Biotechnology Bulletin ›› 2022, Vol. 38 ›› Issue (7): 160-170.doi: 10.13560/j.cnki.biotech.bull.1985.2021-1285
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WANG Hui1(
), MA Yi-wen2, QIAO Zheng-hao3, CHANG Yan-cai3, ZHU Kun3, DING Hai-ping3, NIE Yong-xin3(), PAN Guang-tang1()
Received:2021-10-09
Online:2022-07-26
Published:2022-08-09
Contact:
NIE Yong-xin,PAN Guang-tang
E-mail:wanghui18310256976@163.com;pangt@sicau.edu.cn;nyx03@163.com
WANG Hui, MA Yi-wen, QIAO Zheng-hao, CHANG Yan-cai, ZHU Kun, DING Hai-ping, NIE Yong-xin, PAN Guang-tang. Structural and Functional Characterization of AOX Gene Family[J]. Biotechnology Bulletin, 2022, 38(7): 160-170.
| 引物名称Gene name | 上游引物Upstream primer（5'-3'） | 下游引物Downstream primer（5'-3'） |
|---|---|---|
| 18S | CTGAGAAACGGCTACCACA | CCCAAGGTCCAACTACGAG |
| Zm00001d017727qRT | TGGACCGTCAAATTACTGCG | ATGCGTTCATTCTCCGCCTC |
| Zm00001d002434qRT | CTACTGGGGCATCGACACG | GCAGCGACTTGACGATCAG |
| Zm00001d002435qRT | AGGGGCAGGACAAGAAGGCCG | TACGTGTCCCATGGCCTGAA |
| Zm00001d002436qRT | GCTTATGTCCACGTCCTCCC | TGTACGTCTCCCATGGCCTA |
Table1 Prime Sequence
| 引物名称Gene name | 上游引物Upstream primer（5'-3'） | 下游引物Downstream primer（5'-3'） |
|---|---|---|
| 18S | CTGAGAAACGGCTACCACA | CCCAAGGTCCAACTACGAG |
| Zm00001d017727qRT | TGGACCGTCAAATTACTGCG | ATGCGTTCATTCTCCGCCTC |
| Zm00001d002434qRT | CTACTGGGGCATCGACACG | GCAGCGACTTGACGATCAG |
| Zm00001d002435qRT | AGGGGCAGGACAAGAAGGCCG | TACGTGTCCCATGGCCTGAA |
| Zm00001d002436qRT | GCTTATGTCCACGTCCTCCC | TGTACGTCTCCCATGGCCTA |
| 基因ID Gene ID | 染色体编号 Chrom No. | 氨基酸长 Length/ aa | 分子质量 Molecular weight/ kD | 等电点 pI | 重力值 GRAVY | 亚细胞定位 Location |
|---|---|---|---|---|---|---|
| AtAOX1a_AT3G22370.1 | 3 | 354 | 39.98 | 8.56 | -0.33 | Cytoplasmic |
| AtAOX1b_AT3G22360.1 | 3 | 325 | 37.43 | 8.55 | -0.35 | Cytoplasmic |
| AtAOX1c_AT3G27620.1 | 3 | 329 | 37.82 | 6.91 | -0.33 | Cytoplasmic |
| AtAOX1d_AT1G32350.1 | 1 | 318 | 36.20 | 8.65 | -0.29 | Cytoplasmic |
| AtAOX2_AT5G64210.1 | 5 | 353 | 40.09 | 9.14 | -0.17 | Cytoplasmic |
| BdAOX_KQJ84389 | 5 | 333 | 37.34 | 8.37 | -0.21 | Periplasmic |
| BdAOX_KQJ84390 | 5 | 324 | 36.14 | 7.88 | -0.19 | Periplasmic |
| BdAOX_KQJ84391 | 5 | 330 | 36.77 | 7.29 | -0.22 | Periplasmic |
| BdAOX_KQK00893 | 3 | 394 | 43.98 | 9.37 | -0.24 | Cytoplasmic |
| BdAOX_PNT69270 | 3 | 391 | 43.67 | 9.49 | -0.29 | Cytoplasmic |
| GmAOX_KRH42153 | 8 | 326 | 37.12 | 8.68 | -0.32 | Cytoplasmic |
| GmAOX_KRH42154 | 8 | 333 | 38.14 | 9.36 | -0.27 | Cytoplasmic |
| GmAOX_KRH58272 | 5 | 317 | 36.01 | 9.01 | -0.18 | Cytoplasmic |
| GmAOX_KRH62683 | 4 | 321 | 36.48 | 8.57 | -0.24 | Cytoplasmic |
| OsAOX_Os02t0318100-00 | 2 | 353 | 39.46 | 9.46 | -0.17 | Periplasmic |
| OsAOX_Os02t0700400-01 | 2 | 345 | 37.89 | 8.31 | -0.15 | Cytoplasmic |
| OsAOX_Os04t0600200-01 | 4 | 332 | 37.14 | 7.82 | -0.12 | Cytoplasmic |
| OsAOX_Os04t0600300-01 | 4 | 335 | 37.25 | 7.23 | -0.21 | Periplasmic |
| SbAOX_EES05672 | 4 | 346 | 38.47 | 7.82 | -0.15 | Cytoplasmic |
| SbAOX_EES12781 | 6 | 331 | 37.16 | 8.63 | -0.23 | Periplasmic |
| SbAOX_EES12782 | 6 | 314 | 35.58 | 8.78 | -0.23 | Cytoplasmic |
| SbAOX_EES12783 | 6 | 332 | 36.84 | 7.96 | -0.20 | Cytoplasmic |
| SlAOX_Solyc01g105220.3.1 | 1 | 348 | 39.91 | 8.56 | -0.26 | Cytoplasmic |
| SlAOX_Solyc08g005560.3.1 | 8 | 753 | 85.44 | 8.07 | -0.14 | Cytoplasmic |
| SlAOX_Solyc08g075540.3.1 | 8 | 642 | 72.72 | 8.30 | -0.30 | Periplasmic |
| StAOX_PGSC0003DMT400019707 | 8 | 321 | 36.72 | 6.76 | -0.38 | Cytoplasmic |
| StAOX_PGSC0003DMT400019708 | 8 | 356 | 39.82 | 8.29 | -0.28 | Periplasmic |
| StAOX_PGSC0003DMT400019709 | 8 | 355 | 39.64 | 7.75 | -0.22 | Periplasmic |
| StAOX_PGSC0003DMT400019710 | 8 | 174 | 19.68 | 5.44 | 0.02 | Cytoplasmic |
| StAOX_PGSC0003DMT400032705 | 1 | 353 | 40.36 | 8.45 | -0.19 | Cytoplasmic |
| StAOX_PGSC0003DMT400047562 | 8 | 279 | 31.91 | 9.08 | -0.12 | Cytoplasmic |
| ZmAOX_Zm00001d002434_P001 | 2 | 332 | 36.77 | 8.02 | -0.16 | Cytoplasmic |
| ZmAOX_Zm00001d002435_P001 | 2 | 329 | 37.04 | 8.98 | -0.23 | Periplasmic |
| ZmAOX_Zm00001d002436_P001 | 2 | 329 | 36.90 | 8.84 | -0.20 | Periplasmic |
| ZmAOX_Zm00001d017727_P001 | 5 | 347 | 38.72 | 8.37 | -0.16 | Cytoplasmic |
Table 2 Identification and characteristic features of AOX gene family in eight species
| 基因ID Gene ID | 染色体编号 Chrom No. | 氨基酸长 Length/ aa | 分子质量 Molecular weight/ kD | 等电点 pI | 重力值 GRAVY | 亚细胞定位 Location |
|---|---|---|---|---|---|---|
| AtAOX1a_AT3G22370.1 | 3 | 354 | 39.98 | 8.56 | -0.33 | Cytoplasmic |
| AtAOX1b_AT3G22360.1 | 3 | 325 | 37.43 | 8.55 | -0.35 | Cytoplasmic |
| AtAOX1c_AT3G27620.1 | 3 | 329 | 37.82 | 6.91 | -0.33 | Cytoplasmic |
| AtAOX1d_AT1G32350.1 | 1 | 318 | 36.20 | 8.65 | -0.29 | Cytoplasmic |
| AtAOX2_AT5G64210.1 | 5 | 353 | 40.09 | 9.14 | -0.17 | Cytoplasmic |
| BdAOX_KQJ84389 | 5 | 333 | 37.34 | 8.37 | -0.21 | Periplasmic |
| BdAOX_KQJ84390 | 5 | 324 | 36.14 | 7.88 | -0.19 | Periplasmic |
| BdAOX_KQJ84391 | 5 | 330 | 36.77 | 7.29 | -0.22 | Periplasmic |
| BdAOX_KQK00893 | 3 | 394 | 43.98 | 9.37 | -0.24 | Cytoplasmic |
| BdAOX_PNT69270 | 3 | 391 | 43.67 | 9.49 | -0.29 | Cytoplasmic |
| GmAOX_KRH42153 | 8 | 326 | 37.12 | 8.68 | -0.32 | Cytoplasmic |
| GmAOX_KRH42154 | 8 | 333 | 38.14 | 9.36 | -0.27 | Cytoplasmic |
| GmAOX_KRH58272 | 5 | 317 | 36.01 | 9.01 | -0.18 | Cytoplasmic |
| GmAOX_KRH62683 | 4 | 321 | 36.48 | 8.57 | -0.24 | Cytoplasmic |
| OsAOX_Os02t0318100-00 | 2 | 353 | 39.46 | 9.46 | -0.17 | Periplasmic |
| OsAOX_Os02t0700400-01 | 2 | 345 | 37.89 | 8.31 | -0.15 | Cytoplasmic |
| OsAOX_Os04t0600200-01 | 4 | 332 | 37.14 | 7.82 | -0.12 | Cytoplasmic |
| OsAOX_Os04t0600300-01 | 4 | 335 | 37.25 | 7.23 | -0.21 | Periplasmic |
| SbAOX_EES05672 | 4 | 346 | 38.47 | 7.82 | -0.15 | Cytoplasmic |
| SbAOX_EES12781 | 6 | 331 | 37.16 | 8.63 | -0.23 | Periplasmic |
| SbAOX_EES12782 | 6 | 314 | 35.58 | 8.78 | -0.23 | Cytoplasmic |
| SbAOX_EES12783 | 6 | 332 | 36.84 | 7.96 | -0.20 | Cytoplasmic |
| SlAOX_Solyc01g105220.3.1 | 1 | 348 | 39.91 | 8.56 | -0.26 | Cytoplasmic |
| SlAOX_Solyc08g005560.3.1 | 8 | 753 | 85.44 | 8.07 | -0.14 | Cytoplasmic |
| SlAOX_Solyc08g075540.3.1 | 8 | 642 | 72.72 | 8.30 | -0.30 | Periplasmic |
| StAOX_PGSC0003DMT400019707 | 8 | 321 | 36.72 | 6.76 | -0.38 | Cytoplasmic |
| StAOX_PGSC0003DMT400019708 | 8 | 356 | 39.82 | 8.29 | -0.28 | Periplasmic |
| StAOX_PGSC0003DMT400019709 | 8 | 355 | 39.64 | 7.75 | -0.22 | Periplasmic |
| StAOX_PGSC0003DMT400019710 | 8 | 174 | 19.68 | 5.44 | 0.02 | Cytoplasmic |
| StAOX_PGSC0003DMT400032705 | 1 | 353 | 40.36 | 8.45 | -0.19 | Cytoplasmic |
| StAOX_PGSC0003DMT400047562 | 8 | 279 | 31.91 | 9.08 | -0.12 | Cytoplasmic |
| ZmAOX_Zm00001d002434_P001 | 2 | 332 | 36.77 | 8.02 | -0.16 | Cytoplasmic |
| ZmAOX_Zm00001d002435_P001 | 2 | 329 | 37.04 | 8.98 | -0.23 | Periplasmic |
| ZmAOX_Zm00001d002436_P001 | 2 | 329 | 36.90 | 8.84 | -0.20 | Periplasmic |
| ZmAOX_Zm00001d017727_P001 | 5 | 347 | 38.72 | 8.37 | -0.16 | Cytoplasmic |
Fig. 1 Phylogenetic analysis of AOX in eight species
Fig. 2 Phylogenetic relationship,gene structure,and conserved motifs analysis of AOX
Fig. 3 Collinearity of AOX genes between maize and other species （a）Arabidopsis thaliana.（b）Oryza sativa.（c）Sorghum bicolor.（d）Brachypodium distachyon.（e）Solanum lycopersicum.（f）Glycine max.（g）Solanum tuberosum
| 玉米AOX ZmAOXs | 染色体编号 Chrom No. | 其他物种AOX Other AOXs | 染色体编号 Chrom No. | N | S | Ka | Ks | Ka/Ks | Mya |
|---|---|---|---|---|---|---|---|---|---|
| ZmAOX_Zm00001d002434_P001 | 2 | SbAOX_EES12783 | 6 | 842.4 | 126.6 | 0.05 | 0.47 | 0.10 | 36.49 |
| ZmAOX_Zm00001d002435_P001 | 2 | BdAOX_KQJ84390 | 5 | 824.5 | 141.5 | 0.09 | 1.86 | 0.05 | 143.31 |
| ZmAOX_Zm00001d002435_P001 | 2 | OsAOX_Os04t0600300-01 | 4 | 858.2 | 128.8 | 0.10 | 0.79 | 0.13 | 60.89 |
| ZmAOX_Zm00001d002435_P001 | 2 | SbAOX_EES12782 | 6 | 826 | 113 | 0.02 | 0.24 | 0.08 | 18.32 |
| ZmAOX_Zm00001d002436_P001 | 2 | AtAOX1a_AT3G22370.1 | 3 | 729.6 | 248.4 | 0.20 | 65.03 | 0.00 | 5 002.48 |
| ZmAOX_Zm00001d002436_P001 | 2 | BdAOX_KQJ84389 | 5 | 839.3 | 147.7 | 0.09 | 1.09 | 0.09 | 84.08 |
| ZmAOX_Zm00001d002436_P001 | 2 | GmAOX_KRH62683 | 4 | 738.7 | 218.3 | 0.21 | 72.34 | 0.00 | 5 564.66 |
| ZmAOX_Zm00001d002436_P001 | 2 | OsAOX_Os04t0600200-01 | 4 | 838.9 | 139.1 | 0.08 | 1.12 | 0.07 | 86.45 |
| ZmAOX_Zm00001d002436_P001 | 2 | SbAOX_EES12781 | 6 | 850.2 | 136.8 | 0.01 | 0.29 | 0.03 | 22.22 |
| ZmAOX_Zm00001d002436_P001 | 2 | SlAOX_Solyc01g105220.3.1 | 1 | 747.2 | 230.8 | 0.26 | 23.83 | 0.01 | 1 832.88 |
| ZmAOX_Zm00001d017727_P001 | 5 | BdAOX_KQK00893 | 3 | 856.1 | 157.9 | 0.08 | 1.44 | 0.06 | 110.84 |
| ZmAOX_Zm00001d017727_P001 | 5 | BdAOX_PNT69270 | 3 | 848.1 | 156.9 | 0.11 | 1.85 | 0.06 | 142.36 |
| ZmAOX_Zm00001d017727_P001 | 5 | GmAOX_KRH62683 | 4 | 727.2 | 226.8 | 0.21 | 24.26 | 0.01 | 1 866.37 |
| ZmAOX_Zm00001d017727_P001 | 5 | OsAOX_Os02t0700400-01 | 2 | 864.9 | 161.1 | 0.10 | 1.45 | 0.07 | 111.63 |
| ZmAOX_Zm00001d017727_P001 | 5 | SbAOX_EES05672 | 4 | 865.8 | 169.2 | 0.02 | 0.22 | 0.08 | 16.71 |
| ZmAOX_Zm00001d017727_P001 | 5 | StAOX_PGSC0003DMT400019708 | 8 | 760.2 | 262.8 | 0.28 | 25.43 | 0.01 | 1 955.81 |
| ZmAOX_Zm00001d017727_P001 | 5 | StAOX_PGSC0003DMT400019709 | 8 | 752.6 | 261.4 | 0.32 | 15.51 | 0.02 | 1 193.40 |
Table 3 Ka/Ks for orthologous AOX proteins between Z. mays and other seven species
| 玉米AOX ZmAOXs | 染色体编号 Chrom No. | 其他物种AOX Other AOXs | 染色体编号 Chrom No. | N | S | Ka | Ks | Ka/Ks | Mya |
|---|---|---|---|---|---|---|---|---|---|
| ZmAOX_Zm00001d002434_P001 | 2 | SbAOX_EES12783 | 6 | 842.4 | 126.6 | 0.05 | 0.47 | 0.10 | 36.49 |
| ZmAOX_Zm00001d002435_P001 | 2 | BdAOX_KQJ84390 | 5 | 824.5 | 141.5 | 0.09 | 1.86 | 0.05 | 143.31 |
| ZmAOX_Zm00001d002435_P001 | 2 | OsAOX_Os04t0600300-01 | 4 | 858.2 | 128.8 | 0.10 | 0.79 | 0.13 | 60.89 |
| ZmAOX_Zm00001d002435_P001 | 2 | SbAOX_EES12782 | 6 | 826 | 113 | 0.02 | 0.24 | 0.08 | 18.32 |
| ZmAOX_Zm00001d002436_P001 | 2 | AtAOX1a_AT3G22370.1 | 3 | 729.6 | 248.4 | 0.20 | 65.03 | 0.00 | 5 002.48 |
| ZmAOX_Zm00001d002436_P001 | 2 | BdAOX_KQJ84389 | 5 | 839.3 | 147.7 | 0.09 | 1.09 | 0.09 | 84.08 |
| ZmAOX_Zm00001d002436_P001 | 2 | GmAOX_KRH62683 | 4 | 738.7 | 218.3 | 0.21 | 72.34 | 0.00 | 5 564.66 |
| ZmAOX_Zm00001d002436_P001 | 2 | OsAOX_Os04t0600200-01 | 4 | 838.9 | 139.1 | 0.08 | 1.12 | 0.07 | 86.45 |
| ZmAOX_Zm00001d002436_P001 | 2 | SbAOX_EES12781 | 6 | 850.2 | 136.8 | 0.01 | 0.29 | 0.03 | 22.22 |
| ZmAOX_Zm00001d002436_P001 | 2 | SlAOX_Solyc01g105220.3.1 | 1 | 747.2 | 230.8 | 0.26 | 23.83 | 0.01 | 1 832.88 |
| ZmAOX_Zm00001d017727_P001 | 5 | BdAOX_KQK00893 | 3 | 856.1 | 157.9 | 0.08 | 1.44 | 0.06 | 110.84 |
| ZmAOX_Zm00001d017727_P001 | 5 | BdAOX_PNT69270 | 3 | 848.1 | 156.9 | 0.11 | 1.85 | 0.06 | 142.36 |
| ZmAOX_Zm00001d017727_P001 | 5 | GmAOX_KRH62683 | 4 | 727.2 | 226.8 | 0.21 | 24.26 | 0.01 | 1 866.37 |
| ZmAOX_Zm00001d017727_P001 | 5 | OsAOX_Os02t0700400-01 | 2 | 864.9 | 161.1 | 0.10 | 1.45 | 0.07 | 111.63 |
| ZmAOX_Zm00001d017727_P001 | 5 | SbAOX_EES05672 | 4 | 865.8 | 169.2 | 0.02 | 0.22 | 0.08 | 16.71 |
| ZmAOX_Zm00001d017727_P001 | 5 | StAOX_PGSC0003DMT400019708 | 8 | 760.2 | 262.8 | 0.28 | 25.43 | 0.01 | 1 955.81 |
| ZmAOX_Zm00001d017727_P001 | 5 | StAOX_PGSC0003DMT400019709 | 8 | 752.6 | 261.4 | 0.32 | 15.51 | 0.02 | 1 193.40 |
Fig. 4 Characterization of cis-acting regulatory elements in the promoter region of these identified AOX genes
| miRNA 序号 miRNA accession | 靶基因ID Target accession | E值 Expectation | 抑制作用 Inhibition | miRNA起始 miRNA start | miRNA终止 miRNA end | 基因起始 Target start | 基因终止 Target end |
|---|---|---|---|---|---|---|---|
| ath-miR5021 | AtAOX1c_AT3G27620.1 | 2.5 | Cleavage | 1 | 20 | 6 | 25 |
| bdi-miR5175a | BdAOX_KQK00893 | 3 | Translation | 1 | 21 | 1 686 | 1 706 |
| bdi-miR5175a | BdAOX_PNT69270 | 3 | Translation | 1 | 21 | 1 671 | 1 691 |
| gma-miR1507a | GmAOX_KRH62683 | 3.5 | Translation | 1 | 22 | 370 | 391 |
| sbi-miR6220-5p | SbAOX_EES12782 | 0.5 | Cleavage | 1 | 24 | 1 558 | 1 581 |
| sly-miR319a | SlAOX_Solyc08g005560.3.1 | 3.5 | Cleavage | 1 | 20 | 1 172 | 1 191 |
| stu-miR319a-5p | StAOX_PGSC0003DMT400019708 | 3.5 | Translation | 1 | 21 | 760 | 780 |
| stu-miR319a-5p | StAOX_PGSC0003DMT400019709 | 3.5 | Translation | 1 | 21 | 760 | 780 |
| stu-miR319a-5p | StAOX_PGSC0003DMT400019710 | 3.5 | Translation | 1 | 21 | 132 | 152 |
| stu-miR7981-3p | StAOX_PGSC0003DMT400032705 | 3.5 | Translation | 1 | 24 | 1 394 | 1 417 |
| zma-miR395c-3p | ZmAOX_Zm00001d002435_P001 | 2.5 | Cleavage | 1 | 21 | 78 | 98 |
Table 4 List of putative miRNAs targeted AOX genes identified by psRNATarget online tool
| miRNA 序号 miRNA accession | 靶基因ID Target accession | E值 Expectation | 抑制作用 Inhibition | miRNA起始 miRNA start | miRNA终止 miRNA end | 基因起始 Target start | 基因终止 Target end |
|---|---|---|---|---|---|---|---|
| ath-miR5021 | AtAOX1c_AT3G27620.1 | 2.5 | Cleavage | 1 | 20 | 6 | 25 |
| bdi-miR5175a | BdAOX_KQK00893 | 3 | Translation | 1 | 21 | 1 686 | 1 706 |
| bdi-miR5175a | BdAOX_PNT69270 | 3 | Translation | 1 | 21 | 1 671 | 1 691 |
| gma-miR1507a | GmAOX_KRH62683 | 3.5 | Translation | 1 | 22 | 370 | 391 |
| sbi-miR6220-5p | SbAOX_EES12782 | 0.5 | Cleavage | 1 | 24 | 1 558 | 1 581 |
| sly-miR319a | SlAOX_Solyc08g005560.3.1 | 3.5 | Cleavage | 1 | 20 | 1 172 | 1 191 |
| stu-miR319a-5p | StAOX_PGSC0003DMT400019708 | 3.5 | Translation | 1 | 21 | 760 | 780 |
| stu-miR319a-5p | StAOX_PGSC0003DMT400019709 | 3.5 | Translation | 1 | 21 | 760 | 780 |
| stu-miR319a-5p | StAOX_PGSC0003DMT400019710 | 3.5 | Translation | 1 | 21 | 132 | 152 |
| stu-miR7981-3p | StAOX_PGSC0003DMT400032705 | 3.5 | Translation | 1 | 24 | 1 394 | 1 417 |
| zma-miR395c-3p | ZmAOX_Zm00001d002435_P001 | 2.5 | Cleavage | 1 | 21 | 78 | 98 |
Fig. 5 Gene ontology（GO）annotation analysis of AOX
Fig. 6 Expression analysis of AOX family in maize under four stress condition
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