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Acta Agronomica Sinica ›› 2024, Vol. 50 ›› Issue (8): 1971-1988.doi: 10.3724/SP.J.1006.2024.31080

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

Cloning and functional analysis of ubiquitin-conjugating enzymes TaUBC16 gene in wheat

GAO Wei-Dong1,2(), HU Chen-Zhen1,2, ZHANG Long1,2, ZHANG Yan-Yan1,2, ZHANG Pei-Pei1, YANG De-Long1,2,*(), CHEN Tao1,2,*()   

  1. 1State Key Laboratory of Aridland Crop Science, Lanzhou 730070, Gansu, China
    2College of Life Science and Technology, Gansu Agricultural University, Lanzhou 730070, Gansu, China
  • Received:2023-12-16 Accepted:2024-04-01 Online:2024-08-12 Published:2024-04-18
  • Contact: * E-mail: yangd1@gsau.edu.cn;E-mail: chent@gsau.edu.cn
  • Supported by:
    Central Guidance on Science & Technology Development of Gansu(23ZYQA0322);Industrial Support Plan of Colleges and Universities in Gansu Province(2022CYZC-44);Key Sci & Tech Special Project of Gansu Province(22ZD6NA009);National Natural Science Foundation of China(32360518);National Natural Science Foundation of China(32160487);“Innovation Star” Project of Gansu Province Outstanding Postgraduate Students(2023CXZX-684)

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Abstract:

E2 ubiquitin-conjugating enzyme plays an important role in regulating plant growth and development, and stress signal transduction. In this study, the TaUBC16 gene encoding E2 ubiquitin-conjugating enzyme was cloned from the cDNA of the drought-tolerant wheat cultivar Jinmai 47. The gene was 447 bp in length and encoded 148 amino acids. The cis-acting element analysis showed that the promoter region of TaUBC16 contained various cis-acting elements related to meristem development, stress responses, and plant hormone responses. By the wheat RNA-seq transcriptome data analysis combined with qRT-PCR validation, it was found that TaUBC16 was generally expressed in different tissues/organs and at different growth stages of wheat, whereas the highest expression level was exhibited in developing grains at 30 days after anthesis. The relative expression level of TaUBC16 was highly induced by PEG, mannitol, and ABA stresses. The subcellular localization in tobacco leaves and wheat protoplasts showed that TaUBC16 proteins were located in both cytoplasm and nucleus. The phenotypic analysis of the heterologous expression of TaUBC16 in transgenic Arabidopsis revealed that the transgenic lines had earlier flowering time than the wild type, and its seeds were more plumpness with higher 1000-grain weight than the wild type. Based on the polymorphism of the promoter region -388 bp site (T-A), a kompetitive allele-specific PCR (KASP) marker of TaUBC16 gene was developed and its haplotypes were identified. The haplotype TaUBC16-Hap I had higher thousand-kernel weight, kernel length and width than TaUBC16-Hap II, and had been subjected to positive selection in wheat breeding processes in China. The results of this study provide a theoretical basis for further revealing the involvement of the TaUBC16 gene in the regulation of wheat growth and development and the molecular mechanism responding to adverse stresses.

Key words: wheat, TaUBC16, gene expression, subcellular localization, transgenesis, KASP marker

Table S1

KASP call data at -388 bp in 246 natural population of wheat"

序号
Accession No.		 名称
Name		 标记
Marker (bp)		 基因型
Allele
1 08-133-13-2-2-1-4 −388 T/T
2 09-228-9-2-1-1-1-2 −388 T/T
3 10-160-6-1-1-5-2-3 −388 T/T
4 11-257-4--1 −388 T/T
5 12-37-10-1-4 −388 T/T
6 B160-2-2-1-1 −388 T/T
7 Q9086 −388 T/T
8 北京837 Beijing837 −388 T/T
9 北京8694 Beijing8694 −388 T/T
10 沧麦6001 Cangmai6001 −388 T/T
11 沧麦6005 Cangmai6005 −388 T/T
12 昌乐5 Changle5 −388 T/T
13 冬03-07 Dong03-07 −388 T/T
14 泛麦8 Fanmai8 −388 T/T
15 旱选1 Hanxuan1 −388 T/T
16 衡观35 Hengguan35 −388 T/T
17 济麦19 Jimai19 −388 T/T
18 济麦22 Jimai22 −388 T/T
19 济麦23 Jimai23 −388 T/T
20 济南13 Jinan13 −388 T/T
21 济南17 Jinan17 −388 T/T
22 冀麦32 Jimai32 −388 T/T
23 京冬8 Jingdong8 −388 T/T
24 京双2 Jingshuang2 −388 T/T
25 康庄974 Kangzhuang974 −388 T/T
26 莱州953 Laizhou953 −388 T/T
27 兰天20 Lantian20 −388 T/T
28 兰天21 Lantian21 −388 T/T
29 兰天2 Lantian2 −388 T/T
30 兰天4 Lantian4 −388 T/T
31 良星99 Liangxing99 −388 T/T
32 陇育5 Longyu5 −388 T/T
33 鲁麦15 Lumai15 −388 T/T
34 鲁麦17 Lumai17 −388 T/T
35 轮抗7 Lunkang7 −388 T/T
36 洛旱6 Luohan6 −388 T/T
37 漯麦8 Luomai8 −388 T/T
38 漯优7 Luoyou7 −388 T/T
39 宁冬11 Ningdong11 −388 T/T
40 青麦7 Qingmai7 −388 T/T
41 清山843 Qingshan843 −388 T/T
42 山农辐63 Shannongfu63 −388 T/T
43 太13606 Tai13606 −388 T/T
44 泰山1 Taishan1 −388 T/T
45 泰山23 Taishan23 −388 T/T
46 皖麦19 Wanmai19 −388 T/T
47 西峰16 Xifeng16 −388 T/T
48 西峰28 Xifeng28 −388 T/T
49 西农219 Xinong219 −388 T/T
50 鑫麦296 Xinmai296 −388 T/T
51 偃展1 Yanzhan1 −388 T/T
52 豫麦2 Yumai29 −388 T/T
53 郑丰9962 Zhengfeng9962 −388 T/T
54 郑州24 Zhengzhou24 −388 T/T
55 中7902 Zhong7902 −388 T/T
56 中优9507 Zhongyou9507 −388 T/T
57 周麦18 Zhoumai18 −388 T/T
58 0025-17-1 −388 A/A
59 00-71 −388 A/A
60 45329 −388 A/A
61 1-4-8-1 −388 A/A
62 1R1 −388 A/A
63 1R14 −388 A/A
64 1R25 −388 A/A
65 1R38 −388 A/A
66 21-30 −388 A/A
67 22-23 −388 A/A
68 45318 −388 A/A
69 47151 −388 A/A
70 85-173-4 −388 A/A
71 94164-1 −388 A/A
72 980-4-1-1-2 −388 A/A
73 988-4-2-4-1 −388 A/A
74 99384-2-1 −388 A/A
75 A80-3-1-1-3 −388 A/A
76 A8-4-4-2 −388 A/A
77 A88-4-2-4 −388 A/A
78 B11-2-3-1-1-2 −388 A/A
79 B17-2-3-2-1 −388 A/A
80 B61-2-3-2-1 −388 A/A
81 C130-5-1-1 −388 A/A
82 C42-2-3-3 −388 A/A
83 C47-1-1-2 −388 A/A
84 C49-1-1-1-2 −388 A/A
85 C55-8-1-3-1 −388 A/A
86 C78-3-6-1-3 −388 A/A
87 E69-4-1 −388 A/A
88 E71-2-6 −388 A/A
89 E72-2-2 −388 A/A
90 H-4-2-2-1 −388 A/A
91 白齐麦 Baiqimai −388 A/A
92 百农160 Bainong160 −388 A/A
93 东农024 Dongnong024 −388 A/A
94 冬协2 Dongxie2 −388 A/A
95 丰产1 Fengchan1 −388 A/A
96 邯4589 Han4589 −388 A/A
97 邯6172 Han6172 −388 A/A
98 旱选2 Hanxuan2 −388 A/A
99 旱选3 Hanxuan3 −388 A/A
100 航选01 Hangxuan01 −388 A/A
101 航选121 Hangxuan121 −388 A/A
102 衡136 Heng136 −388 A/A
103 衡216 Heng216 −388 A/A
104 衡4399 Heng4399 −388 A/A
105 衡5229 Heng5229 −388 A/A
106 衡7228 Heng7228 −388 A/A
107 衡水6404 Hengshui6404 −388 A/A
108 衡优18 Hengyou18 −388 A/A
109 红良4 Hongliang4 −388 A/A
110 互助红 Huzhuhong −388 A/A
111 花培6 Huapei6 −388 A/A
112 华北187 Huabei187 −388 A/A
113 淮麦18 Huaimai18 −388 A/A
114 淮麦25 Huaimai25 −388 A/A
115 淮沭10 Huaishu10 −388 A/A
116 济麦20 Jimai20 −388 A/A
117 济麦262 Jimai62 −388 A/A
118 济麦44 Jimai44 −388 A/A
119 济麦4 Jimai4 −388 A/A
120 济麦6 Jimai6 −388 A/A
121 冀麦22 Jimai22 −388 A/A
122 冀麦26 Jimai26 −388 A/A
123 冀麦29 Jimai29 −388 A/A
124 冀麦6 Jimai6 −388 A/A
125 冀麦9 Jimai9 −388 A/A
126 鉴26 Jian26 −388 A/A
127 晋2148-7 Jin2148-7 −388 A/A
128 晋麦17 Jinmai17 −388 A/A
129 晋麦25 Jinmai25 −388 A/A
130 晋麦39 Jinmai39 −388 A/A
131 晋麦44 Jinmai44 −388 A/A
132 晋麦51 Jinmai51 −388 A/A
133 晋麦54 Jinmai54 −388 A/A
134 晋麦68 Jinmai68 −388 A/A
135 晋麦72 Jinmai72 −388 A/A
136 京东82东307 Jingdong82dong307 −388 A/A
137 京花1 Jinghua1 −388 A/A
138 科农199 Kenong199 −388 A/A
139 兰天10 Lantian10 −388 A/A
140 兰天12 Lantian12 −388 A/A
141 兰天13 Lantian13 −388 A/A
142 兰天14 Lantian14 −388 A/A
143 兰天15 Lantian15 −388 A/A
144 临138 Lin138 −388 A/A
145 临汾8050 Linfen8050 −388 A/A
146 临丰3(临旱5) Linfeng3 (Linhan5) −388 A/A
147 临丰615 Linfeng615 −388 A/A
148 临旱51241 Linhan51241 −388 A/A
149 临旱538 Linhan538 −388 A/A
150 陇鉴103 Longjian103 −388 A/A
151 陇鉴107 Longjian107 −388 A/A
152 陇鉴110 Longjian110 −388 A/A
153 陇鉴111 Longjian111 −388 A/A
154 陇鉴127 Longjian127 −388 A/A
155 陇鉴294 Longjian294 −388 A/A
156 陇鉴301 Longjian301 −388 A/A
157 陇麦079 Longmai079 −388 A/A
158 陇麦838 Longmai838 −388 A/A
159 陇麦847 Longmai847 −388 A/A
160 陇育218 Longyu218 −388 A/A
161 陇原937 Longyuan937 −388 A/A
162 陇源036 Longyuan036 −388 A/A
163 陇中1 Longzhong1 −388 A/A
164 陇中2 Longzhong2 −388 A/A
165 鲁德1 Lude1 −388 A/A
166 鲁麦14 Lumai14 −388 A/A
167 鲁麦19 Lumai19 −388 A/A
168 鲁麦3 Lumai3 −388 A/A
169 鲁麦5 Lumai5 −388 A/A
170 轮选987 Lunxuan987 −388 A/A
171 洛旱11 Luohan11 −388 A/A
172 洛旱2 Luohan2 −388 A/A
173 洛旱3 Luohan3 −388 A/A
174 洛旱7 Luohan7 −388 A/A
175 洛旱8 Luohan8 −388 A/A
176 洛麦21 Luomai21 −388 A/A
177 洛麦22 Luomai22 −388 A/A
178 洛麦23 Luomai23 −388 A/A
179 漯抗2 Luokang2 −388 A/A
180 漯麦9 Luomai9 −388 A/A
181 内麦11 Neimai11 −388 A/A
182 宁麦12 Ningmai12 −388 A/A
183 农大146 Nongda146 −388 A/A
184 清农3 Qingnong3 −388 A/A
185 清山 851 Qingshan851 −388 A/A
186 清山782 Qingshan782 −388 A/A
187 清山821 Qingshan821 −388 A/A
188 山农优麦2 Shannongyoumai2 −388 A/A
189 陕229 Shan229 −388 A/A
190 陕旱8675 Shanhan8675 −388 A/A
191 陕优225 Shanyou225 −388 A/A
192 石4185 Shi4185 −388 A/A
193 石家庄8 ShiJiazhuang8 −388 A/A
194 石麦12 Shimai12 −388 A/A
195 石麦13 Shimai13 −388 A/A
196 石麦15 Shimai15 −388 A/A
197 石麦19 Shimai19 −388 A/A
198 石优17 Shiyou17 −388 A/A
199 石优20 Shiyou20 −388 A/A
200 舜麦1718 Shunmai1718 −388 A/A
201 四棱红葫芦头 Silenghonghulutou −388 A/A
202 太原633 Taiyuan633 −388 A/A
203 温麦6 Wenmai6 −388 A/A
204 西峰20 Xifeng20 −388 A/A
205 西峰24 Xifeng24 −388 A/A
206 西农1018 Xinong1018 −388 A/A
207 西农1043 Xinong1043 −388 A/A
208 西农189 Xinong189 −388 A/A
209 西农318 Xinong318 −388 A/A
210 西农688 Xinong688 −388 A/A
211 西农797 Xinong797 −388 A/A
212 咸农4 Xiannong4 −388 A/A
213 新冬18 Xindong18 −388 A/A
214 新冬22 Xindong22 −388 A/A
215 徐州21 Xuzhou21 −388 A/A
216 烟农19 Yannong19 −388 A/A
217 烟农21 Yannong20 −388 A/A
218 延安15 Yanan15 −388 A/A
219 豫麦13 Yumai13 −388 A/A
220 豫麦29 Yumai29 −388 A/A
221 豫农416 Yunong416 −388 A/A
222 豫农949 Yunong949 −388 A/A
223 豫展4 Yuzhan4 −388 A/A
224 原冬3 Yuandong3 −388 A/A
225 运旱102 Yunhan102 −388 A/A
226 运旱115 Yunhan115 −388 A/A
227 运旱2028 Yunhan2028 −388 A/A
228 运旱21-30 Yunhan21-30 −388 A/A
229 运旱618 Yunhan618 −388 A/A
230 运旱719 Yunhan719 −388 A/A
231 运旱805 Yunhan805 −388 A/A
232 长4640 Chang4640 −388 A/A
233 长4738 Chang4738 −388 A/A
234 长6154 Chang6154 −388 A/A
235 长6359 Chang6359 −388 A/A
236 长6878 Chang6878 −388 A/A
237 长844 Chang844 −388 A/A
238 长8744 Chang8744 −388 A/A
239 长旱4738 Changhan4738 −388 A/A
240 长武521 Changwu521 −388 A/A
241 长治516 Changzhi516 −388 A/A
242 长治620 Changzhi620 −388 A/A
243 长治6406 Changzhi6406 −388 A/A
244 中麦36 Zhongmai36 −388 A/A
245 中麦553 Zhongmai553 −388 A/A
246 周麦16 Zhoumai16 −388 A/A

Table 1

Primers used in this study"

引物名称Primer name 引物序列Primer sequence (5'-3') 用途Purpose
TaUBC16-F ATGGCGTCCAAGAGGATCCT TaUBC16基因克隆
TaUBC16-R GCCCATGGCGTACTTCTGTG Cloning of TaUBC16
TaUBC16-qRT-PCR-F CGTTCACCGGTGGTCTATTT TaUBC16荧光定量PCR
TaUBC16-qRT-PCR-R GGCTCCACTGTTCCTTGAGA TaUBC16 fluorescent quantitative PCR
TaUBC16-OE-F CGACAGTGGTCCCAAAGAT 异源表达拟南芥鉴定
TaUBC16-OE-R GCCCATGGCGTACTTCTGTG Identification of heterologous expression in Arabidopsis
TaACTIN-F CCTTCCGTGTTCCCACTGTTG 小麦qRT-PCR内参(胁迫)[30]
TaACTIN-R ATGCCCTTGAGGTTTCCCTC qRT-PCR internal reference gene of wheat (stress)
TaGAPDH-F GACCCAGACAACTCGCAAC 小麦qRT-PCR内参(组织)[31]
TaGAPDH-R GGAATCCATGACCACCTAC qRT-PCR internal reference gene of wheat
(organization)
AtACTIN2-F GGCTCCTCTTAACCCAAAGGC 拟南芥RT-PCR内参[32]
AtACTIN2-R CACACCATCACCAGAATCCAG RT-PCR internal reference gene of Arabidopsis
TaUBC16-KASP-F1 GAAGGTCGGAGTCAACGGATTGTGGGGAGGGAAATAAGCA 竞争性等位基因特异性PCR (KASP)标记引物
Kompetitive allele-specific PCR (KASP) marker
TaUBC16-KASP-F2 GAAGGTGACCAAGTTCATGCTGGTGGGGAGGGAAATAAGCT
TaUBC16-KASP-R TGGCGTCTTGTTTGCGAA

Table 2

Websites for software used in bioinformatics analysis"

软件Software 用途Function 网址Website
GSDS [39] 基因结构分析 Gene structure analysis http://gsds.gao-lab.org/
PlantCARE [40] 顺式作用元件分析 Cis-element analysis https://bioinformatics.psb.ugent.be/webtools/plantcare/html/
ChiPlot [41] 进化分析 Phylogenetic analysis https://www.chiplot.online/chitree.html
STRING [42] 蛋白互作分析 Protein interaction analysis https://string-db.org/
Gpos-mPLoc [43] 亚细胞定位预测 Subcellular localization prediction http://www.csbio.sjtu.edu.cn/bioinf/Gposmulti/

Fig. 1

CDS sequence cloning of TaUBC16 A: PCR amplification of TaUBC16 CDS sequence. B: sequence alignment of TaUBC16 gene in JM47 and Chinese Spring. C: structural analysis of TaUBC16 gene in wheat."

Fig. 2

Subcellular localization of TaUBC16 A: subcellular localization of TaUBC16 in tobacco leaves. B: subcellular localization of TaUBC16 in wheat protoplasts. The vector control (35S::GFP) and fusion protein vector (35S::TaUBC16-eGFP) were each introduced into tobacco leaves and wheat protoplasts. GFP was observed with laser scanning confocal microscope. Bar: 10 μm."

Fig. 3

TaUBC16 sequence analysis A: conservative motif analysis of wheat TaUBC16 protein. B: analysis of cis-acting elements in wheat TaUBC16 promoter. GD: growth and development; HR: hormonal response; SR: stress response."

Table 3

Cis-acting elements and functional annotations of TaUBC16 gene"

顺式元件
Cis-acting element		 数量
Number		 功能
Function
as-1 1 压力响应元件 Pressure response element
CCGTCC-box 2 响应昼夜节律相关顺式作用元件 Response to circadian rhythm related cis-acting elements
CCGTCC motif 2 分生组织表达顺式作用元件 Expression of cis-acting elements in meristem tissue
CGTCA-motif 1 茉莉酸响应顺式作用元件 Jasmonic acid responsive cis-acting element
circadian 1 分生组织特异性激活顺式作用元件 Meridian specific activation cis-acting elements
ERE 1 乙烯响应元件 Ethylene responsive element
GC-motif 1 缺氧特异性诱导元件 Hypoxia specific induction element
LTR 3 低温响应元件 Low temperature responsive elements
STRE 5 热休克、营养饥饿和低pH诱导响应元件
Response elements induced by heat shock, nutritional starvation and low pH
TATC-box 1 环境响应和抗性相关元件 Environmental response and resistance related elements
TCA-element 2 水杨酸反应涉及的顺式作用元件 Cis-acting elements involved in salicylic acid reaction
TGACG-motif 1 MeJA反应的顺式作用元件 Cis-acting element of MeJA reaction
WRE3 1 损伤诱导元件 Damage inducing element

Fig. 4

Phylogenetic and interaction network of TaUBC16 protein A: phylogenetic analysis of the SPP proteins from wheat and other plants. Ta: Triticum aestivum; Zm: Zea mays; Os: Oryza sativa; At: Arabidopsis thaliana; Tu: Triticum urartu; Sl: Solanum lycopersicum; As: Aegilops speltoides; Nt: Nicotiana tabacum; Gm: Glycine max; St: Solanum tuberosum; Bd: Brachypodium distachyon; Hv: Hordeum vulgare. B: TaUBC16 protein interaction network."

Fig. 5

Relative expression pattern of TaUBC16 gene at different developmental stage in wheat A: relative expression heatmap of TaUBC16 gene in different growth stages and different tissues/organs of Chinese Spring. B: relative expression pattern of TaUBC16 in different tissues of wheat. C: relative expression pattern of TaUBC16 in grains of wheat. D: relative expression pattern of TaUBC16 in different tissues of wheat grains. The error bar represents mean ± SD."

Fig. 6

Relative expression pattern of TaUBC16 gene in wheat seedling under different abiotic stress treatments A: relative expression heatmap of TaUBC16 gene under different abiotic stresses in Chinese spring. B: 200 mmol L-1 NaCl treatment. C: 20% PEG-6000 treatment. D: 200 mmol L-1 mannitol treatment. E: 100 μmol L-1 ABA treatment. Error bar represents mean ± SD. *: P < 0.05; **: P < 0.01."

Fig. 7

Nucleotide polymorphisms and development of KASP markers for TaUBC16 A: schematic diagram of TaUBC16 gene structure and SNPs existed in two TaUBC16 haplotypes. B: KASP assays for SNP-388 bp in the accessions in TaUBC16. The blue circles represent accessions that have the FAM-type allele and the red circles represent the HEX-type allele; the black squares are the non-template control. Allele ‘A’ in FAM and ‘T’ in HEX cluster."

Fig.8

Association analysis, spatial and temporal distribution of TaUBC16 haplotype A, B, C: association analysis of TaUBC16 allelic variation and yield-related traits in five environments. E1-E3 indicates Tongwei farm station, Gansu, China in 2020, 2021, and 2022; E4-E5 indicates Zhuanglang farm station, Gansu, China in 2022 and 2023. D: geographic distribution of varieties with TaUBC16 haplotypes in China. Chinese standard map: Map approval number GS (2022) 4310, with no modifications of the map boundaries. E: frequencies of TaUBC16 allelic variation in Chinese wheat breeding programs in different decades. The presence of asterisk denotes significant difference between means (* P < 0.05; ** P < 0.01). Error bar: ±SE. Different colors represent different haplotypes."

Fig. 9

Identification of TaUBC16 heterologous expression in Arabidopsis A: Identification of TaUBC16 heterologous expression in Arabidopsis. L1-L6: Line 1-6; WT: wild type; P: plasmids. B: RT-PCR was used to determine the relative expression level of TaUBC16 in transgenic Arabidopsis."

Fig. 10

Observation of phenotype between WT and TaUBC16 transgenic lines of Arabidopsis A: representative photographs of wild-type (WT) and transgenic lines. B: flowering time (the total rosette leaf number) of WT and transgenic lines. Rosette leaf numbers were counted after bolting. C: representative siliques of WT and transgenic lines. D: silique length of WT and transgenic lines. E: plant height of WT and transgenic lines, bar: 5 cm. F: statistics of plant height of WT and transgenic lines. G: representative grain morphology of WT and transgenic lines, bar: 100 μm. H: statistics of TKW of WT and transgenic lines. * and ** denote significant differences in WT at the 0.05 and 0.01 probability levels by Student’s tests, respectively."

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