Scientia Agricultura Sinica ›› 2020, Vol. 53 ›› Issue (5): 874-889.doi: 10.3864/j.issn.0578-1752.2020.05.002

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

Transcriptome Analysis of Maize pTAC2 Effects on Chlorophyll Synthesis in Seedling Leaves

ZHANG Wen,MENG ShuJun,WANG QiYue,WAN Jiong,MA ShuanHong,LIN Yuan,DING Dong(),TANG JiHua()   

  1. College of Agronomy, Henan Agricultural University/National Key Laboratory of Wheat and Maize Crop Science, Zhengzhou 450002
  • Received:2019-07-22 Accepted:2019-09-30 Online:2020-03-01 Published:2020-03-14
  • Contact: Dong DING,JiHua TANG E-mail:dingdong0216@hotmail.com;tangjihua1@163.com

Abstract:

【Objective】Chlorophyll is the most important photosynthetic pigment involved in plant photosynthesis. The development of chloroplasts and the synthesis of chlorophyll depend on the bi-directional signaling between the plastid and the nuclear genome. Plastid transcriptionally active chromosome proteins (pTACs) are essential for maintaining the transcriptional activity of PEP (plastid-encoded RNA polymerase) genes, whereas the function of pTACs in maize is still poorly understood. 【Method】The CRISPR/Cas9-ZmpTAC2 maize transgenic editing homozygous mutants were supplied. Transmission electron microscope were used to observe the ultrastructure of the chloroplast, with spectrophotometer to measure the chlorophyll content in maize leaves, respectively. Transcriptome sequencing of the negative material (CK) and CRISPR/Cas9-ZmpTAC2 transgenic homozygous (zmptac2) seedling leaves was performed. Bioinformatics toolbox was performed to identify the differently expressed genes between CK and zmptac2 leaves. Relative quantification of expression of selected differently expressed genes were verified using qRT-PCR. The interacting proteins of ZmpTAC2 were screened by yeast two-hybrid system. 【Result】 A total of 15 T0 transgenic seedlings were obtained, including 7 with green leaves and 8 with white ones. Among the seven green-leaf seedlings, 3 were transgenic negative together with 4 transgenic positive including 2 seedlings were edited. On the other hand, all 8 white-leaf seedlings were transgenic positive with homozygous editing. Compared with CK, zmptac2 chloroplast was abnormal with significantly reduced chlorophyll content. The results of RNA-seq showed that 1 367 genes were differentially expressed between CK and zmptac2, of which 618 genes were up-regulated (zmptac2/CK) and 749 genes down-regulated (zmptac2/CK). GO enrichment analysis revealed that the down-regulated genes were significantly enriched in chloroplasts and plastids. KEGG analysis indicated that down-regulated genes were abundant in the pathways of phenylalanine, tyrosine, and iso-quinoline alkaloid metabolism. Relative expression values of 15 selected differently expressed genes showed similar expression patterns and are consistent with sequencing data, which indicated that the sequencing results were reliable. The expression of PEP (plastid-encoded RNA polymerase) dependent genes in zmptac2 was significantly decreased, while the expression of NEP (nuclear gene-encoded RNA polymerase) genes increased. ZmpTAC3 was identified to be interacted with ZmpTAC2 by cDNA screening and verified by interaction assay. 【Conclusion】 This study first reported that mutations in the ZmpTAC2 gene cause early chloroplast biosynthesis to be hindered, indicating that this gene is involved in chloroplast development and chlorophyll synthesis, which is achieved by ZmpTAC2 regulated PEP-related gene expression.

Key words: maize (Zea mays L.), chlorophyll content, ZmpTAC2, RNA-seq, gene expression regulation

Fig. 1

Phenotypic identification and target site detection of CK and zmptac2 A: Leaf phenotype of CK and zmptac2 seedlings; B: CK and zmptac2 target site detection sequencing results"

Table 1

Mutations detected in the putative CRISPR/Cas9 off-target sites"

编号
Serial number
潜在脱靶位置
Putative off-target locus
潜在脱靶序列
Sequence of the putative off-target
site (5′-3′)
错配碱基数
No. of mismatching bases
测试株数 T0
No. of plants tested
突变株数 T0
No. of plants with mutations
Off-target1 Chr.7:109756398-109756420 AgCTGGaGTAtAGCCTtATACGG 4 8 0
Off-target2 Chr.1 :145160658-145160680 AcCTGGGGTACAGCCaGATcAGG 3 8 0
Off-target3 Chr.6:44283532-44283554 cGaCCACGCAGCTATGTcTGAGG 3 8 0
Off-target4 Chr.4:230687431-230687453 cGaCCACGCAGCTATGTcTGAGG 3 8 0
Off-target5 Chr.7:8936191-8936213 TGGCCACGCgGCTAcGTgTGGGG 3 8 0
Off-target6 Chr.7:8936289-8936311 TGGCCACGCgGCTAcGTgTGGGG 3 8 0

Fig. 2

zmptac2 pure mutant chlorophyll content determination A: Chloroplast ultrastructure of zmptac2 mutant. G: Thylakoid granule; PG: Plastid globule; S: Matrix. B: Chlorophyll content determination. Chla: Chlorophyll a; Chlb: Chlorophyll b; Chl: Total chlorophyll. * indicates difference at the 0.05 level; ** indicates difference at the 0.01 level. The same as below"

Table 2

Output statistics of sequencing analysis"

样品
Sample
总碱基数
Total bases (Billion)
GC含量
GC percentage (%)
Q30 比例
Q30 percentage (%)
比对序列比例
Total mapping reads percentage (%)
CK_1 15 47.52 92.90 98.71
CK_2 16 47.50 91.94 98.75
zmptac2_1 12 47.52 90.29 98.87
zmptac2_2 16 47.92 92.17 98.56

Fig. 3

Analysis of differentially expressed genes in GO enrichment"

Fig. 4

KEGG enrichment analysis of differentially expressed genes A: Up-regulation of the expression gene KEGG (Pathway) enrichment analysis; B: Down-regulation of expression gene KEGG (Pathway) enrichment analysis"

Table 3

Differentially expressed genes verified by qRT-PCR"

基因编号
Gene ID
zmptac2 CK 差异倍数
log2Fold change
P
P-value
基因名称
Synonyms
描述
Description
Zm00001d039206 189.7162285 4.75059079 5.370830095 7.82E-06 Bzip118 bZIP转录因子超家族蛋白
Putative bZIP transcription factor superfamily protein
Zm00001d043825 80.63331881 0 8.789501589 0.00185833 CtpA1 羧基末端加工肽酶1
Carboxyl-terminal-processing peptidase 1 chloroplastic
Zm00001d027476 176.7085969 0 9.921454443 4.88E-06 DNA polymerases 依赖DNA的DNA聚合酶
DNA-directed DNA polymerases
Zm00001d031503 1000.059518 22.40077408 5.473911936 0.00680168 CPN60 伴侣蛋白亚基
Chaperonin 60 subunit alpha 2 chloroplastic
Zm00001d008221 0 351.1761292 -21.80949 1.54E-09 Cyc5 细胞周期蛋白5
Cyclin5
Zm00001d022599 363.2261699 3395.326772 -3.03756614 5.64E-14 ZmpTAC2 质体转录活性染色体2
Plastid transcriptionally active chromosome 2 homolog
Zm00001d033365 0 362.4571584 -23.97922 0.0000335 Cyclin A3 1 细胞周期蛋白A3-1 Putative cyclin-A3-1
Zm00001d027540 0 1170.714751 -25.15007 0.0000113 Gst12 谷胱甘肽S-转移酶12
Glutathione S-transferase12
Zm00001d048353 0 168.1203061 -22.56015 1.08E-08 Gst13 谷胱甘肽转移酶13 Glutathione transferase13
Zm00001d027760 0 1660.523115 -24.97806 1.32E-05 H2A 组蛋白H2A Histone H2A
Zm00001d051591 10.74539904 2639.275824 -7.938035 4.88E-05 his2b5 组蛋白2B5 Histone 2B5
Zm00001d042730 87.36474604 4052.072328 -5.535586 5.51E-05 H3 组蛋白H3 Histone H3
Zm00001d012276 103.9578986 6414.512969 -5.947576 0.000341 H3.2 组蛋白H3.2 Histone H3.2
Zm00001d039497 40.62122946 4971.062871 -6.93312404 8.97E-28 ClpC1 伴侣蛋白ClpC1(线粒体)
Chaperone protein ClpC1 chloroplastic
Zm00001d042062 0 2272.297402 -9.395263783 0.00021753 ORG3 转录因子ORG3 Transcription factor ORG3

Fig. 5

qRT-PCR expression analysis of zmptac2 and CK differential genes"

Fig. 6

zmptac2 mutations in the body rely on PEP, NEP related gene relative expression A: The relative expression of plasmid genes that rely on PEP; B: The relative expression of plasmid genes that rely on NEP"

Fig. 7

Transcriptional activation analysis and interaction protein screening A: Yeast one-hybrid assay to verify the transcriptional activation activity of ZmpTAC2 and ZmpTAC3; B: Toxicity verification of bait protein ZmpTAC2; C: Self-activation verification of bait vector pGBKT7-ZmpTAC2; D: Point-to-point verification"

Table 4

Yeast two-hybrid system sieve library obtains ZmpTAC2 inter-made proteins"

编号
No.
基因编号
Gene ID_v4
亚细胞定位
Subcellular localization
基因描述
Gene description
1 Zm00001d022242 细胞膜Cell membrane 胞间连丝胼胝质结合蛋白5 PLASMODESMATA CALLOSE-BINDING PROTEIN 5
2 Zm00001d010039 细胞壁Cell wall 含纤维素酶的蛋白质Cellulase containing protein
3 Zm00001d023305 叶绿体Chloroplast Protein LURP-one-related 2
4 Zm00001d049153 叶绿体Chloroplast 催化/水解酶Catalytic/ hydrolase
5 Zm00001d041550 叶绿体Chloroplast 热休克蛋白3 Heat shock 70 kDa protein 3
6 Zm00001d035270 叶绿体Chloroplast SAM结构域蛋白Sterile alpha motif (SAM) domain-containing protein
7 Zm00001d028221 叶绿体Chloroplast ATP合酶4 ATP synthase4
8 Zm00001d046073 叶绿体Chloroplast Protein trichome birefringence-like 26
9 Zm00001d032373 叶绿体Chloroplast 叶绿体RNA剪接体1 Chloroplast RNA splicing1
10 Zm00001d007417 叶绿体Chloroplast ATP依赖性DNA解旋酶ATP-dependent DNA helicase chloroplastic
11 Zm00001d024248 叶绿体Chloroplast PPR蛋白Pentatricopeptide repeat*-59040
12 Zm00001d016660 细胞质Cytoplasm 肽基脯氨酰异构酶1 Peptidyl-prolyl isomerase1
13 Zm00001d033623 细胞质Cytoplasm 脂氧合酶 Lipoxygenase
14 Zm00001d018441 细胞质,细胞核
Cytoplasm. Nucleus
核苷三磷酸水解酶超家族蛋白
P-loop containing nucleoside triphosphate hydrolases superfamily protein
15 Zm00001d040681 细胞质,细胞核
Cytoplasm. Nucleus
alpha/beta水解超家族蛋白
Alpha/beta-Hydrolases superfamily protein
16 Zm00001d038857 线粒体Mitochondrion 伴侣蛋白CPN60 Chaperonin CPN60-like 2 mitochondrial
17 Zm00001d035201 线粒体Mitochondrion 60S核糖体蛋白P060S acidic ribosomal protein P0
18 Zm00001d053434 细胞核Nucleus RING锌指结构域超家族蛋白 Putative RING zinc finger domain superfamily protein
19 Zm00001d032422 细胞核Nucleus 休眠相关蛋白1 Dormancy-associated protein 1
20 Zm00001d044246 细胞核Nucleus 组蛋白H2A Histone H2A
21 Zm00001d044429 细胞核Nucleus 硫氧还蛋白超家族蛋白 Thioredoxin superfamily protein
22 Zm00001d021954 细胞核Nucleus MO25蛋白 Putative MO25-like protein
23 Zm00001d032646 细胞核Nucleus RHC1A
24 Zm00001d016876 细胞核Nucleus Trihelix转录因子ASIL2 Trihelix transcription factor ASIL2
25 Zm00001d043914 细胞核Nucleus Homeobox-DDT结构域蛋白RLT1 Homeobox-DDT domain protein RLT1
26 Zm00001d014858 细胞核Nucleus DNA结合蛋白MNB1B DNA-binding protein MNB1B
27 Zm00001d036494 细胞核Nucleus GATA转录因子25 GATA transcription factor 25
28 Zm00001d013159 细胞核Nucleus α-微管蛋白3 Alpha-tubulin 3
29 Zm00001d001847 细胞核Nucleus NUMOD3基序家族蛋白 NUMOD3 motif family protein expressed; protein
30 Zm00001d032790 细胞核Nucleus 质体转录活性3 Plastid transcriptionally active 3
31 Zm00001d052298 细胞核Nucleus 锌指(C3HC4型RING指)家族蛋白 Zinc finger (C3HC4-type RING finger) family protein
32 Zm00001d027652 液泡Vacuole 水通道蛋白TIP1-1 Aquaporin TIP1-1
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