catalase, and ascorbate peroxidase were 1.52, 1.49, 1.47, 1.43, 1.44, 1.41, 1.53, 1.41, and 1.35 times, but the malondialdehyde content was 0.65 times that of the wild type. The PAL5-deficient Arabidopsis mutant was sensitive to drought. Under drought stress, its physiological and biochemical indexes showed the opposite trend to those of overexpression of ZmPAL5 maize. 【Conclusion】 Six core genes (ZmPAL3, ZmPAL5, ZmPAL6, ZmPAL8, ZmPAL11, and ZmPAL13) were screened in response to drought stress, in which the expression of ZmPAL5 was positively correlated with drought resistance. ZmPAL5 positively regulated the drought resistance and resilience of the plant by influencing the content of osmotically regulated substances and antioxidant enzyme activities.

Key words: maize, phenylalanine ammonia-lyase, ZmPAL5, drought resistance, physiology and biochemistry

Table 1

qRT-PCR primers for gene"

引物名称Primer name 引物序列Primer sequence (5′-3′) 用途Purpose
ZmPAL3-F TCGGATTCACTGGCTTGCTG 检测基因在干旱胁迫下的表达量
Detection of gene expression under drought stress
ZmPAL3-R GAGGATTGGACCGAAGTGGTA
ZmPAL5-F ATGAACGGCACCGACAGCTA
ZmPAL5-R CAGGGTGTTGATGCGGACGA
ZmPAL6-F AGTGCTAGTGCTGCTACCCT
ZmPAL6-R TGTGATGATGCTGATGCGGT
ZmPAL8-F TCACCGTGTTCTTGACGGAG
ZmPAL8-R TCCTCAAGCTCATGTCGTCC
ZmPAL11-F TGGCCCTCGTGCAAAGTATC
ZmPAL11-R TTGGTTTCCCATCTGGCGAT
ZmPAL13-F ACGCGCCAGCATTGAGGAA
ZmPAL13-R TGATGAACGGCACCGACAG
18S-F CCTGCGGCTTAATTGACTC 内参基因Reference gene
18S-R GTTAGCAGGCTGAGGTCTGG
ZmPAL5-WMV013-BamHI-F AGGTCGACTCTAGAGGATCCATGGAGTGCGAGAACGGACA 构建玉米ZmPAL5过表达载体
Construction of maize ZmPAL5 overexpression vector
ZmPAL5-WMV013-SmaI-R TCTTTGTAGTCCATCCCGGGGCCTCCACCCCCGCCACCGCAGATGGGCAGGGGCTCAC
AT3G10340-PKI1.1R-F ATTGGACAGTTATGGAGTTACCAC 构建拟南芥CRISPR/Cas9敲除载体及菌落验证
Construction of an Arabidopsis CRISPR/Cas9 knockout vector and colony validation
AT3G10340-PKI1.1R-R AAACGTGGTAACTCCATAACTGTC
U6.26-F TGTCCCAGGATTAGAATGATTAGGC

Fig. 1

Correlation analysis and aggregate analysis of different modules and physiological and biochemical indexes in the process of drought and rewatering A: Hierarchical clustering tree of corepresentation modules, different colors represent different modules. ABA: Abscisic acid; Sp: Soluble protein; Pro: Proline; POD: Peroxidase; SOD: Superoxide dismutase; CAT: Catalase; MDA: Malondialdehyde; GSH: Glutathione; AsA: Ascorbic acid. B: Correlation analysis of ZmPAL gene in different modules"

Table 2

Analysis of physicochemical properties and prediction of subcellular localization of ZmPAL protein in maize"

基因名称
Gene name		 基因ID
Gene ID		 物理位置
Location
(bp)		 长度
Length (aa)		 分子量
Molecular weight (kDa)		 等电点
pI		 亲水性系数
Grand average of hydropathicity		 亚细胞定位预测
Prediction of subcellular localization
ZmPAL1 Zm00001d029015 Chr.1:54941440-54943661 398 43.19 6.52 -0.033 细胞质，叶绿体
Cytoplasmic, Chloroplast
ZmPAL2 Zm00001d029648 Chr.1:81308232-81312047 848 95.13 5.82 -0.293 叶绿体Chloroplast
ZmPAL3 Zm00001d031071 Chr.1:175969709-175971563 386 43.31 9.05 -0.214 叶绿体，线粒体
Chloroplast, Mitochondrial
ZmPAL4 Zm00001d033286 Chr.1:257622515-257624760 698 75.66 5.85 -0.04 质膜Plasma membrane
ZmPAL5 Zm00001d003015 Chr.2:29467931-29470598 715 76.78 5.63 -0.079 叶绿体，质膜，内质网
Chloroplast, Plasma membrane, Endoplasmic reticulum
ZmPAL6 Zm00001d003016 Chr.2:29538173-29541434 884 96.71 5.99 -0.195 质膜，叶绿体，线粒体
Plasma membrane, Chloroplast, Mitochondrial
ZmPAL7 Zm00001d048874 Chr.4:6825874-6829872 778 87.89 5.30 -0.296 细胞质Cytoplasmic
ZmPAL8 Zm00001d051161 Chr.4:146706971-146710589 557 60.43 6.02 -0.055 叶绿体Chloroplast
ZmPAL9 Zm00001d051163 Chr.4:146793740-146798809 718 77.43 6.12 -0.121 叶绿体，内质网
Chloroplast, Endoplasmic reticulum
ZmPAL10 Zm00001d051166 Chr.4:146846109-146848259 775 84.54 5.37 -0.163 叶绿体，质膜，细胞核
Chloroplast, Plasma membrane, Nuclear
ZmPAL11 Zm00001d013534 Chr.5:13763873-13782041 187 20.48 7.64 -0.441 叶绿体，线粒体
Chloroplast, Mitochondrial
ZmPAL12 Zm00001d017274 Chr.5:191418711-191422345 703 75.46 5.96 -0.069 叶绿体，质膜，内质网
Chloroplast, Plasma membrane, Endoplasmic reticulum
ZmPAL13 Zm00001d017275 Chr.5:191467430-191471500 719 77.4 6.20 -0.100 叶绿体，内质网
Chloroplast, Endoplasmic reticulum
ZmPAL14 Zm00001d017276 Chr.5:191474696-191476810 704 75.84 5.89 -0.066 叶绿体，内质网，细胞核
Chloroplast, Endoplasmic reticulum, Nuclear
ZmPAL15 Zm00001d017279 Chr.5:191539072-191541219 715 76.93 5.89 -0.083 叶绿体，质膜，细胞核
Chloroplast, Plasma membrane, Nuclear
ZmPAL16 Zm00001d017617 Chr.5:201803815-201807716 87 9.29 5.25 -0.266 叶绿体Chloroplast
ZmPAL17 Zm00001d021368 Chr.7:150079651-150084317 321 36.34 9.51 -0.302 叶绿体Chloroplast
ZmPAL18 Zm00001d023655 Chr.10:13756073-13759615 366 40.32 9.02 0.296 叶绿体，质膜，液泡
Chloroplast, Plasma membrane, Vacuolar
ZmPAL19 Zm00001d024512 Chr.10:75069687-75075183 727 81.54 5.32 -0.227 细胞核Nuclear

Fig. 2

Bioinformatics analysis of PALs of different species A: Phylogenetic classification; B: Gene structure, domains and conserved motifs; C: cis-acting element. Zm: Zea mays L.; At: Arabidopsis thaliana; Sb: Sorghum bicolor L.; Os: Oryza sativa L."

Fig. 3

ZmPAL gene coexpression network (A), heat map (B) and expression of ZmPAL gene under drought (C) T0Y, T5dY, TR3dY and T0G, T5dG, TR3dG: Y represents leaf, G represents root, and T0, T5d, TR3d represents pre-drought, 5 d after drought and 3 d after rewatering, respectively"

Fig. 4

Analysis of phenotypes and expression of ZmPAL5 in different inbred lines under drought treatment A: Phenotype after drought treatment; B: Expression analysis of ZmPAL5 under different time drought treatments; C: Expression analysis of ZmPAL5 in different tissues. *P<0.05, **P<0.01. The same as below"

Fig. 5

Seedling phenotypes and index identification of ZmPAL5 transgenic maize under drought stress A: Seedling phenotypes of wild-type and ZmPAL5 transgenic maize under drought stress; B: Expression levels of the obtained positive transgenic strains; C: Survival rate of both plants under drought stress; D: The lignin content of both plants under drought stress; E: The relative water content of both plants under drought stress; F: Chlorophyll content of both plants under drought stress; G: Malondialdehyde content of both plants under drought stress; H-I: Osmoregulators (Pro and Sp) content of both plants under drought stress; J-M: The antioxidant enzymes (SOD, POD, CAT, and APX) activities of both plants under drought stress. T0, T7d, TR3d represents pre-drought, 7 d after drought and 3 d after rewatering, respectively. The same as below"

Fig. 6

Mutation sequence, Seedling phenotypes and index identification of PAL5 transgenic Arabidopsis thaliana under drought stress A: Results of CDS sequence comparison between maize ZmPAL5 gene and Arabidopsis homologous genes and target sequences; B: Gene structure, mutation sites and sequences of Arabidopsis genes; C: Seedling phenotypes of wild-type and transgenic Arabidopsis pal5 under drought stress; D: The lignin content of both plants under drought stress; E: The relative water content of both plants under drought stress; F: Chlorophyll content of both plants under drought stress; G: Malondialdehyde content of both plants under drought stress; H-I: Osmoregulators (Pro and Sp) content of both plants under drought stress; J-M: The antioxidant enzymes (SOD, POD, CAT, and APX) activities of both plants under drought stress"

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