Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (14): 2812-2824.doi: 10.3864/j.issn.0578-1752.2022.14.011

• HORTICULTURE • Previous Articles     Next Articles

Map-Based Cloning and Molecular Marker Development of Watermelon Fruit Shape Gene

DUAN YaRu1(),GAO MeiLing1,2(),GUO Yu1,LIANG XiaoXue1,LIU XiuJie3,XU HongGuo1,LIU JiXiu3,GAO Yue3,LUAN Feishi4   

  1. 1. College of Life Sciences, Agriculture and Forestry, Qiqihar University, Qiqihar 161006, Heilongjiang
    2. Heilongjiang Provincial Key Laboratory of Resistance Gene Engineering and Preservation of Biodiversity in Cold Areas, Qiqihar 161006, Heilongjiang
    3. Qiqihar Agricultural Technology Extension Center, Qiqihar 161006, Heilongjiang
    4. College of Horticulture and Landscape Architecture, Northeast Agricultural University, Harbin 150030
  • Received:2021-11-03 Accepted:2022-02-03 Online:2022-07-16 Published:2022-07-26
  • Contact: MeiLing GAO E-mail:1141941808@qq.com;gaomeiling0539@163.com

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Abstract:

【Objective】 Based on the result of fruit shape gene preliminary mapping by genotyping-by-sequencing (GBS) high-density genetic map, the fine mapping of the fruit shape gene was conducted by using map-based cloning method, and the functional molecular markers were developed in watermelon. The present study could facilitate comprehensive study on the function of fruit shape gene and molecular marker-assisted selection breeding. 【Method】GWAS (Genome-wide association study) analysis was performed on 114 watermelon inbred lines by using whole-genome re-sequencing data and their fruit shape index phenotypes. The candidate regions of fruit shape gene ClFSI were confirmed by combing the results of GWAS with fruit shape gene preliminary mapping. The F2 segregating population were derived from a cross between two inbred lines K2 (oval, FSI=1.54±0.13) and L1 (round, FSI=1.11±0.07), which were purified from commercial small watermelon varieties. Fine-mapping of the fruit shape gene ClFSI was conducted by developing molecular markers. Candidate gene was identified by gene annotation of the candidate region in watermelon reference genome ‘97103’ v1 and validated by using real-time quantitative PCR (qRT-PCR). 【Result】 The 1 152 F2 plants were used for fine mapping and the ClFSI gene was finally mapped into 63 kb region on chromosome 3 between FMFSI-1 and FMFSI-2, containing a total of 5 annotated genes. The Cla011257 gene belonged to the SUN gene family that has been reported to control the fruit shape. There were two SNPs identified in the genomic region of third exon of ClFSI gene in the watermelon oval line K2. One SNP was a mutation from G to A at Chr3: 26846636 (‘97103’ v1), which resulted in a mutation from asparagine acid (Asn) to aspartic acid (Asp). Another SNP was a mutation from G to A at Chr3: 26846636 (‘97103’ v1), which resulted in another mutation from glutamic acid (Glu) to lysine acid (Lys). The FSICAPS-2 functional molecular marker was developed based on the Chr3: 26847041 SNP site. qRT-PCR expression analysis showed that candidate gene expression level was not significantly difference in K2 (oval) and Charleston Gray (elongated), but both were significantly higher than that in L1 (round). 【Conclusion】In this study, the ClFSI gene was mapped into a 63 kb candidate region on chromosome 3, and Cla011257 was the good candidate gene. Chr3: 26847041 and Chr3: 26846636 mutations were important loci that caused elongation of different degrees in fruit shape. A functional marker FSICAPS-2 was developed, which could identify multiple mutation types of Cla011257 simultaneously.

Key words: watermelon, fruit shape gene, map-based cloning, molecular marker

Fig. 1

Phenotype of mature fruit and ovary of parents K2 and L1 A: Matured fruit of oval watermelon K2; B: Matured fruit of round watermelon L1; C: Ovary of oval watermelon K2; D: Ovary of round watermelon L1"

Table 1

Primers information of candidate gene clones"

引物名称Primer name 正向序列
Forward primer		 反向序列
Reverse primer		 产物长度
Product length (bp)
FSIgene-1 GGACTCAATTTGTAGAGCATGG AAGAACGCAGTGATGAGCAA 460
FSIgene-2 TCGAGTTTGCTCATCACTGC CGGAATTAAGCGACGACCTA 463
FSIgene-3 TCCGGCAATCTGGGATTT ATTAGGCGAGGAAAGCACTG 556
FSIgene-4 CAGTGCTTTCCTCGCCTAAT GAAAAATGGGGAGAGCAACC 547

Table 2

Candidate gene qRT-PCR primers information"

引物名称 Primer name 正向序列 Forward primer 反向序列 Reverse primer
qClFSI AAGGGTTTCGTTGAATGAATTG GGCTTCTTGAACTTGAGAACA
Actin CCATGTATGTTGCCATCCAG GGATAGCATGGGGTAGAGCA

Table 3

Statistics of phenotypic fruit shape related traits"

性状
Trait		 K2 (n=20) L1 (n=20) F1 (n=20) 2016F2
均值±标准差
Mean±SD		 均值±标准差
Mean±SD		 均值±标准差
Mean±SD		 均值±标准差
Mean±SD		 范围
Range		 峰度
Kurtosis		 偏度
Skewness
果实纵径 Fruit length (cm) 20.4±3.0A 15.3±2.4B 19.3±2.6A 16.2±2.6 10.8-23.6 -0.18 0.40
果实横径 Fruit width (cm) 13.3±1.5b 13.8±1.8b 15.4±1.3a 13.6±1.2 9.7-18.5 -0.42 0.16
果形指数 Fruit shape index (cm) 1.54±0.13A 1.11±0.07B 1.26±0.22B 1.20±0.20 0.92-1.77 0.27 1.09

Fig. 2

Frequency distribution of fruit shape related traits in F2 population"

Table 4

Spearman's rank correlation coefficients among fruit shape traits"

性状 Trait 果实纵径 Fruit length 果实横径 Fruit diameter 果形指数 Fruit shape index
果实纵径 Fruit length 1
果实横径 Fruit width 0.43** 1
果形指数 Fruit shape index -0.38** 0.67** 1

Fig. 3

Linkage analysis between qfsi3.1 and phenotypic markers of fruit shape index (FSI) The red, green and blue lines are the fruit shape index, fruit length and fruit width respectively"

Fig. 4

Fine mapping of the ClFS1 A: Results of the preliminary designation of GBS high-density genetic mapping; B: The primary mapping of ClFS1 gene, numbers above markers indicated the linkage genetic distance; C: Fine mapping of the ClFS1 gene, numbers under markers indicated the numbers of recombinants; D: Candidate genes within the mapping interval, the while arrows indicated annotated open reading frames and the black arrows indicated candidate genes in this region; E: Structure of ClFS1 gene, black represents three exons, and red triangle represents the mutation site on the exon"

Table 5

KAPS primers used for fine mapping"

引物名称
Primer name		 物理位置（V1）
Physical position		 变异位点
Variation locus		 引物序列
Pprimer sequence (5' to 3')
FMFSI-3 chr3-26695927 C/A Fa: GAAGGTGACCAAGTTCATGCTGTAAGAACAGCCAAATGTTGAACAAATC
Fb: GAAGGTCGGAGTCAACGGATTTTGTAAGAACAGCCAAATGTTGAACAAATA
R: CAAGACAGTGATCTTTTCACAACACAATAATT
FMFSI-4 chr3-26775520 G/C Fa: GAAGGTGACCAAGTTCATGCTGTAATAAATGTGGAGGAAATATGGCTAC
Fb: GAAGGTCGGAGTCAACGGATTGTAATAAATGTGGAGGAAATATGGCTAG
R: TAACCATTTACTTTTTTGGTTTTGGTTTTTGAAAA
FMFSI-1 chr3-26801978 C/T Fa: GAAGGTGACCAAGTTCATGCTACACATTCTAATGCCCTAGTTAGTAC
Fb: GAAGGTCGGAGTCAACGGATTCACACATTCTAATGCCCTAGTTAGTAT
R: TTGGATCATCGAATTTTATGAACACTCCTAT

Table 6

CAPS and dCAPSprimers used for fine mapping"

引物名称
Primer name		 物理位置（V1）
Physical position		 变异位点
Variation locus		 正向序列
Forward sequence		 反向序列
Reverse sequence		 限制性内切酶Restriction endonuclease
GFSI-1 chr3-26846636 C/T AGACTACTTCTCGATTCCATGAATT CGGAATTTCCATGACTCTGA EcoR I (dCPAS)
FSICAPS-2 chr3-26847041 C/T ACCGCCAGAGTTCACAAATC ATTAGGCGAGGAAAGCACTG Taq I
FM-FSI-2 chr3-26864789 C/G AATTGATGGGGGTATCGTGA TGGTTGGGGTTATTTGGGTA Rsa I
CW3CAPS47 chr3-26882166 T/G GAACCAATACCAACGGGAAT TGCATGAGCCAAAATTCACT Xho I
CHR3-FSI-3 chr3-26940134 T/C CTTTGAAGTTCGGAGGTTGG ATGGATCAAACAGACGCAAA Taq I
CHR3-FSI-5 chr3-26945758 A/G CCAAGCAGGCCAAATAACAT GCCAAATTTTCGAAGCACAG Hind II
CHR3-FSI-7 chr3-27106460 G/A CAAAAGCCTCCAAGTTCCAG AAGCTGGTGGTCTTGGTTTG Taq I
CHR3-FSI-11 chr3-27121470 C/T TTGATCGCTGGAGATGAATG GCATCGGTTTTGGAAGGATA Hind III

Table 7

Information of predicted genes in candidate segments"

编号
No.		 基因号
Gene ID		 基因功能
Gene function		 基因位置
Region in ‘97103’ v1
1 Cla011252 低温诱导蛋白 Cold induced protein like (AHRD V1 *---Q94JH8_ORYSJ) Chr3: 26806979-26807611 (+strand) 633 bp
2 Cla011253 精氨酸tRNA合成酶 Arginine tRNA synthetase (AHRD V1 **** O23247_ARATH);
含有Interpro结构域IPR001278 Contains interpro domains IPR001278,精氨酸tRNA合成酶 Arginine tRNA synthetase,IC类 Class IC		 Chr3: 26809083-26816437 (-strand) 7355 bp
3 Cla011254 未知蛋白质 Unknown protein (AHRD V1) Chr3: 26819389-26819613 (+strand) 225 bp
4 Cla011255 激酶家族蛋白 Kinase family proteins (AHRD V1 ***-D7MCM2_ARALL);含有Interpro结构域IPR002290 Contains interpro domains IPR002290,丝氨酸/苏氨酸蛋白激酶 Serine/ Threonine protein kinase Chr3: 268219 46-26833394 (+strand) 11449 bp
5 Cla011256 果胶酯酶 Pectin esterase (AHRD V1 ***-B9RKG6_RICCO);含有Interpro结构域IPR000070 Contains interpro domains IPR000070,果胶酯酶 Pectin esterase,具有催化作用 With catalysis Chr3: 26838409-26839804 (+strand) 1396 bp
6 Cla011257 钙调素结合家族蛋白 Calmodulin binding family proteins (AHRD V1 **-* Q9ZU28_ ARATH);含有Interpro域IPR000048 IQ Contains interpro domains IPR000048 IQ,钙调蛋白结合区 Calmodulin-binding domain Chr3: 26846490-26847637 (-strand) 1148 bp

Fig. 5

Locus of watermelon fruit shape was identified through GWAS"

Fig. 6

The changes of fruit shape related traits at different developmental stages of watermelon"

Fig. 7

Expression analysis of Cla011257 in different strains Data are the means of three replicates (±SD). Analysis of relative transcript abundance used expression of Cla011257 in L1 as the reference (*: P<0.05)"

Fig. 8

FSICAPS-2 Molecular markers for the identification of fruit shape in selected natural watermelon populations 1-6: Elonglate watermelon strains; 7-12: Oval watermelon strains; 13-18: Round watermelon strains"

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