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Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (4): 873-885.doi: 10.3724/SP.J.1006.2022.14043

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

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 Online:2022-04-12 Published:2021-07-24
  • Contact: WANG Jun E-mail:dxf6285210@126.com;128wan@163.com
  • 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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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

Table 1

Primers used in this study"

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

Fig. 1

Phenotypes and ultrastructure of chloroplasts in Changnong 35, E1005, and E752 at seeding stage A-C: Changnong 35; D-F: E1005; G-I: E752; GL: grana lamellae; SG: starch granule; OP: osmiophilic granule."

Table 2

Comparison of pigment contents in leaves among Changnong 35, E752, and E1005 at seeding stage (mg g-1)"

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**

Table 3

Prediction, validation, and comparison of RNA editing sites among Changnong 35, E752, and E1005"

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 + + +

Table 4

Comparison of RNA editing sites between Setaria italica and other seven monocots"

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 + +/- + +/- + + +

Fig. 2

Editing efficiency of rpoB among Changnong 35, E752, and E1005"

Fig. 3

Relative expression patterns of rpoB genes at different development stages * and ** mean significant difference at the 0.05 and 0.01 probability levels, respectively."

Fig. 4

Relative expression patterns of photosynthetic pathway genes at different development stages * and ** mean significant difference at the 0.05 and 0.01 probability levels, respectively."

Fig. 5

Protein structure on rpoB before and after editing A: the prediction of trans-membrane structure of rpoB before and after editing; the horizontal axis represents the sequence number of amino acid residues; the vertical axis represents the probability value of each amino acid in different position of membrane. B: the prediction of protein secondary structure of rpoB before and after editing; the arrows refer to the editing sites; blue: α-helix; green: β-fold; yellow: random coil; red: extended strand."

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