谷子SiPRR37基因对光温、非生物胁迫的响应特点及其有利等位变异鉴定

doi:10.3724/SP.J.1006.2021.04139

Abstract

Abstract:

In this study, the clock gene SiPRR37 was cloned from the foxtail millet variety Yangu 11, and bioinformatics analysis, tissue specific expression analysis, diurnal expression patterns analysis under four different photo-thermal combinational conditions and responsive characteristics analysis to five abiotic stresses such as NaCl, ABA, PEG, low temperature and Fe were performed to reveal the mechanisms that SiPRR37 participated in regulating of photo-thermal interaction and coped with abiotic stresses. Mutation sites of SiPRR37 were detected by re-sequencing of 160 millet materials, which were used for haplotype analysis to explore the effect of SiPRR37 on main agronomic traits. The results showed that the CDS length of SiPRR37 gene was 2247 bp, which encoded 748 amino acids and contained REC and CCT domains. The phylogenetic analysis based on PRR37 proteins showed that foxtail millet had the closest relationship with broomcorn millet, sorghum and maize. Promoter prediction analysis found that various responsive elements to light, temperature, auxin, GA, ABA, MeJA, drought and salt stresses were detected in promoter region of SiPRR37. The decreasing order of relative expression level of SiPRR37 was root, panicle neck, panicle, parietal leaf, secondary parietal leaf and stem. Under four photo-thermal combinational conditions, SiPRR37 gave only one expression peak during the light period, and regardless of high temperature (27℃) or low temperature (22℃), the expression peak advanced under short-day condition compared to long-day condition, regardless of long-day or short-day, the expression peak advanced at low temperature (22℃) compared to high temperature (27℃). The expression of SiPRR37 was inhibited by NaCl and low temperature (15℃) stresses, induced by PEG-simulated drought stress and Fe stress. SiPRR37 participated in ABA signaling transduction process. The 10 SNPs in CDS region of SiPRR37 divided 160 millet materials into 19 haplotypes, of which Hap_7, Hap_10 and Hap_19 were favorable haplotypes for improving panicle traits. SiPRR37 exhibited circadian expression, and was regulated by photoperiod and temperature simultaneously. SiPRR37 participated in the responses of foxtail millet to salt stress, low temperature stress, drought stress and Fe stress. At the same time, SiPRR37 was correlated with heading stage and multiple panicle traits, showing certain application potential in high-yield molecular-assisted breeding of foxtail millet.

Key words: foxtail millet, SiPRR37, photo-thermal combinations, abiotic stress, expression analysis, haplotype

JIA Xiao-Ping, LI Jian-Feng, ZHANG Bo, QUAN Jian-Zhang, WANG Yong-Fang, ZHAO Yuan, ZHANG Xiao-Mei, WANG Zhen-Shan, SANG Lu-Man, DONG Zhi-Ping. Responsive features of SiPRR37 to photoperiod and temperature, abiotic stress and identification of its favourable allelic variations in foxtail millet (Setaria italica L.)[J].Acta Agronomica Sinica, 2021, 47(4): 638-649.

Figures/Tables 15

Table S1

160 foxtail millet resources used in this study"

序号 Serial number	国家统一编号 National unified number	品种名 Variety name	来源地 Origin region
1	00027956	郑谷2 Zhenggu 2	中国河南 Henan, China
2	00027954	豫谷6 Yugu 6	中国河南 Henan, China
3	00024231	郑06-6 Zheng 06-6	中国河南 Henan, China
4	00024221	豫谷3 Yugu3	中国河南 Henan, China
5	00027933	郑05-2 Zheng 05-2	中国河南 Henan, China
6	00024226	郑州12 Zhengzhou 12	中国河南 Henan, China
7	00024231	郑315 Zheng 315	中国河南 Henan, China
8	00024262	郑8041 Zheng 8041	中国河南 Henan, China
9	00024195	安5424 An 5424	中国河南 Henan, China
10	00027946	豫谷15 Yugu 15	中国河南 Henan, China
11	00027948	豫谷11 Yugu 11	中国河南 Henan, China
12	00028386	豫谷16 Yugu 16	中国河南 Henan, China
13	00027937	安4117 An 4117	中国河南 Henan, China
14	00027952	豫谷13号Yugu 13	中国河南 Henan, China
15	00028387	豫谷18号Yugu 18	中国河南 Henan, China
16	00027937	安04-5014 An 04-5014	中国河南Henan, China
17	00024170	豫谷2号Yugu2	中国河南 Henan, China
18	00010182	十里香Shilixiang	中国河南 Henan, China
19	00007844	毛毛亮Maomaoliang	中国河南 Henan, China
20	00020503	大黄糯谷Dahuangnuogu	中国河南 Henan, China
21	00027920	冀谷27 Jigu 27	中国河北 Hebei, China
22	00027921	冀谷28 Jigu 28	中国河北 Hebei, China
23	00027925	冀谷17 Jigu 17	中国河北 Hebei, China
24	00027919	金谷1号Jingu 1	中国河北 Hebei, China
25		冀特5号Jite 5	中国河北 Hebei, China
26	00027910	冀谷24 Jigu 24	中国河北 Hebei, China
27	00027909	冀谷22 Jigu 22	中国河北 Hebei, China
28	00027907	冀谷18 Jigu 18	中国河北 Hebei, China
29	00027906	冀谷31 Jigu 31	中国河北 Hebei, China
30	00027905	复12 Fu 12	中国河北 Hebei, China
31	00027924	冀谷15 Jigu 15	中国河北 Hebei, China
32	00027912	冀谷29 Jigu 29	中国河北 Hebei, China
33	00027911	冀谷26 Jigu 26	中国河北 Hebei, China
34	00027922	冀谷30 Jigu 30	中国河北 Hebei, China
35	00027733	谷丰1号Gufeng 1	中国河北 Hebei, China
36		532
37	00007619	张农8 Zhangnong 8	中国河北 Hebei, China
38	00022106	坝谷6 Bagu 6	中国河北 Hebei, China
39	00022109	坝谷81 Bagu 81	中国河北 Hebei, China
40	00022123	坝谷210 Bagu 210	中国河北 Hebei, China
41	00022173	坝91-0130 Ba 91-0130	中国河北 Hebei, China
42	00022116	坝谷139 Bagu 139	中国河北 Hebei, China
43	00022162	坝91-0053 Ba 91-0053	中国河北 Hebei, China
44	00022166	坝91-0079 Ba 91-0079	中国河北 Hebei, China
45	00007036	毛毛谷Maomaogu	中国河北 Hebei, China
46	00007040	沙粒滚Shaligun	中国河北 Hebei, China
47	00019241	大九根齐Dajiugenqi	中国河北 Hebei, China
48	00022090	矮41 Ai 41	中国河北 Hebei, China
49	000027926	衡谷9号Henggu 9	中国河北 Hebei, China
50	00022052	毛谷2号Maogu 2	中国河北 Hebei, China
51	00022608	南育3号Nanyu 3	中国河北 Hebei, China
52	00027898	承谷11 Chenggu 11	中国河北 Hebei, China
53	00028046	矮88 Ai 88	中国河北 Hebei, China
54	00012329	小青谷Xiaoqinggu	中国河北 Hebei, China
55	00012587	黄毛谷Huangmaogu	中国河北 Hebei, China
56	00022881	齐头白Qitoubai	中国河北 Hebei, China
57	00022525	老绳头Laoshengtou	中国河北 Hebei, China
58	00008960	龙爪谷Longzhuagu	中国河北 Hebei, China
59	00008461	小白苗Xiaobaimiao	中国河北 Hebei, China
60	00007568	黑色腰Heiseyao	中国河北 Hebei, China
61	00024082	济叶冲4 Jiyechong 4	中国山东Shandong, China
62	00019597	鲁谷3号Lugu 3	中国山东Shandong, China
63	00023553	早白糯Zaobainuo	中国山东Shandong, China
64	00012887	钱串子Qianchuanzi	中国山东Shandong, China
65	00014233	拔谷Bagu	中国山东Shandong, China
66	00012877	红根子谷Honggenzigu	中国山东Shandong, China
67	00011078	早谷Zaogu	中国山东Shandong, China
68	00006337	晋汾13 Jinfen 13	中国山西Shanxi, China
69	00027993	晋谷35号Jingu 35	中国山西Shanxi, China
70	00027995	汾选5号Fenxuan 5	中国山西Shanxi, China
71	00018008	皇龙谷Huanglonggu	中国山西Shanxi, China
72	00017042	红腿谷Hongtuigu	中国山西Shanxi, China
73	00024502	大同黄Datonghuang	中国山西Shanxi, China
74	00020590	龙谷26 Longgu 26	中国黑龙江Heilongjiang, China
75	00027854	白谷9号Baigu 9	中国吉林Jilin, China
76	00027862	公谷66号Gonggu 66	中国吉林Jilin, China
77	00027699	公谷69号Gonggu 69	中国吉林Jilin, China
78	00027704	公矮3号Gong’ai 3	中国吉林Jilin, China
79	00000785	白杆白沙Baiganbaisha	中国吉林Jilin, China
80	00000077	糟皮一把奇Zaopiyibaqi	中国黑龙江Heilongjiang, China
81	00015441	龙爪粘Longzhuanian	中国黑龙江Heilongjiang, China
82	00015445	安丰Anfeng	中国黑龙江Heilongjiang, China
83	00000011	老来变Laolaibian	中国黑龙江Heilongjiang, China
84	00027903	06-766	中国北京 Beijing, China
85	00012037	小早谷Xiaozaogu	中国北京Beijing, China
86	00018398	红杆谷Honggangu	中国陕西Shaanxi, China
87	00026203	呼和浩特大毛谷Huhehaotedamaogu	中国陕西Shaanxi, China
88	00028011	延谷11号Yangu 11	中国陕西Shaanxi, China
89		11郄1071 11qie1071
90	00014610	米泉谷Miquangu	中国新疆Xinjiang, China
91	00014612	沙湾谷子Shawanguzi	中国新疆Xinjiang, China
92	00018817	谷子Guzi	中国新疆Xinjiang, China
93	00018811	谷子Guzi	中国新疆Xinjiang, China
94	00021709	谷上谷Gushanggu	中国甘肃 Gansu, China
95	00028014	陇谷11号Longgu 11	中国甘肃Gansu, China
96	00027972	塞外香谷子Saiwaixiangguzi	中国宁夏Ningxia, China
97	00021671	红燃谷Hongrangu	中国宁夏Ningxia, China
98	00018751	小苗谷Xiaomiaogu	中国宁夏Ningxia, China
99	00003251	大青苗鱼刺Daqingmiaoyuci	中国甘肃Gansu, China
100	00018675	尕红谷Gahonggu	中国甘肃Gansu, China
101	00002910	黄玉3 Huangyu 3	中国内蒙古 Inner Mongolia, China
102	00003005	籼紫灰谷Xianzihuigu	中国内蒙古Inner Mongolia, China
103	00003008	二白谷Erbaigu	中国内蒙古Inner Mongolia, China
104	00022053	蒜皮白Suanpibai	中国内蒙古Inner Mongolia, China
105	00015547	金香玉Jinxiangyu	中国内蒙古Inner Mongolia, China
106	00014740	朝鲜谷子Chaoxianguzi	朝鲜Korea
107	00015037	SET3/80	德国Germany
108	00015049	ISE-430	美国 America
109	00014718	大王国Dawangguo	日本Japan
110	00014938	ISE-245	印度 India
111	00015012	法谷28-81 Fagu 28-81	法国 France
112	00014729	骨绿早1 Gulyuzao 1	朝鲜DPRK
113	00022367	ISE 770	国际半干旱研究所ICRISAT
114	00022370	ISE 775	国际半干旱研究所ICRISAT
115	00014697	岛原Daoyuan	日本Japan
116	00014706	六十日Liushiri	日本Japan
117	00015402	金德Jinde	美国America
118	00022430	Red manna	南非South Africa
119	00026837	K-3606	俄罗斯Russia
120	00014949	Ise-455	美国America
121	00015029	Set 64/82	德国Germany
122	00027931	8322-14
123	00027915	白米1号Baimi 1	中国辽宁 Liaoning, China
124	00027927	2013
125	0027917	谷丰2号Gufeng 2	中国河北Hebei, China
126	00015128	芝麻粟Zhimasu
127	00014623	大头糯Datounuo	中国湖南 Hunan, China
128	00022285	乐山白糯Leshanbainuo	中国四川 Sichuan, China
129	00022313	黄谷Huanggu	中国西藏 Tibet, China
130	00026488	黄粟Huangsu	中国广西 Guangxi, China
131	00025646	黄谷子Huangguzi	中国青海Qinghai, China
132	00025962	喇叭黄Labahuang	中国青海Qinghai, China
133		15HN-206	中国河北Hebei, China
134		15HN-138	中国河北Hebei, China
135		15HN-79	中国河北Hebei, China
136		六十天还家 Liushitianhuanjia	中国吉林Jilin, China
137		谷子Guzi	中国青海Qinghai, China
138		红糯谷Hongnuogu	中国宁夏Ningxia, China
139		小明谷子Xiaomingguzi	中国甘肃Gansu, China
140		粘子糯Nianzinuo
141		毛粟Maosu
142	00018651	茄谷Qiegu	中国甘肃Gansu, China
143		然谷Rangu	中国陕西Shaanxi, China
144		铁谷4号Tiegu 4	中国辽宁 Liaoning, China
145		红苗2 Hongmiao 2	中国吉林Jilin, China
146		叩根Kougen	中国吉林Jilin, China
147	00021176	铁7924 Tie 7924	中国辽宁 Liaoning, China
148	00020837	小金苗Xiaojinmiao	中国吉林Jilin, China
149	00015437	嫩选十号Nenxuanshi	中国黑龙江Heilongjiang, China
150	00028013	陇谷10号Longgu 10	中国甘肃Gansu, China
151	00027871	辽谷1号Liaogu 1	中国辽宁 Liaoning, China
152	00027852	嫩选十六Nenxuanshiliu	中国黑龙江Heilongjiang, China
153	00027882	蒙早谷9号Mengzaogu 9	中国内蒙古Inner Mongolia, China
154		红钙谷Honggaigu	中国天津Tianjin, China
155	00007028	黑谷子Heiguzi	中国河北Hebei, China
156	00021303	赤谷6号Chigu 6	中国内蒙古Inner Mongolia, China
157		二不黄Erbuhuang	中国山西Shanxi, China
158		白罗砂Bailuosha	中国河北Hebei, China
159		竹叶青Zhuyeqing	中国河北Hebei, China
160		压塌车Yatache	中国河北Hebei, China

Table S1

Table 1

Fig. 1

Fig. 2

Fig. S1

Fig. 3

Fig. S2

Fig. 4

Fig. 5

Table 2

Fig. 6

Fig. 7

Table 3

Table S2

Distribution of haplotypes of the coding region of SiPRR37 gene in 160 millet varieties"

单倍型 Haplotype	个数 Number	品种 Variety
Hap_1	84	郑谷2, 豫谷6, 郑06-6, 郑05-2, 郑州12, 郑315, 安5424, 豫谷11, 豫谷16, 安4117, 豫谷13号, 安04-5014,大黄糯谷, 冀谷27, 冀谷28, 冀谷17, 金谷1号, 冀谷24, 冀谷22, 冀谷18, 冀谷31, 复12, 冀谷15, 冀谷29号, 冀谷26号, 冀谷30, 谷丰1号, 532, 坝91-0130, 坝91-0053, 大九根齐, 矮41, 衡谷9号, 南育3号, 承谷11, 矮88, 黄毛谷, 齐头白, 老绳头, 济叶冲4, 早白糯, 钱串子, 拔谷, 红根子谷, 晋谷35号, 皇龙谷, 龙谷26, 白谷9号, 公谷66号, 公谷69号, 公矮3号, 白杆白沙, 安丰, 老来变, 06-766, 延谷11号, 黄玉3, 金香玉, ISE-430, 大王国, ISE-245, 骨绿早1, ISE775, 岛原, 六十日, 金德, Set64/82, 8322-14, 白米1号, 2013, 芝麻粟, 大头糯, 乐山白糯, 黄谷, 喇叭黄, 15HN-138, 然谷, 红苗2, 铁7924, 小金苗, 嫩选十六, 黑谷子, 赤谷6号, 压塌车 Zhenggu 2, Yugu 6, Zheng 06-6, Zheng 05-2, Zhengzhou 12, Zheng 315, An 5424, Yugu 11, Yugu 16, An 4117, Yugu 13, An 04-5014, Dahuangnuogu, Jigu 27, Jigu 28, Jigu 17, Jingu 1, Jigu 24, Jigu 22, Jigu 18, Jigu 31, Fu 12, Jigu 15, Jigu 29, Jigu 26, Jigu 30, Gufeng 1, 532, Ba 91-0130, Ba 91-0053, Dajiugenqi, Ai 41, Henggu 9, Nanyu 3, Chenggu 11, Ai 88, Huangmaogu, Qitoubai, Laoshengtou, Jiyechong 4, Zaobainuo, Qianchuanzi, Bagu, Honggenzigu, Jingu 35, Huanglonggu, Longgu 26, Baigu 9, Gonggu 66, Gonggu 69, Gong’ai 3, Baiganbaisha, Anfeng, Laolaibian, 06-766, Yangu 11, Huangyu 3, Jinxiangyu, ISE-430, Dawangguo, ISE-245, Gulyzao 1, ISE775, Daoyuan, Liushiri, Jinde, Set64/82, 8322-14, Baimi1, 2013, Zhimasu, Datounuo, Leshanbainuo, Huanggu, Labahuang, 15HN-138, Rangu, Hongmiao 2, Tie7924, Xiaojinmiao, Nenxuanshiliu, Heiguzi, Chigu 6, Yatache
Hap_2	2	豫谷3号, 鲁谷3号 Yugu 3, Lugu 3
Hap_3	1	郑8041 Zheng 8041
Hap_4	1	豫谷15 Yugu 15
Hap_5	2	豫谷18号, 沙粒滚 Yugu 18, Shaligun
Hap_6	48	豫谷2号, 十里香, 坝谷6, 坝谷81, 坝谷210, 坝91-0079, 毛毛谷, 毛谷2号, 小青谷, 龙爪谷, 黑色腰, 早谷,晋汾13, 汾选5号, 红腿谷, 龙爪粘, 红杆谷, 呼和浩特大毛谷, 11郄1071, 米泉谷, 谷上谷, 塞外香谷子, 红燃谷, 小苗谷, 大青苗鱼刺, 尕红谷, 籼紫灰谷, 二白谷, Red manna, Ise-455, 黄粟, 黄谷子, 15HN-206, 15HN-79,六十天还家, 谷子, 红糯谷, 毛粟, 茄谷, 铁谷4号, 嫩选十号, 陇谷10号, 辽谷1号, 蒙早谷9号, 红钙谷, 二不黄, 白罗砂, 竹叶青 Yugu 2, Shilixiang, Bagu 6, Bagu 81, Bagu 210, Ba 91-0079, Maomaogu, Maogu 2, Xiaoqinggu, Longzhuagu, Heiseyao, Zaogu, Jinfen 13, Fenxuan 5, Hongtuigu, Longzhuanian, Honggangu, Huhehaotedamaogu, 11qie1071, Miquangu, Gushanggu, Saiwaixiangguzi, Hongrangu, Xiaomiaogu, Daqingmiaoyuci, Gahonggu, Xianzihuigu, Erbaigu, Red manna, Ise-455, Huangsu, Huangguzi, 15HN-206, 15HN-79, Liushitianhuanjia, Guzi, Hongnuogu, Maosu, Qiegu, Tiegu 4, Nenxuanshi, Longgu 10, Liaogu1, Mengzaogu 9, Honggaigu, Erbuhuang, Bailuosha, Zhuyeqing
Hap_7	2	毛毛亮, 陇谷11号 Maomaoliang, Longgu 11
Hap_8	1	冀特5号 Jite 5
Hap_9	3	张农8, 谷子, 蒜皮白 Zhangnong8, Guzi, Suanpibai
Hap_10	1	坝谷139 Bagu 139
Hap_11	2	小白苗, K-3606 Xiaobaimiao, K-3606
Hap_12	1	大同黄 Datonghuang
Hap_13	3	糟皮一把奇, 朝鲜谷子, SET3/80 Zaopiyibaqi, Chaoxianguzi, SET3/80
Hap_14	2	小早谷, 谷子 Xiaozaogu, Guzi
Hap_15	2	沙湾谷子, 谷丰2号 Shawanguzi, Gufeng 2
Hap_16	2	法谷28-81, 叩根 Fagu 28-81, Kougen
Hap_17	1	ISE770 ISE770
Hap_18	1	小明谷子 Xiaomingguzi
Hap_19	1	粘子糯 Nianzinuo

Table S2

Fig. 8

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引物名称 Primer name	引物序列 Primer sequences (5°-3°)	预期片段大小 Expected fragment size (bp)	用途 Purpose
PRR37-1	F: TGACAACGACGAGGACG R: CGTTAGCAATCTCCGTGT	1295	克隆SiPRR37 Cloning SiPRR37
PRR37-2	F: CCATTTGCTGACTCGCCTAC R: TCCTGTCCCGCCTTGAT	1586
PRR37-3	F: AAGGCTCCAATGGCAGTAG R: GAACCAGCGAAGGAAGAATC	1267
SiActin	F: GGCAAACAGGGAGAAGATGA R: GAGGTTGTCGGTAAGGTCACG	229	内参荧光定量 Internal reference fluorescence quantification
RtPRR37	F: CACCACTTTCGTCTACCTCTT R: CTGGCATCTCTTCTAACGG	91	SiPRR37荧光定量 SiPRR37 fluorescence quantification

调控元件 Regulatory element	核心序列 Core sequence	数目 Number	分布区域 Distribution region (bp)	功能 Function
LTR	CCGAAA	1	658-663	参与低温响应顺式激活元件 cis-acting element involved in low-temperature responsiveness
G-box	CACGTG, TCCACATGGCA, CACGAC	4	123-128, 1870-1879, 1103-1108, 1517-1522	参与光响应顺式作用元件 cis-acting regulatory element involved in light responsiveness
AE-box	AGAAACTT	1	409-416	部分光响应元件 Part of a light responsive element
Box II	CCACGTGGC	1	122-130	部分光响应元件 Part of a light responsive element
Sp1	GGGCGG	1	23-28	光响应元件 Light responsive element
3-AF1 binding site	TAAGAGAGGAA	1	1045-1054	光响应元件 Light responsive element
AuxRR-core	GGTCCAT	1	1536-1542	参与生长素响应顺式作用元件 cis-acting regulatory element involved in auxin responsiveness
TGACG-motif	TGACG, CGTCA	2	29-33, 1563-1567	参与茉莉酸甲酯响应的顺式激活元件 cis-acting regulatory element involved in the MeJA- responsiveness
TATC-box	TATCCCA	1	925-931	参与赤霉素响应顺式激活元件 cis-acting element involved in gibberellin-responsiveness
P-box	CCTTTTG	1	1726-1732	赤霉素响应元件 Gibberellin-responsive element
Myb-binding site	CAACAG	1	1154-1159	参与干旱、盐胁迫等逆境响应 Involved in drought, salt dresses responsiveness
DRE1	ACCGAGA	1	342-348	干旱胁迫响应元件
ABRE	ACGTG, CACGTG	2	31-35, 123-128	参与ABA响应的顺式激活元件 cis-acting element involved in the abscisic acid responsiveness

参数 Parameter	5°非翻译区 5° UTR	外显子区 Exon region	内含子区 Intron region	3°非翻译区 3° UTR	全长 Full length
序列长度Sequence length (bp)	978	2247	10,440	678	14,343
SNP数目 Number of SNPs	6	10	31	0	47
SNP频率SNP frequency (bp SNP^-1)	163	224.7	336.77	0	305.17

Responsive features of SiPRR37 to photoperiod and temperature, abiotic stress and identification of its favourable allelic variations in foxtail millet (Setaria italica L.)

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