Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (16): 3168-3182.doi: 10.3864/j.issn.0578-1752.2023.16.010

• HORTICULTURE • Previous Articles     Next Articles

Mining Genes Related to Fruit Quality in Sweet Oranges Based on Specific Locus Amplified Fragment Sequencing

LI RenJing(), SHEN WanXia, ZHAO WanTong, CHENG Li, LI Pei, JIANG Dong()   

  1. Citrus Research Institute, Southwest University, Chongqing 400712
  • Received:2022-12-17 Accepted:2023-02-13 Online:2023-08-16 Published:2023-08-18

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Abstract:

【Objective】By using specific locus amplified fragment sequencing (SLAF-seq) sequencing method and combined with fixation indices analysis on different sweet orange populations, the candidate genes related with some excellent traits in sweet orange were mined, so as to provide some candidate genes for the further molecular breeding in sweet orange. 【Method】SLAF-seq technology was used to genotype 240 sweet orange germplasm resources, which represented extensive genetic diversity and from different geographical origins accessions preserved in the National Citrus Germplasm Repository in Beibei of Chongqing. The genomic SNP genotype data were obtained using the sweet orange genome as the reference, and the Fst and XP-CLR values between different subpopulations were calculated. 【Result】A total of 497.82 Mb-reads were obtained by sequencing 240 sweet oranges accessions with SLAF-seq technology, after the sequencing reads were mapped on to the reference genome by BWA software, and a total of 1 467 968 SNPs were identified by GATK and samtools. The Fst and XP-CLR indices were used to screen out candidate genes related to three traits, including fruit navel occurrence, fruit weight, and titratable acid content. Those genes adjacent to the selected SNPs were called. The result showed that orange1.1G044639m and orange1.1g023641m which annotated auxin efflux vector were related to the formation of navel in sweet orange. SNP in orange1.1G023641m which encoded E3 ubiquitin ligase had the highest Fst score between two different single-fruit weight population, and orange1.1G046891m might affect fruit weight by regulating carbohydrate formation; orange1.1G011684m encoding dihydrolipoamide transacetylase of PDH, and the SNP caused a nonsynonymous mutation in its CDS region, which might determine the citric acid content in fruit; orange1.1G034502m encodes Serine/threonine protein kinase, annotated as phosphorylation dephosphorylation function also related with the citric acid content in fruit. 【Conclusion】In this study, the Fst indices were used to screen six candidate genes associated with three fruit traits in sweet orange by using SNPs from SLAF-seq data. Finally, the relevant genes were screened out for three horticultural traits, including navel occurrence, fruit weight and titratable acid content, and the identified candidate genes should be giving further investigation to explore their regulation mechanism in these traits.

Key words: SLAF-seq, Fst, XP-CLR, sweet orange, fruit weight, titratable acids content, fruit navel occurrence

Table 1

240 accessions of sweet oranges used in this study"

编号 Code 材料名称 Common name 编号 Code 材料名称 Common name
1 橘园甜橙 Ju Yuan Sweet Orange 40 广东选育雪柑 Xue Gan (Guangdong Selection)
2 塔罗科血橙（Thermal） Tarocco Thermal Blood Orange 41 眉红橙 Mei Hong Navel Orang
3 塔罗科血橙（Bream） Tarocco Bream Blood Orange 42 眉红脐橙 Mei Hong Navel Orang
4 瓦尼利亚甜橙 Vaniglia Sanguigno Acidless Sweet Orange 43 金儿柑 Jin Er Gan
5 嘉法甜橙 Jaffa Sweet Orange 44 脐橙 Navel Orange
6 利马甜橙 Lima Sweet Orange 45 桃叶橙18号Peach Leaf Sweet Orange No.18
7 哈资3号 Hua Zhi No.3 46 宜园3号 Yi Yuan Jin Cheng No.3
8 威尼 Wheeny 47 埃及2号糖橙 Egypt Sweet Orange No.2
9 脐橙 Navel Orange 48 埃及2号甜橙 Egypt Sweet Orange No.2
10 猴橙 Hou Cheng 49 椭圆哈姆林 Hamlin (Tuo Yuan)
11 甜橙 Sweet Orange 50 江北梅柑 Jiang Bei Mei Gan
12 利马甜橙 Lima Sweet Orange 51 克拉斯特脐橙 Cluster Navel
13 罗布脐橙 Rhobs El Arsa 52 云南黄果Yun Nan Huang Guo
14 澳大利亚红 Australian Red 53 秭归2号甜橙 Zi Gui Tian Cheng No.2
15 意大利 Italian 54 日本柳叶橙 Liu Ye Cheng (Japan)
16 晚红8号 Wan Hong No.8 55 兴国甜橙 Xing Guo Sweet Orange
17 普通甜橙 Sweet Orange 56 江津柳叶橙 Liu Ye Cheng (Jiangjin)
18 纽荷尔脐橙 Newhall Navel Orange 57 凤梨甜橙 Pineapple Sweet Orange
19 夏金脐橙 Summer Gold Navel Orange 58 哈姆林 Hamlin
20 脐橙 Navel Orange 59 帕森布朗 Parson Brown
21 脐橙 Navel Orange 60 皱皮柑 Zhou Pi Gan
22 脐橙 Navel Orange 61 埃及1号甜橙 Egypt Sweet Orange No.1
23 脐橙 Navel Orange 62 早熟雪柑 Early Xue Gan
24 晚熟甜橙 Late Season Sweet Orange 63 福本脐橙 Fukumoto Navel Orange
25 普通甜橙 Sweet Orange 64 小叶先锋橙 Xiao Ye Xian Feng Cheng
26 塔罗科血橙 Tarocco Blood Orange 65 松林1号 Song Lin No.1
27 类橘脐橙 Mandarin Navel Orange 66 云南高尖黄果 Yun nan Gao Jian Huang Guo
28 柳江甜橙 Liu Jiang Sweet Orange 67 花叶香橙 Hua Ye Xiang Cheng
29 宽皮桔 Mandarin 68 古巴花叶橙 Gu Ba Hua Ye Cheng
30 脐橙 Navel Orange 69 花叶锦橙 Variegated Jin Cheng
31 佩拉甜橙 Pera Sweet Orange 70 香水橙 Xiang Shui Cheng
32 夏橙 Valencia Sweet Orange 71 红毛橙 Hong Mao Cheng
33 夏橙 Valencia Sweet Orange 72 冰糖橙（仁5） Bing Tang Cheng (Ren No.5)
34 脐橙 Navel Orange 73 冰糖橙（仁4） Bing Tang Cheng (Ren No.4)
35 脐橙 Navel Orange 74 福贡甜橙 Fu Gong Tian Cheng
36 塔罗科血橙Tarocco Blood Orange 75 先锋橙4号 Xian Feng Cheng No.4
37 夏橙 Valencia Sweet Orange 76 津华橙 Jin Hua Cheng
38 夏橙 Valencia Sweet Orange 77 金山橙（广东） Jin Shan Cheng (Guangdong)
39 脐橙 Navel Orange 78 蓬安100号 Peng An No.100 Jin Cheng
79 梨橙2号 Pear Shape Sweet Orange No. 2 119 脐血橙 Washington Sanguine Blood Orange
80 纽荷尔 Newhall Navel Orange 120 脐血橙 Washington Sanguine Blood Orange
81 甜皮甜橙（西农） Tian Pi Sweet Orange (Xinong) 121 蜜奈夏橙 Midknight Valencia
82 索尔斯蒂安娜 Salustiano Orange 122 鲍威尔 Powell Navel Orange
83 零号甜橙 Sweet Orange No.0 123 路德红夏橙 Rhod Red Valencia Orange
84 巴西脐橙9号 Brasiliano Navel Orange No.9 124 奥林达夏橙 Olinda Valencia Orange
85 中育8号 Zhong Yu No.8 125 康拜尔夏橙 Campbell Valencia Orange
86 大红8号 Da Hong No.8 126 阿尔及尔夏橙 Algiers Valencia Orange
87 摩洛血橙 Moro Blood Orange 127 岛仔51甜橙 Dao Zai No.51 Sweet Orange
88 78-1 128 夏橙（珠心系） Valencia Nucellar
89 脐血橙5号（实生） Washington Sanguine (seedling No.5) 129 伏罗斯特夏橙（N.L） Frost Valencia Orange (N.L)
90 脐血橙3号（实生） Washington Sanguine (seedling No.3) 130 夏橙 Valencia
91 红肉暗柳橙 Pink Flesh An Liu Chen 131 刘金刚夏橙 Liu Jin Gang Valencia Orange
92 脐血橙2号（实生） Washington Sanguine (seedling No.2) 132 五月红51-13夏橙 Wu Yue Hong 51-13
93 脐血橙1号（实生） Washington Sanguine (seedling No.1) 133 五月红51-14夏橙 Wu Yue Hong 51-14
94 奥伐来血橙 Ovale Blood Orange 134 晚熟6号 Wan Shu No.6
95 红玉血橙 Ruby Blood Orange 135 晚脐 Late Navel Orange
96 塔罗科（valencia）Tarocco (valencia) 136 蓬安晚脐 Peng An Late Navel Orange
97 塔罗科（O.L） Tarocco (O.L) 137 晚熟脐橙 Late Navel Orange
98 塔罗科（Rosso Italy） Tarocco (Rosso Italy) 138 夏田脐橙 Summer Field Navel Orange
99 塔罗科（N.L） Tarocco (N.L) 139 早熟脐橙 Early Navel Orange
100 桑吉内劳血橙 Sanguinello 140 大三岛脐橙 Omishima Navel Orange
101 红江橙 Hong Jiang Cheng 141 丰脐 High Yield Navel Orange
102 脐血橙（2号） Washington Sanguine (No.2) 142 森田脐橙 Morita Navel Orange
103 脐血橙2号 Washington Sanguine No.2 143 吉田脐橙 Yoshida Navel Orange
104 洛比血橙（O.L） Ruby Blood Orange (O.L.) 144 白柳脐橙 Shirayanagi Navel Orange
105 洛比血橙（澳） Ruby Blood Orange (AUS) 145 福本脐橙Fukumoto Navel Orange
106 木索血橙 Aroncio Tarocco Dal Muso Blood Orange 146 铃木脐橙 Suzuki Navel Orange
107 马尔他斯血橙 Maltese Blood Orange 147 费希尔脐橙 Fisher Navel Orange
108 靖县血橙 Jing Xian Blood Orange 148 伏罗斯特脐橙 Frost Navel Orange
109 血橙 Blood Orange 149 阿特伍德脐橙 Atwood Navel Orange
110 血橙 Blood Orange 150 锦红最甜 Jin Hong Bing Tang Cheng (Zui Tian)
111 实美橙 Shi Mei Cheng 151 锦红大果 Jin Hong Bing Tang Cheng (Da Guo)
112 沃克曼脐橙 Workman Navel Orange 152 锦红最红 Jin Hong Bing Tang Cheng (Zui Hong)
113 阿华6-2 A Hua 6-2 153 林娜脐橙（西） Navelina Navel Orange (Xi)
114 宜红橙 Yi Hong Orange 154 林娜脐橙（O.L）Navelina Navel Orange (O.L)
115 卡特尼拉 Cadenera 155 纽荷尔脐橙 Newhall Navel Orange
116 早金 Early Gold Sweet Orange 156 卡尔特脐橙 Carter Navel Orange
117 班菲尔晚脐橙 Barnfield Late Navel Orange 157 卡尔特（美国） Carter Navel Orange (USA)
118 橙固酸橙 Cheng Gu Sour Orange 158 清家脐橙 Seike Navel Orange
159 哈姆林甜橙 Hamlin 200 仑头橙 Lun Tou Cheng
160 奉节4-21 Feng Jie 4-21 201 早熟甜橙（万县） Early Sweet Orange (Wanxian)
161 柳叶橙 Willow Leaf Sweet Orange 202 开县无核甜橙 Kai Xian Seedless Tian Cheng
162 古巴柳叶橙 Liu Ye Cheng (Cuba) 203 1号安江大红甜橙 Da Hong Tian Cheng No.1
163 印子柑 Yin Zi Gan 204 卡特尼拉（联合国） Cadenera Sweet Orange (U.N.)
164 冰糖橙 Bing Tang Cheng 205 卡特尼拉（摩洛哥） Cadenera Sweet Orange (Morocco）
165 冰糖柑53-3 Bing Tang Gan 53-3 206 卡特尼拉（珠心系） Cadenera Nucellar Sweet Orange
166 冰糖柑53-93 Bing Tang Gan 53-93 207 红毛橙 Hong Mao Cheng
167 冰糖柑53-94 Bing Tang Gan 53-94 208 8045甜橙 Sweet Orange 8045
168 冰糖柑53-4 Bing Tang Gan 53-4 209 桃叶橙8号 Tao Ye Cheng No.8
169 汤姆逊 Thompson Navel Orange 210 广西香水橙 Guang Xi Xiang Shui Cheng
170 华脐214 Washinton Navel Orange No.214 211 朱砂柑 Zhu Sha Gan
171 石棉脐橙 Shi Mian Navel Orange 212 新会红橙 Xin Hui Hong Cheng
172 汤姆逊脐橙（美N.L） Thompson Navel Orange (USA N.L) 213 义安橙 Yi An Cheng
173 实生华脐 Washington Navel Orange (Seedling) 214 乔伯橙 Joppa Sweet Orange
174 华脐 Washinton Navel Orange 215 C3
175 突尼斯脐橙 Tunisia Navel Orange 216 籍发橙 Jaffa Sweet Orange
176 埃及脐橙 Egypt Navel Orange 217 八棱甜橙 Ba Leng Tian Cheng
177 罗脐 Robertson Navel Orange 218 黄皮甜橙 Huang Pi Sweet Orange
178 鲁滨逊脐橙 Robertson Navel Orange 219 桔红橙 Ju Hong Cheng
179 金堂脐橙 Early Navel Orange (Jintang) 220 武夷橙 Wu Yi Cheng
180 新华1号脐橙 Xin Hua Navel Orange No.1 221 宜园161 Yi Yuan 161 Jin Cheng
181 锦橙（铜水72-1） Jin Cheng (Tongshui 72-1) 222 9号桐子柑 Tong Zi Gan No.9
182 开县72-1锦橙 Jin Cheng (Kaixian 72-1) 223 桐子柑57-36Tong Zi Gan 57-36
183 72-12先锋橙 Xian Feng Cheng 72-12 224 化州橙（实生） Hua Zhou Cheng (Seedling)
184 S20先锋橙 Xian Feng Cheng (S20) 225 化州橙（O.L） Hua Zhou Cheng (O.L)
185 S26锦橙Jin Cheng (S26) 226 红橘广柑 Hong Ju Guang Gan
186 鹅蛋柑8号 E Dan Gan No.8 227 改良橙 Gai Liang Cheng
187 447锦橙 447 Jin Cheng 228 重瓣甜橙 Chong Ban Tian Cheng
188 梨形甜橙 Pear Shape Sweet Orange 229 槾先橙 Man Xian Cheng
189 雪柑（N.L) Xue Gan (N.L) 230 广橘甜橙 Guang Ju Tian Cheng
190 雪柑（一区） Xue Gan (Yiqu) 231 卡拉卡拉红肉脐橙 Cara Cara Navel Orange
191 汉源无核甜橙 Han Yuan Seedless Sweet Orange 232 晚棱脐橙 Lane's Late Navel Orange
192 无核甜橙 Seedless Sweet Orange 233 塔罗科血橙（新系） Tarocco New Line
193 大萼甜橙（万县） Da E Tian Cheng 234 8号血橙 Blood Orange No.8
194 深红皮甜橙 Shen Hong Pi Tian Cheng 235 塔罗科血橙 Tarocco Blood Orange
195 深红皮甜橙 Shen Hong Pi Tian Cheng 236 瓦尼利亚甜橙 Vaniglia Sanguigno Acidless Sweet Orange
196 辰溪早熟甜橙 Early Tian Cheng (Chenxi) 237 夏橙 Valencia Sweet Orange
197 南充单胚甜橙 Nan Chong Dan Pei Tian Cheng 238 95-1奉晚脐橙 Feng Jie Late Navel Orange (95-1)
198 普通甜橙（7-26） Sweet Orange (72-6) 239 大果锦橙 Large Fruit Jing Chen
199 开县薄皮甜橙 Kai Xian Bao Pi Tian Cheng 240 93-3脐橙 Navel Orange 93-3

Table 2

qPCR primers"

引物名称
Primer name		 正向引物序列
Forward primer sequence		 反向引物序列
Reverse primer sequence
orange1.1g011684m GTTGGAGCATCAAAGCCAAT ATTCGGTGATCAGCGGTTAC
orange1.1g034502 ACGCTAGTGATGGGAAATTCTCA AAGGTTAAGCTTGTTGTCGGAA
β-Actin CCCCATCGTTACCGTCCAG CGCCTTGCCAGTTGAATATCC

Fig. 1

The principal component analysis of 240 sweet orange accessions"

Fig. 2

Population structure analysis of 240 sweet orange accessions Blue refer to Q1, Red refer to Q2, Green refer to Q3"

Fig. 3

Genome-wide Fst values (A) and XP-CLR selective sweep analysis (B) of fruit navel occurrence in two sweet orange populations"

Fig. 4

Genome-wide Fst values (A) and XP-CLR selective sweep analysis (B) of fruit weight in two different sweet orange populations"

Fig. 5

Genome-wide Fst values (A) and XP-CLR selective sweep analysis (B) calculated using two high-acid and low-acid sweet orange populations"

Fig. 6

Content and change trend of TA in the juice of six sweet orange cultivars"

Fig. 7

Relative expression of orange1.1g034502m during orange fruit development"

Fig. 8

Relative expression of orange1.1g011684m during fruit development for six sweet orange cultivars"

Fig. 9

The mutation occurring in orange1.1g011684 resulted in amino acid G change to S"

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