Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (3): 508-518.doi: 10.3864/j.issn.0578-1752.2023.03.009

• HORTICULTURE • Previous Articles     Next Articles

Cloning and Analysis of Key Genes for Vitamin C Synthesis in Cucumber Fruit

WANG ZhuangZhuang1,2(), DONG ShaoYun1(), ZHOU Qi1, MIAO Han1, LIU XiaoPing1, XU KuiPeng2, GU XingFang1(), ZHANG ShengPing1()   

  1. 1Institute of Vegetable and Flowers, Chinese Academy of Agricultural Sciences/Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture and Rural Affairs/State Key Laboratory of Vegetable Biobreeding, Beijing 100081
    2College of Horticulture, Qingdao Agricultural University, Qingdao 266000, Shandong
  • Received:2022-04-13 Accepted:2022-06-13 Online:2023-02-01 Published:2023-02-14
  • Contact: GU XingFang, ZHANG ShengPing E-mail:wangzhuangz2021@163.com;dongshaoyun@caas.cn;guxingfang@caas.cn;zhangshengping@caas.cn

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Abstract:

【Objective】The aim of this study was to identify the location, quantity and expression characteristics of genes involved in regulating the synthesis of vitamin C (Vc) by L-galactose pathway in cucumber fruits, and to clone the key genes, so as to lay a foundation for the regulation of Vc synthesis in cucumber.【Method】According to the reported Vc-related genes within the L-galactose pathway in Arabidopsis, the encoded amino acid sequence was used for BLAST in Cucumber 9930_V2 reference genome database. TBtools software was used to map the gene position on cucumber chromosomes. The expression of these genes in two cucumber accessions with significant differences in fruit Vc content was analyzed by qRT-PCR. The homologous genes encoding rate limiting enzymes GDP-L-galactose phosphorylase (GGP) and GDP mannose-3'5'- epimerase (GME) were cloned by PCR amplification, and the sequence differences of these genes in cucumber with high Vc and low Vc were analyzed by sequencing. Phylogenetic tree was constructed to analyze the relatedness cucumber GME, GGP and homologs in other species.【Result】Twenty one homologous genes involved in the synthesis of Vc related enzymes, including PMI, PMM, GMPase, GME, GGP, GPP, GalLDH, and GalLDH in L-galactose pathway, were compared in cucumber and were obtained by BLAST, which were distributed on seven chromosomes, with the most numbers on chromosome 5 and chromosome 1. By analyzing the expression of these genes in R48 (with low Vc) and CG45 (with high Vc), it was found that the genes regulating PMI, PMM, GMPase, GME and GalLDH were significantly different between the two materials. The sequence analysis of Vc synthesis rate-limiting enzyme GGP and GME related genes showed that the full length of CsGME2 gene was 3 537 bp in R48 and 3 541 bp in CG45. There were multiple SNP sites and Indel difference between the two materials, among which one mutation site was located in the CDS region, and resulted in the amino acids changes. Through the analysis of the protein properties of rate limiting enzymes GME and GGP regulating vitamin C synthesis, it was found that the protein properties of GME and GGP in different species were not significantly different, which were hydrophilic proteins and their functions were relatively conservative. Evolutionary tree analysis found that the clusters with close genetic relationship among different species were highly conservative during evolution.【Conclusion】Twenty one L-galactose pathway related genes of cucumber Vc synthesis were identified, which were distributed on seven chromosomes. It was speculated that the key enzymes including PMI, PMM, GMPase, GME, GalLDH and GGP might affect the Vc content in cucumber fruits. The functions of key enzymes GME and GGP regulating the rate limiting step of Vc synthesis were relatively conservative. The SNP site on CsGME2 gene in the two materials of high Vc and low Vc resulted in changes in amino acid sequence.

Key words: cucumber, vitamin C, gene clone, expression analysis

Table 1

Real-time qPCR primers for homologous genes of L-galactose pathway"

基因 Gene 正向引物 Forward primer (5′-3′) 反向引物 Reverse primer (5′-3′)
Csa1G181570 TTATCTCAAGGACCATTATCCC TCCATCAAGAGGATCAACG
Csa1G183590 ATTGGACCATTCGACACC TAACAGCATCCATCACCG
Csa1G006280 CACCAGTTTGGAGAGTTGATT TCGAAACACCTTGAATTGTG
Csa1G600810 CCTGAGGATGTTGGAACC CTACAGCACCATTCCGTCT
Csa2G011460 TCTAGTGCTTGCATCTATCCTG AGCTTCTCCAGACCGTAGG
Csa2G013230 TGAAAGGCAGGGAATGTATC CCATGCCCAATAATCGAA
Csa2G249820 CAAGCAGCAGAGGAGTCTATG CATCAATGGGATCTAAAACCC
Csa3G300600 AAGTCTGCTCTAAGGTTGGC TTCCTTGGCTGTTAATTGC
Csa3G829100 GCTGATCCGGTCACTAATG CCTTCCCGATGAATTGAG
Csa3G133160 ACCTGATAGCCGATTTGC GATTAGCAGCACACCACG
Csa4G236360 AAGTGAGGAAGCCATACAGC TCAAGGGCAAGTAGTTTATCG
Csa4G015100 CTCTATTATCAACATCGGATCG TGGGATGAACTGCATGAG
Csa5G011690 TCGAAATGGGATGCTTAAC CTCCCGAAGGATAGAAACC
Csa5G167200 TTGGCGAGATCCTTGAAC AACTTCTCTGCATCAGCACA
Csa5G182060 TTAGAAGTTGCTACGATGAAGG TTGCTAACAACACGACCG
Csa5G512920 CACTGGATCGAAGGATAACTTG GGCAAGCAAGATGGTATATTTG
Csa5G272920 TGTATGGGCTTGACTGGAG TCAGTGCCAACCAGGATT
Csa6G008750 GCGAGCCATTCTTTGTCC CACACCGTATTTGGAAGGC
Csa6G511690 ATGGAGCTGACTGATGAGC AACTGTTGGAACTTTGCCA
Csa7G067450 GGTGACAAGGAGCATTGAC GGAATCGTCTCGTTCACAC
Csa7G219200 AGGTCCTCTTCCGGTTTG CAATAGTGGCGCAACCAC
Actin TCCACGAGACTACCTACAACTC GCTCATACGGTCAGCGAT

Table 2

Primers of GME and GGP related genes"

引物名称 Primer name 正向引物 Forward 反向引物 Reverse
CsGME1-1 TGTCTGAGTCCAAGAGAACG GCATCTGACTCCTTCAAGCT
CsGME1-2 TGAGGAAGAAAGTACGCAAC TGAGTTACGACCACGGACAC
CsGME1-3 AGACTTCCGTGAGCCAGTGA ACGGTGGACCTCATAATATC
CsGME2-1 TTAGGCAGCCAATCGTCGGA CTGTCCACTAGATGAGAGCCA
CsGME2-2 TCCTTGTGTGACAATCATC CAGTCAATGGTTCGCTACTGC
CsGME2-3 ACATATGGACCGAGAATGA AGTAGTGGCATGAGTCGAGA
CsGGP-1 CCCTAGAAGATTCGAAGTA GCCAGATATCTTGTTCAGC
CsGGP-2 GCTTTCATTCCTAGTGGATA ATCCGTTGCCCACAATCAGC
CsGGP-3 GATGGAGTGATCATCTCTGA AGGACCATTAGTGATAGGTA

Table 3

Key enzymes and related genes of vitamin C synthesis in cucumber"

酶
Enzyme		 登录号（拟南芥）
Accession No. (Arabidopsis)		 登录号（黄瓜）
Accession No. (cucumber)		 基因名称
Gene name		 染色体位置
Chromosome		 物理位置
Location (bp)
PMI AT3G02570 Csa3G300600
Csa5G167200		 CsPMI1
CsPMI2		 Chr3
Chr5		 17101685-17104783 (+)
6525799-6529720 (-)
PMM AT2G45790 Csa5G011690 CsPMM Chr5 410127-419862 (+)
GMPase AT2G39770 Csa6G008750
Csa3G829100
Csa1G006280
Csa2G013230
Csa1G600810		 CsGMPase1
CsGMPase2
CsGMPase3
CsGMPase4
CsGMPase5		 Chr6
Chr3
Chr1
Chr2
Chr1		 901131-904917 (+)
901131-904917 (+)
1169141-1173256 (+)
2269704-2282961 (-)
23233328-23240457 (+)
GME AT5G28840 Csa2G011460
Csa5G182060
Csa5G512920		 CsGME1
CsGME2
CsGME3		 Chr2
Chr5
Chr5		 2039207-2042353 (+)
8093540-8097076 (+)
17891804-17895624 (-)
GGP AT4G26850
AT5G55120		 Csa7G219200
 CsGGP Chr7 7788896-7792047 (+)
GPP AT3G02870 Csa1G181570
Csa6G511690
Csa1G183590
Csa2G249820		 CsGPP1
CsGPP2
CsGPP3
CsGPP4		 Chr1
Chr6
Chr1
Chr2		 11166020-11169584 (+)
26388577-26391259 (-)
11213505-11222521 (+)
12197999-12203006 (+)
GalDH AT4G33670 Csa7G067450
Csa5G272920
Csa4G015100
Csa3G133160		 CsGalDH1
CsGalDH2
CsGalDH3
CsGalDH4		 Chr7
Chr5
Chr4
Chr3		 4137998-4141177 (+)
11505791-11512104 (+)
1982420-1984762 (+)
8687749-8692048 (-)
GalLDH AT3G47930 Csa4G236360 CsGalLDH Chr4 10080624-10094987 (+)

Fig. 1

Position of vitamin C synthesis related genes on chromosome in cucumber"

Fig. 2

Relative expression of vitamin C synthesis related genes in cucumber fruit of R48 and CG45 1: CsPMI1; 2: CsPMI2; 3: CsPMM; 4: CsGMPase1; 5: CsGMPase2; 6: CsGMPase3; 7: CsGMPase4; 8: CsGMPase5; 9: CsGME1; 10: CsGME2; 11: CsGME3; 12: CsGGP; 13: CsGPP1; 14: CsGPP2; 15: CsGPP3; 16: CsGPP4; 17: CsGalDH1; 18: CsGalDH2; 19: CsGalDH3; 20: CsGalDH4; 21: CsGalLDH"

Fig. 3

L-galactose pathway The circle in the left column is the relative expression of R48, and the circle in the right column is the relative expression of CG45"

Fig. 4

Sequence analysis of CsGME2 gene between the two materials"

Fig. 5

Analysis of conserved domain of CsGME2 gene"

Table 4

The physicochemical properties of different species of GME"

物种
Species		 氨基酸长度
Length (aa)		 蛋白质量
Mw (kD)		 等电点
pI		 不稳定系数
II		 总平均疏水性
GRAVY		 序列号
Accession
黄瓜 Cucumis sativus 376 42.52 5.94 41.85 -0.411 XP_004139232
甜瓜 Cucumis melo var. makuwa 409 46.50 6.05 49.3 -0.429 TYK18415.1
冬瓜 Benincasa hispida 376 42.62 5.94 42.09 -0.432 XP_038890351
南瓜 Cucurbita moschata 376 42.54 6.05 41.96 -0.415 XP_022946492
苦瓜 Momordica charantia 376 42.51 5.81 39.45 -0.414 XP_022143153
银葫芦亚种 Cucurbita argyrosperma subsp. sororia 397 44.78 5.74 43.98 -0.409 KAG6586308
桑葚 Morus notabilis 379 42.87 6.21 40.5 -0.437 XP_024025147
向日葵 Helianthus annuus 376 42.60 5.84 43.02 -0.408 XP_022002729
开心果 Pistacia vera 376 42.48 5.93 39.46 -0.410 XP_031268788
石榴 Punica granatum 386 43.47 6.16 38.39 -0.383 OWM82038

Fig. 6

Evolutionary tree of GME in cucumber and other species"

Table 5

The physicochemical properties of different species of GGP"

物种
Species		 氨基酸长度
Length (aa)		 蛋白质量
Mw (kD)		 等电点
pI		 不稳定系数
II		 总平均疏水性
GRAVY		 序列号
Accession
黄瓜 Cucumis sativus 445 49.99 5.18 44.23 -0.224 XP_004139797.1
甜瓜 Cucumis melo var. makuwa 537 60.04 5.13 45.37 -0.174 TYK23075.1
冬瓜 Benincasa hispida 448 50.23 5.24 43.20 -0.163 XP_038897875.1
苦瓜 Momordica charantia 446 49.77 4.86 48.18 -0.206 XP_022139724.1
南瓜 Cucurbita moschata 445 49.58 5.14 49.30 -0.167 XP_022940636.1
银葫芦亚种 Cucurbita argyrosperma subsp. sororia 445 49.61 5.09 48.32 -0.165 KAG7037363.1
西葫芦 Cucurbita pepo subsp. pepo 445 49.57 5.10 48.71 -0.162 XP_023524925.1
开心果 Pistacia vera 449 50.05 4.77 48.15 -0.222 XP_031282295.1
核桃 Juglans regia 449 49.83 5.16 46.50 -0.180 XP_018812019.2
桑葚 Morus notabilis 443 49.28 5.07 40.97 -0.126 XP_010096115.1
棉花 Gossypium hirsutum 450 50.55 5.10 54.38 -0.230 XP_040942951.1

Fig. 7

Evolutionary tree analysis of GGP in cucumber and other species"

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