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作物学报 ›› 2022, Vol. 48 ›› Issue (4): 873-885.doi: 10.3724/SP.J.1006.2022.14043

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

谷子叶绿体基因RNA编辑位点的鉴定与分析

杜晓芬(), 王智兰, 韩康妮, 连世超, 李禹欣, 张林义, 王军*()   

  1. 山西农业大学谷子研究所 / 杂粮种质创新与分子育种山西省重点实验室 / 杂粮种质资源发掘与遗传改良山西省重点实验室, 山西长治 046011
  • 收稿日期:2021-03-15 接受日期:2021-07-12 出版日期:2022-04-12 网络出版日期:2021-07-24
  • 通讯作者: 王军
  • 作者简介:杜晓芬, E-mail: dxf6285210@126.com第一联系人：**同等贡献
  • 基金资助:
    山西省农业科学院国家自然科学基金培育项目(YGJPY1906);山西省自然基金面上项目(201901D1114545);山西省青年基金面上项目(201901D211556);山西省农业科学院农业科技创新研究课题(YCX2020YQ35);山西省农业科学院杂粮分子育种平台专项资助(YGC2019FZ3)

Identification and analysis of RNA editing sites of chloroplast genes in foxtail millet [Setaria italica (L.) P. Beauv.]

DU Xiao-Fen(), WANG Zhi-Lan, HAN Kang-Ni, LIAN Shi-Chao, LI Yu-Xin, ZHANG Lin-Yi, WANG Jun*()   

  1. Millet Research Institute of Shanxi Agricultural University / Shanxi Key Laboratory of Minor Crop Germplasm Innovation and Molecular Breeding / Shanxi Key Laboratory of Genetic Resources and Breeding in Minor Crops, Changzhi 046011, Shanxi, China
  • Received:2021-03-15 Accepted:2021-07-12 Published:2022-04-12 Published online:2021-07-24
  • Contact: WANG Jun
  • About author:First author contact:**Contributed equally to this work
  • Supported by:
    Natural Science Foundation Cultivation Project of Shanxi Academy of Agricultural Sciences(YGJPY1906);Shanxi Province Science Fund(201901D1114545);Shanxi Province Youth Fund(201901D211556);Agricultural Science and Technology Innovation Research Project of Shanxi Academy of Agricultural Sciences(YCX2020YQ35);Minor Crop Molecular Breeding Platform Special Project of Shanxi Academy of Agricultural Sciences(YGC2019FZ3)

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摘要：

RNA编辑是高等植物叶绿体基因转录后加工修饰的现象, 它会影响叶绿体发育, 导致植株叶片出现黄化或白化等表型。本研究以长农35号及其2份叶色突变体(E752和E1005)为试验材料, 利用紫外分光光度计测定了苗期叶绿素含量, 通过透射电镜观察了叶绿体结构; 利用在线工具Prep-Cp对谷子叶绿体基因RNA编辑位点进行了预测, 通过PCR、RT-PCR及测序等方法对预测到的编辑位点进行了验证, 并与其他单子叶作物的编辑位点进行了比较分析; 进一步利用荧光实时定量方法, 分析rpoB及依赖PEP转录的光合途径相关基因(ndhG、psaA、psbA和rbcL)在不同发育时期的表达水平; 最后, 利用生物信息学分析ropB编辑前后蛋白二级结构的变化。结果表明, 与长农35号相比, 2份叶色突变体叶绿素含量显著降低, 叶绿体发育异常; 在谷子中, 有10个叶绿体基因共计20个位点发生RNA编辑, 所有编辑位点均为胞嘧啶(C)和尿嘧啶(U)的转换, 不同基因的编辑位点存在数量差异, 其中ndhB编辑位点数量最多, 共计6个; 20个编辑位点中, 有19个位点在物种进化上具有较高保守性, 只有rpoC1-2753为谷子中特有的编辑位点; 在长农35号及其2份叶色突变体中, rpoB的3个编辑位点(rpoB-467、rpoB-545和rpoB-560)存在编辑效率差异, 而这种编辑效率的改变导致rpoB表达水平改变, 进一步可能影响了ndhG、psaA、psbA和rbcL表达水平的变化; 生物信息学分析表明, rpoB-467和rpoB-560编辑前后影响了蛋白二级结构。研究结果为解析叶绿体RNA编辑参与谷子叶绿体发育的分子机制奠定了一定基础。

关键词: 谷子, 叶绿体, RNA编辑, 突变体

Abstract:

RNA editing is one of the post-transcriptional regulation mechanisms of gene expression in the chloroplast genomes of higher plants, which affects the chloroplast development and leads to albino phenotype or yellow phenotype of plant leaves. In this study, chlorophyll content was measured with a UV spectrophotometer at seeding stage among Changnong 35, E752, and E1005, and chloroplast structure of leaves was observed with a transmission electron microscopy; the online tool Prep-CP was used to predict the RNA editing sites of chloroplast genes; RNA editing site was verified by PCR, RT-PCR, and sequencing method, and the editing sites were compared and analyzed between foxtail millet and other monocotyledon. Furthermore, the relative expression patterns of rpoB and PEP-transcription-dependent photosynthetic pathway related genes (ndhG, psaA, psbA, and rbcL) were analyzed by qRT-PCR at different developmental stages, and the secondary structure of rpoB protein before and after editing was analyzed by bioinformatics. The results showed that chlorophyll content of E752 and E1005 were significantly lower and their chloroplasts were abnormal compared with Changnong 35. A total of 20 RNA editing sites of 10 chloroplast genes were identified, among which all were C to U conversion; the number of editing sites among chloroplast genes was varied, and ndhB had the most editing sites with the number of 6. Among the 20 editing sites, 19 editing sites were highly conserved in the evolution of species, however rpoC1-2753 was a unique editing site in foxtail millet. The editing efficiency of rpoB-467, rpoB-545, and rpoB-560 was distinctly different from those of the other editing sites among Changnong 35, E752, and E1005, leading to the expression level change of ropB, which might further affect the expression levels changes of ndhG, psaA, psbA, and rbcL. Bioinformatics analysis revealed that secondary structure of rpoB protein was changed due to the RNA editing of rpoB-467 and rpoB-560. Our results laid a foundation for the molecular mechanism analysis of chloroplast RNA editing in chloroplast development of foxtail millet.

Key words: foxtail millet, chloroplast, RNA editing, mutant

表1

引物信息"

引物名称
Marker name		 引物序列
Sequence (5'-3')		 产物大小
Product size (bp)		 引物名称
Marker name		 引物序列
Sequence (5'-3')		 产物大小
Product size (bp)
atpA-F1 TCGCTTAATTGAATCTCCTG 946 rpoB-F1 ATCAGGGCTTGGCAGAAGA 875
atpA-R1 CGTTCCGGTATAAATGGTAG rpoB-R1 ATCCGCAACCGAACGAATA
ccsA-F1 TCTTAGTTTCTCGTTGGGTTTC 641 rpoC1-F1 AGGACGACTCAGAAGAAGAAT 1042
ccsA-R1 TGCAAATATGGTCCAGGTAAT rpoC1-R1 GAACAGTTGGATGCCGAC
matK-F1 GAGGGGTATTCAGAAAAACA 918 rps8-F1 ATGGGCAAGGACACTATTG 404
matK-R1 TTGTGAGAAATTGACAAGGTAA rps8-R1 ATATAACATAAGACTTCTCCCC
matK-F2 CACTTTTCTGGGAAGATGGA 780 rps14-F1 AAAAGTTTGATTCAGAGGGAG 302
matK-F2 CACCAGGTCATTGATACGG rps14-R1 TACCAACTGGATCTTGTTGC
ndhA-F1 ATGGATTCTACCCATTTTGAC 982 ycf3-F1 CTAGATCCCGTATAAATGGAA 498
ndhA-R1 TGTTAATAAGAGATTGCCCAG ycf3-R1 GCTTCGTAATCTTCAACCAGT
ndhB-F1 TTTATGTGGTGCTAACGATT 1073 ndhG-Real-Time-F GCCTTTTCGCTGGGATTAG 155
ndhB-R1 GGTTCATTGATATTCCTGGT ndhG-Real-Time-R GACCACTCTGAGCCGTTTACA
ndhD-F1 ACTTGTTGTTTTGCCGATAT 759 psaA-Real-Time-F TTTCTTAGGCGCTCATTTTGTC 151
ndhD-R1 ATCAATCCGTATGCTCCC psaA-Real-Time-R TATAATGCTCAAGGCTCTAGGC
ndhF-F1 TAATCCCTCTTCTCCCACTT 1132 psbA-Real-Time-F TTATGATTGTATTCCAGGCGGA 154
ndhF-R1 AAACCACCCATAAGAACCAT psbA-Real-Time-R GCAGACTCATTTTCAGTGGTTT
ndhF-F2 TGATCACTCATGCTTATTCGA 1010 rbcL-Real-Time-F CCGAAATCTTTGGAGACGATTC 105
ndhF-R2 ACCAGCAAGACCTACTCCAT rbcL-Real-Time-R CTTCTAAAGCCACACGATTAGC
petB-F1 ATGAGTATGAAATTTTCATATAC 689 rpoB-Real-Time-F AAACGTATTCGTTCGGTTGC 135
petB-R1 ATACCTTGCTTACGTATCA rpoB-Real-Time-R TACCAAAGTTTGTGGAGTCGG
rpl20-F1 AGAGTTCCGCGAGGATAT 325 SiActin-7-F TGATCTCACTGACAGTCTGATG 88
rpl20-R1 TCGTGTAAAGATTATTTGGATT SiActin-7-R GATGTCTCTTACAATTTCCCGC

图1

长农35号和突变体苗期表型及叶绿体超微结构 A~C: 长农35号; D~F: E1005; G~I: E752; GL: 基粒片层; SG: 淀粉粒; OP: 嗜饿体。"

表2

长农35号和叶色突变体苗期叶片色素含量比较"

材料
Material name		 总叶绿素含量
Total chlorophyll		 叶绿素a
Chlorophyll a		 叶绿素b
Chlorophyll b		 类胡萝卜素
Carotenoid
长农35号 Changnong 35 2.12±0.060 1.68±0.019 0.45±0.004 0.69±0.016
E752 1.55±0.050** 1.28±0.072* 0.27±0.031** 0.36±0.010**
E1005 0.99±0.017** 0.76±0.018** 0.24±0.002** 0.34±0.008**

表3

谷子叶绿体基因RNA编辑位点预测、验证及长农35号与E752和E1005编辑位点的比较"

基因
Gene ID		 密码子位置
Codon position		 密码子变化
Codon conversion		 氨基酸转变
Amino acid conversion		 长农35号
Changnong 35		 E752 E1005
atpA 1148 uCa→uUa S→L + + +
ccsA 641 aCu→aUu T→I - - -
matK 331 Cuu→Tuu L→F - - -
1258 Cau→Uau H→Y - - -
ndhA 47 uCg→uUg S→L + + +
470 uCa→uUa S→L + + +
560 uCa→uUa S→L + + +
ndhB 467 cCa→cUa P→L + + +
586 Cau→Uau H→Y + + +
611 uCa→uUa S→L + + +
737 cCa→cUa P→L + + +
830 uCa→uUa S→L + + +
1481 cCa→cUa P→L + + +
ndhD 878 uCa→uUa S→L + + +
ndhF 62 uCa→uUa S→L - - -
1834 Cuu→Tuu L→F - - -
1909 Cuu→Tuu L→F - - -
petB 668 cCa→cUa P→L - - -
rpl20 308 uCa→uUa S→L + + +
rpoB* 467 uCa→uUa S→L +/- +/- +/-
545 uCa→uUa S→L +/- +/- +/-
560 uCa→uUa S→L +/- +/- +/-
617 cCa→cUa P→L + + +
rpoC1 2753 uCa→uUa S→L + + +
rps8 182 uCa→uUa S→L + + +
rps14 80 uCa→uUa S→L + + +
ycf3 44 uCc→uUc S→F - - -
191 aCg→aUg T→M + + +

表4

谷子与7种单子叶植物叶绿体基因RNA编辑位点的比较"

基因
Gene		 密码子位置
Codon
position		 谷子
Setaria italica		 水稻
Oryza
sativa		 黑麦
Lolium
perenne		 玉米
Zea
mays		 小麦
Triticum asetivum		 大麦
Hordeum vulgare		 野生二粒小麦
Triticum
dicoccoides		 乌拉尔图小麦
Triticum
urartu
atpA 1148 + + + + + + + +
ccsA 641 -
matK 1258 - + +/- + + +
ndhA 47 + - + + + -
470 + + + + + + + +
560 + + + + + + + +
ndhB 467 + + + + + + + +
586 + + + + + + + +
基因
Gene		 密码子位置
Codon
position		 谷子
Setaria italica		 水稻
Oryza
sativa		 黑麦
Lolium
perenne		 玉米
Zea
mays		 小麦
Triticum asetivum		 大麦
Hordeum vulgare		 野生二粒小麦
Triticum
dicoccoides		 乌拉尔图小麦
Triticum
urartu
611 + +/- + + + + + +
737 + + + + + + + -
830 + + + + + + + +
1481 + +/- + + + + + +
ndhD 878 + + +/- + + + + +
ndhF 62 - + + + + + - +
petB 668 - - + + - + +
rpl20 308 + - +/- + + + + +
rpoB 467 +/- +/- +/- + +/- + + +
545 +/- +/- +/- + +/- + + +
560 +/- +/- +/- + +/- + + +
617 + - - + + + +
rpoC1 2753 +
rps8 182 + + + + + - + +
rps14 80 + + - + - - +
ycf3 44 - - + + + + +
191 + +/- + +/- + + +

图2

长农35号及E752与E1005中rpoB编辑效率分析"

图3

rpoB在不同发育时期的表达水平分析 *、**分别表示在P < 0.05和P < 0.01水平差异显著。"

图4

不同发育时期光合途径相关基因的表达水平分析 *、**分别表示在P < 0.05和P < 0.01水平差异显著。"

图5

rpoB编辑前后蛋白结构分析 A: 编辑前后跨膜结构域分析; 横坐标表示氨基酸残基序号; 纵坐标表示横轴上每个氨基酸位于膜内侧(inside)、膜外侧(outside)和跨膜螺旋区(transmembrane)的概率值。B: 编辑位点二级结构分析; 箭头表示编辑位点; 蓝色表示α-螺旋; 绿色表示β-折叠; 黄色表示无规则卷曲; 红色表示延伸链。"

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