Welcome to Acta Agronomica Sinica,

Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (5): 1152-1168.doi: 10.3724/SP.J.1006.2022.14003

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

Codon usage bias analysis of S-locus genes SRK, SLG, and SP11/SCR in Brassica oleracea

ZHANG Yi-Zhong1,2(), ZENG Wen-Yi1, DENG Lin-Qiong2, ZHANG He-Cui1, LIU Qian-Ying1, ZUO Tong-Hong1, XIE Qin-Qin1, HU Deng-Ke1, YUAN Chong-Mo1, LIAN Xiao-Ping1, ZHU Li-Quan1,*()   

  1. 1College of Agronomy and Biotechnology, Southwest University, Chongqing 400715, China
    2Ecological Engineering School, Guizhou University of Engineering Science, Bijie 551700, Guizhou, China
  • Received:2021-01-11 Accepted:2021-09-09 Online:2022-05-12 Published:2021-10-18
  • Contact: ZHU Li-Quan E-mail:z8300300@163.com;zhuliquan@swu.edu.cn
  • About author:First author contact:**Contributed equally to this work
  • Supported by:
    National Natural Science Foundation of China(31572127);Fundamental Research Funds for the Central Universities(XDJK2020D024)

Abstract:

S-locus is the key locus in Brassica that controls the recognition and initiation of the self-incompatibility response. To clarify the codon usage characteristics of the S domain of S-locus genes SRK and SLG as well as of SP11/SCR coding sequence in Brassica oleracea, the codon usage bias of 41, 36, and 11 alleles of SRK, SLG, and SP11/SCR were analyzed by Codon W, SPSS, Python, and EMBOSS online tools, respectively. Neutrality, ENC-GC3, and Parity Rule 2 (PR2) plotting together with multivariate statistical analysis were also used for the exploration of possible factors that might affect the formation of the codon usage bias of these genes. The cluster analysis performed using various methods showed that S domains of SRK, SLG, and SP11/SCR genes of Brassica oleracea were rich in AT base pairs, the codon preference ended with A/T base and had a lower codon usage bias, which were affected by the natural selection (a main factor) and the mutational pressure (a secondary factor) as well as dinucleotide abundance. Based on the RSCU values, 4 over-expressed codons of SRK and SLG, and 11 over-expressed codons of SP11/SCR were identified. Cluster analysis based on RSCU could accurately reflect the relationship among SRK, SLG, and SP11/SCR alleles in Brassica oleracea, which was consistent and reliable with CDS sequence clustering. According to codon usage bias and cluster relationship, the S domain of SRK and the SP11/SCR coding sequence might be coevolutionary in the codon usage bias. This study enhances our understanding of the mechanism of distribution of codons and the evolution of SRK, SLG, and SP11/SCR genes in Brasscia oleracea.

Key words: Brassica oleracea, self-incompatibility, S-locus genes, codon usage bias, cluster analysis

Table 1

Information of SRK, SLG, and SP11/SCR alleles in Brassica oleracea"

序号
No.
基因登录号
Gene accession ID
基因名称
Gene name
类型
Class
参考文献
Reference
序号
No.
基因登录号
Gene accession ID
基因名称
Gene name
类型
Class
参考文献
Reference
1 AB054706.1 SRK1 I Sato et al., 2002 45 X55275.1 SLG13 I Dwyer et al., 1991
2 AB054709.1 SRK11 I Sato et al., 2002 46 D85228.1 SLG14 I Kusaba et al., 1997
3 AB180901.1 SRK12 I Fujimoto et al., 2006 47 D85202.1 SLG16 I Kusaba et al., 1997
4 AB024420.2 SRK13 I Kusaba et al., 2000 48 AB054728.1 SLG20 I Sato et al., 2002
5 AB298891.1 SRK14 I Takuno et al., 2007 49 AB013719.1 SLG23 I Kusaba et al., 1999
6 AB054710.1 SRK16 I Sato et al., 2002 50 D85204.1 SLG25 I Kusaba et al., 1997
7 AB054711.1 SRK20 I Sato et al., 2002 51 D85205.1 SLG28 I Kusaba et al., 1997
8 AB013720.1 SRK23 I Kusaba et al., 1999 52 X16123.1 SLG29 I Trick et al., 1989
9 AB054713.1 SRK25 I Sato et al., 2002 53 X79431.1 SLG3 I Delorme et al., 1995
10 AB190355.1 SRK28 I Fujimot, 2004 54 D88765.1 SLG32 I Kusaba et al., 1997
11 Z30211.1 SRK29 I Kumar et al., 1994 55 AB054730.1 SLG33 I Sato et al., 2002
12 X79432.1 SRK3 I Delorme et al., 1995 56 D85206.1 SLG35 I Kusaba et al., 1997
13 AB050482.1 SRK32 I Kimura et al., 2000 57 AB054731.1 SLG36 I Sato et al., 2002
14 AB054714.1 SRK33 I Sato et al., 2002 58 D85207.1 SLG39 I Kusaba et al., 1997
15 AB054715.1 SRK35 I Sato et al., 2002 59 AB054732.1 SLG45 I Sato et al., 2002
16 AB054716.1 SRK36 I Sato et al., 2002 60 AB054733.1 SLG50 I Sato et al., 2002
17 AB054718.1 SRK39 I Sato et al., 2002 61 D85209.1 SLG51 I Kusaba et al., 1997
18 AB054719.1 SRK45 I Sato et al., 2002 62 D85210.1 SLG52 I Kusaba et al., 1997
19 AB054720.1 SRK50 I Sato et al., 2002 63 AB054734.1 SLG57 I Sato et al., 2002
20 AB054721.1 SRK51 I Sato et al., 2002 64 AB054735.1 SLG58 I Sato et al., 2002
21 AB298901.1 SRK52 I Takuno et al., 2007 65 Y00268.1 SLG6 I Nasrallah et al., 1987
22 AB054722.1 SRK57 I Sato et al., 2002 66 AB054736.1 SLG62 I Sato et al., 2002
23 AB054723.1 SRK58 I Sato et al., 2002 67 D85212.1 SLG64 I Kusaba et al., 1997
24 M76647.1 SRK6 I Stein et al., 1991 68 AB054737.1 SLG65 I Sato et al., 2002
25 AB054724.1 SRK62 I Sato et al., 2002 69 D85199.1 SLG7 I Kusaba et al., 1997
26 AB054725.1 SRK64 I Sato et al., 2002 70 AB054727.1 SLG8 I Sato et al., 2002
27 AB054726.1 SRK65 I Sato et al., 2002 71 D85211.1 SLG63 I Kusaba et al., 1997
28 AB180898.1 SRK7 I Fujimoto et al., 2006 72 D85208.1 SLG46 I Kusaba et al., 1997
29 AB054708.1 SRK8 I Sato et al., 2002 73 D85200.1 SLG9 I Kusaba et al., 1997
30 AB054707.1 SRK7b I Sato et al., 2002 74 AB054729.1 SLG31 I Sato et al., 2002
31 AB032473.1 SRK18 I Suzuki et al., 2000 75 D85203.1 SLG17 I Kusaba et al., 1997
32 AB298890.1 SRK4 I Takuno et al., 2007 76 D85229.1 SLG22 I Kusaba et al., 1997
33 AB298902.1 SRK61 I Takuno et al., 2007 77 AB024415.1 SLG2 II Kusaba et al., 2000
34 AB298905.1 SRK68 I Takuno et al., 2007 78 AF195626.1 BoSCR13 I Schopfer et al., 1999
35 AB054717.1 SRK38 I Sato et al., 2002 79 EF577028.1 BoSCR13b I Lan et al., 2007
36 AB054712.1 SRK24 I Sato et al., 2002 80 AJ278643.1 BoSCR3 I Vanoosthuyse et al., 2001
37 AB024422.2 SRK13b I Kusaba et al., 2000 81 AB180900.1 BoSP11-12 I Fujimoto et al., 2006
38 AB180903.1 SRK15 II Fujimoto et al., 2006 82 AB176545.1 BoSP11-15 II Shiba et al., 2004
39 AB024416.1 SRK2 II Kusaba et al., 2000 83 AB067447.1 BoSP11-2 II Shiba et al., 2002
40 Y18259.1 SRK5 II Cabrillac et al., 1999 84 AB190356.1 BoSP11-28 I Fujimoto, 2004
41 AB032474.1 SRK60 I Suzuki et al., 2000 85 AB067448.1 BoSP11-5 II Shiba et al., 2002
42 D85198.1 SLG1 I Kusaba et al., 1997 86 AF195625 BoSCR6 I Schopfer et al., 1999
43 AB326957.1 SLG11 I Takuno et al., 2008 87 AB180898.1 BoSP11-7 I Fujimoto et al., 2006
44 AB180902.1 SLG12 I Fujimoto et al., 2006 88 AB180904.1 BoSP11A-15 II Fujimoto et al., 2006

Table 2

Nucleotide composition and ENC of SRK, SLG, and SP11/SCR coding sequences"

核苷酸组成和ENC
Nucleotide composition and ENC
基因Gene
SRK SLG SP11/SCR
A (%) 27.47±0.50 27.30±0.45 29.68±1.42
T (%) 26.84±0.40 26.76±0.50 31.90±1.93
C (%) 20.56±0.42 20.72±0.47 16.49±1.87
G (%) 25.13±0.44 25.23±0.38 21.92±2.43
A3 (%) 20.11±0.93 20.07±0.96 27.79±3.76
T3 (%) 30.28±1.07 30.14±1.13 38.59±4.04
C3 (%) 24.46±1.12 24.54±0.95 16.47±3.46
G3 (%) 25.15±1.07 25.25±0.80 17.15±3.70
GC (%) 45.69±0.47 45.95±0.51 38.42±2.02
AT (%) 54.31±0.47 54.05±0.51 61.58±2.02
GC1 (%) 42.27±0.87 42.33±0.81 37.32±3.55
GC2 (%) 45.18±0.84 45.72±0.98 44.32±3.86
GC3 (%) 49.61±1.39 49.79±1.26 33.61±2.78
GC12 (%) 43.72±0.50 44.02±0.58 40.82±2.75
ENC 56.37±1.20 55.66±1.17 48.55±4.40

Table 3

Relative synonymous codon usage (RSCU) patterns of SRK, SLG, and SP11/SCR"

氨基酸
Amino acid
密码子
Codon
相对同义密码子RSCU 氨基酸
Amino acid
密码子
Codon
相对同义密码子RSCU
SRK SLG SP11/SCR SRK SLG SP11/SCR
Phe UUU 0.72 0.73 1.10 Thr ACU 0.81 0.76 1.93
UUC 1.28 1.27 0.90 ACC 0.97 1.04 0.33
Leu UUA 0.25 0.21 2.38 ACA 1.44 1.46 1.52
UUG 1.50 1.52 1.81 ACG 0.78 0.74 0.22
CUU 1.93 2.06 0.16 Ala GCU 1.67 1.78 2.45
CUC 1.26 1.21 0.26 GCC 0.53 0.45 0.78
CUA 0.39 0.37 0.89 GCA 1.06 1.04 0.57
CUG 0.67 0.63 0.50 GCG 0.74 0.72 0.21
Ile AUU 0.93 0.92 1.11 Gln CAA 1.15 1.17 1.71
AUC 1.24 1.31 0.71 CAG 0.85 0.83 0.29
AUA 0.83 0.77 1.18 Asn AAU 1.05 1.03 1.72
Val GUU 0.69 0.64 2.22 AAC 0.95 0.97 0.28
GUC 1.09 1.11 0.22 Lys AAA 1.10 1.03 1.24
GUA 0.56 0.54 0.57 AAG 0.90 0.97 0.76
GUG 1.66 1.71 0.99 Asp GAU 1.28 1.19 1.45
Ser UCU 1.13 1.15 1.45 GAC 0.72 0.81 0.36
UCC 0.66 0.68 0.30 Glu GAA 0.68 0.70 1.53
UCA 1.25 1.26 2.23 GAG 1.32 1.30 0.47
UCG 0.67 0.61 0.64 Cys UGU 1.52 1.51 1.16
AGU 1.49 1.48 0.57 UGC 0.48 0.49 0.84
AGC 0.81 0.81 0.81 Arg CGU 0.31 0.29 1.17
Pro CCU 0.99 1.08 2.30 CGC 0.20 0.19 1.08
CCC 0.78 0.68 0.58 CGA 0.97 0.99 0.29
CCA 1.33 1.33 0.51 CGG 0.87 0.92 0.35
CCG 0.90 0.92 0.61 AGA 2.25 2.27 1.41
Tyr UAU 0.71 0.71 1.59 AGG 1.41 1.34 1.70
UAC 1.29 1.29 0.41 Gly GGU 1.37 1.39 1.04
His CAU 0.80 0.68 1.36 GGC 0.42 0.34 0.64
CAC 1.15 1.32 0.45 GGA 1.01 1.02 2.03
GGG 1.20 1.26 0.29

Fig. 1

Correspondence analysis of codon usage patterns"

Fig. 2

PR2-bias plot analysis"

Fig. 3

ENC-GC3 plot analysis ENC: effective number of codons."

Fig. 4

Neutrality plot analysis"

Table 4

Correlation analysis between nucleotide constraints in SRK gene"

A3% T3% C3% G3% GC3% AT3%
A% 0.609** 0.006 -0.321* -0.199 -0.410** 0.410**
T% -0.070 0.534** -0.098 -0.370* -0.362* 0.362*
C% -0.328* -0.157 0.447** -0.028 0.337** -0.337*
G% -0.314* -0.338* 0.023 0.587** 0.468** -0.468**
GC% 1.000** -0.028 -0.422** -0.399** -0.645** 0.645**
AT% 0.581** 0.459** -0.419** -0.524** -0.738** 0.738**

Table 5

Correlation analysis between nucleotide constraints in SLG gene"

A3% T3% C3% G3% GC3% AT3%
A% 0.634** -0.343* -0.036 -0.232 -0.173 0.173
T% -0.110 0.693** -0.500** -0.253 -0.537** 0.537**
C% -0.206 -0.453** 0.629** 0.137 0.561** -0.561**
G% -0.347* 0.057 -0.085 0.436** 0.212 -0.212
GC% -0.466** -0.366* 0.523** 0.452** 0.681** -0.681**
AT% 0.466** 0.366* -0.523** -0.452** -0.681** 0.681**

Table 6

Correlation analysis between nucleotide constraints in SP11/SCR gene"

A3% T3% C3% G3% GC3% AT3%
A% 0.257 -0.188 0.475 -0.500 -0.074 0.074
T% -0.646* 0.865** -0.374 0.061 -0.383 0.383
C% 0.719* -0.381 0.410 -0.700* -0.420 0.420
G% -0.192 -0.286 -0.298 0.787** 0.675* -0.675*
GC% 0.436 -0.697* 0.022 0.296 0.421 -0.421
AT% -0.436 0.697* -0.022 -0.296 -0.421 0.421

Table 7

Correlation analysis between the first axes and relative abundance of dinucleotides in SRK, SLG, and SP11/SCR genes"

基因
Gene
参数
Parameter
AA AU AG AC UU UA UC UG
SRK 范围Range 0.76-0.91 0.88-1.06 0.87-1.03 0.98-1.20 0.71-0.85 0.62-0.73 1.03-1.34 1.07-1.23
Mean±SD 0.84±0.03 0.97±0.05 0.94±0.04 1.01±0.05 0.80±0.04 0.67±0.03 1.23±0.06 1.17±0.04
第一轴Axes1 0.039 -0.064 0.221 -0.115 0.294* -0.334* -0.227 0.274*
SLG 范围Range 0.80-0.88 0.89-1.03 0.86-1.05 1.01-1.18 0.73-0.88 0.61-0.72 1.05-1.31 1.09-1.27
Mean±SD 0.84±0.02 0.96±0.04 0.96±0.05 1.09±0.04 0.79±0.04 0.67±0.02 1.21±0.07 1.19±0.04
第一轴Axes1 0.166 -0.044 -0.170 0.182 0.525** 0.058 -0.537** 0.108
SP11/SCR 范围Range 0.63-0.12 0.94-1.16 0.69-1.03 0.45-1.12 0.71-0.86 0.58-0.96 0.64-1.28 1.17-1.41
Mean±SD 0.81±0.14 1.06±0.07 0.90±0.11 0.81±0.25 0.78±0.05 0.78±0.12 0.95±0.21 1.29±0.06
第一轴Axes1 0.437 0.221 0.023 -0.383 0.110 -0.546* 0.522* -0.224
基因
Gene
参数
Parameter
CC CA CU CG GG GA GU GC
SRK 范围Range 0.65-0.92 0.96-1.17 0.95-1.23 0.71-1.00 0.75-0.91 1.16-1.35 0.85-1.05 0.59-0.81
Mean±SD 0.82±0.06 1.09±0.05 1.10±0.06 0.83±0.06 0.85±0.03 1.25±0.05 0.94±0.04 0.71±0.05
第一轴Axes1 0.283* 0.226 -0.023 -0.342* -0.131 0.032 -0.145 0.236
SLG 范围Range 0.72-0.98 0.96-1.18 0.99-1.22 0.67-0.96 0.78-0.94 1.20-1.35 0.87-1.02 0.61-0.78
Mean±SD 0.85±0.07 1.09±0.05 1.12±0.05 0.79±0.06 0.84±0.04 1.26±0.03 0.95±0.04 0.70±0.04
第一轴Axes1 0.281* -0.002 -0.192 -0.159 0.087 -0.204 -0.407** 0.291*
SP11/SCR
范围Range 0.46-1.08 1.06-1.38 0.85-1.21 0.43-1.07 0.51-0.88 0.76-1.18 0.67-1.03 1.01-1.63
Mean±SD 0.80±0.18 1.22±0.10 1.01±0.14 0.77±0.21 0.71±0.11 1.00±0.13 0.84±0.11 1.43±0.23
第一轴Axes1 -0.054 0.260 -0.648* 0.681* -0.451 -0.083 0.559* -0.172

Fig. 5

CDS cluster analysis (A) and RSCU cluster analysis (B) of SRK genes in Brassica oleracea The same lowercase letter indicates the same gene in the empty box. Class II haplotype genes are in the red empty box, and the rest are Class I haplotype genes."

Fig. 6

CDS cluster analysis (A) and RSCU cluster analysis (B) of SP11/SCR genes in Brassica oleracea The same lowercase letter indicates the same gene in the empty box. Class II haplotype genes are in the red empty box, and the rest are Class I haplotype genes."

Fig. 7

CDS cluster analysis (A) and RSCU cluster analysis (B) of SRK and SLG genes in Brassica oleracea The same lowercase letter indicates the same gene in the empty box. Class II haplotype genes are in the red empty box, and the rest are Class I haplotype genes."

[1] Chamary J V, Parmley J L, Hurst L D. Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat Rev Genet, 2006, 7:98-108.
pmid: 16418745
[2] Plotkin J B, Dushoff J, Desai M M, Fraser H B. Codon usage and selection on proteins. J Mol Evol, 2006, 63:635-653.
pmid: 17043750
[3] Plotkin J B, Kudla G. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet, 2011, 12:32-42.
doi: 10.1038/nrg2899 pmid: 21102527
[4] Bulmer M G. The selection-mutation-drift theory of synonymous codon usage. Genetics, 1991, 129:897-907.
doi: 10.1093/genetics/129.3.897 pmid: 1752426
[5] Hershberg R, Petrov D A. Selection on codon bias. Annu Rev Genet, 2008, 42:287-299.
doi: 10.1146/annurev.genet.42.110807.091442 pmid: 18983258
[6] 张乐, 金龙国, 罗玲, 王跃平, 董志敏, 孙守红, 邱丽娟. 大豆基因组和转录组的核基因密码子使用偏好性分析. 作物学报, 2011, 37:965-974.
Zhang L, Jin L G, Luo L, Wang Y P, Dong Z M, Sun S H, Qiu L J. Analysis of nuclear gene codon bias on soybean genome and transcriptome. Acta Agron Sin, 2011, 37:965-974 (in Chinese with English abstract).
[7] 寇莹莹, 宋英今, 杨少辉, 王洁华. 植酸酶phyA基因的密码子优化及其在大豆中的表达. 作物学报, 2016, 42:1798-1804.
doi: 10.3724/SP.J.1006.2016.01798
Kou Y Y, Song Y J, Yang S H, Wang J H. Codon optimization and expression of phyA gene in soybean(Glycine max Merr.). Acta Agron Sin, 2016, 42:1798-1804 (in Chinese with English abstract).
[8] Tao P, Dai L, Luo M, Tang F, Tien P, Pan Z. Analysis of synonymous codon usage in classical swine fever virus. Virus Genes, 2009, 38:104-112.
doi: 10.1007/s11262-008-0296-z pmid: 18958611
[9] Wu Y, Zhao D, Tao J. Analysis of codon usage patterns in Herbaceous Peony (Paeonia lactiflora Pall.) based on transcriptome data. Genes, 2015, 6:1125-1139.
doi: 10.3390/genes6041125
[10] Yan Z, Wang R, Zhang L, Shen B, Wang N, Xu Q, He W, He W, Li G, Su S. Evolutionary changes of the novel influenza D virus hemagglutinin-esterase fusion gene revealed by the codon usage pattern. Virulence, 2019, 10:1-9.
doi: 10.1080/21505594.2018.1551708
[11] Liu Y S, Zhou J H, Chen H T, Ma L N, Pejsak Z, Ding Y Z, Zhang J. The characteristics of the synonymous codon usage in enterovirus 71 virus and the effects of host on the virus in codon usage pattern. Infect Genet Evol, 2011, 11:1168-1173.
doi: 10.1016/j.meegid.2011.02.018
[12] Ma J J, Zhao F, Zhang J, Zhou J H, Ma L N, Ding Y Z, Chen H T, Gu Y X, Liu Y S. Analysis of synonymous codon usage in dengue viruses. J Anim Vet Adv, 2013, 12:88-98.
[13] Moratorio G, Iriarte A, Moreno P, Musto H, Cristina J. A detailed comparative analysis on the overall codon usage patterns in West Nile virus. Infect Genet Evol, 2013, 14:396-400.
doi: 10.1016/j.meegid.2013.01.001 pmid: 23333335
[14] Seligmann H, Warthi G. Genetic code optimization for cotranslational protein folding: codon directional asymmetry correlates with antiparallel betasheets, tRNA synthetase classes. Comput Struct Biotechnol J, 2017, 15:412-424.
doi: 10.1016/j.csbj.2017.08.001
[15] Ahn I, Jeong B J, Bae S E, Jung J, Son H S. Genomic analysis of influenza A viruses, including avian flu (H5N1) strains. Eur J Epidemiol, 2006, 21:511-519.
doi: 10.1007/s10654-006-9031-z
[16] Angellotti M C, Bhuiyan S B, Chen G, Wan X F. Codon O: Codon usage bias analysis within and across genomes. Nucleic Acids Res, 2007, 35:132-136.
pmid: 17537810
[17] Lu H, Zhao W M, Zheng Y, Wang H, Qi M, Yu X P. Analysis of synonymous codon usage bias in Chlamydia. Acta Biochim Biophys Sin(Shanghai), 2005, 37:1-10.
doi: 10.1093/abbs/37.1.1
[18] Boël G, Letso R, Neely H, Price W N, Wong K H, Su M, Luff J D, Valecha M, Everett J K, Acton T B, Xiao R, Montelione G T, Aalberts D P, Hunt J F. Codon influence on protein expression in E. coli correlates with mRNA levels. Nature, 2016, 529:358-363.
doi: 10.1038/nature16509
[19] Yan X, Hoek T A, Vale R D, Tanenbaum M E. Dynamics of translation of single mRNA molecules in vivo. Cell, 2016, 165:976-989.
doi: 10.1016/j.cell.2016.04.034
[20] Hanson G, Coller J. Translation and protein quality control: codon optimality, bias and usage in translation and mRNA decay. Nat Rev Mol Cell Biol, 2018, 19:20-30.
doi: 10.1038/nrm.2017.91
[21] Pan L L, Wang Y, Hu J H, Ding Z T, Li C. Analysis of codon use features of stearoyl-acyl carrier protein desaturase gene in Camellia sinensis. J Theor Biol, 2013, 334:80-86.
doi: 10.1016/j.jtbi.2013.06.006
[22] Pek H B, Klement M, Ang K S, Chung B K, Ow D S, Lee D Y. Exploring codon context bias for synthetic gene design of a thermostable invertase in Escherichia coli. Enzyme Microbial Technol, 2015, 75/76:57-63.
doi: 10.1016/j.enzmictec.2015.04.008
[23] Schopfer C R, Nasrallah M E, Nasrallah J B. The male determinant of self-incompatibility in Brassica. Science, 1999, 286:1697-1700.
pmid: 10576728
[24] Takayama S, Shimosato H, Shiba H, Funato M, Che F S, Watanabe M, Iwano M, Isogai A. Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature, 2001, 413:534-538.
doi: 10.1038/35097104
[25] Stein J C, Howlett B, Boyes D C, Nasrallah M E, Nasrallah J B. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci USA, 1991, 88:8816-8820.
doi: 10.1073/pnas.88.19.8816
[26] Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai A, Hinata K. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature, 2000, 403:913-916.
doi: 10.1038/35002628
[27] Stein J C, Nasrallah J B. A plant receptor-like gene, the S-locus receptor kinase of Brassica oleracea L., encodes a functional serine/threonine kinase. Plant Physiol, 1993, 101:1103-1106.
doi: 10.1104/pp.101.3.1103 pmid: 8310048
[28] Shimosato H, Yokota N, Shiba H, Iwano M, Entani T, Che F S, Watanabe M, Isogai A, Takayama S. Characterization of the SP11/SCR high affinity binding site involved in self/nonself recognition in Brassica self-incompatibility. Plant Cell, 2007, 19:107-117.
pmid: 17220204
[29] Nasrallah J B, Yu S M, Nasrallah M E. Self-incompatibility genes of Brassica oleracea: expression, isolation, and structure. Proc Natl Acad Sci USA, 1988, 85:5551-5555.
doi: 10.1073/pnas.85.15.5551
[30] Kusaba M, Nishio T. Comparative analysis of S haplotypes with very similar SLG alleles in Brassica rapa and Brassica oleracea. Plant J, 1999, 17:83-91.
pmid: 10069069
[31] Dixit R, Nasrallah M E, Nasrallah J B. Post-transcriptional maturation of the S receptor kinase of Brassica correlates with co-expression of the S-locus glycoprotein in the stigmas of two Brassica strains and in transgenic tobacco plants. Plant Physiol, 2000, 124:297-311.
pmid: 10982444
[32] Silva N F, Stone S L, Christie L N, Sulaman W, Nazarian K A P, Burnett L A, Arnoldo M A, Rothstein S J, Goring D R. Expression of the S receptor kinase in self-compatible Brassica napus cv. Westar leads to the allele-specific rejection of self-incompatible Brassica napus pollen. Mol Genet Genomics, 2001, 265:552-559.
pmid: 11405639
[33] Nasrallah J B, Nishio T, Nasrallah M E. The self-incompatibility genes of Brassica: expression and use in genetic ablation of floral tissues. Annu Rev Plant Physiol Plant Mol Biol, 1991, 42:393-422.
doi: 10.1146/arplant.1991.42.issue-1
[34] Ma R, Han Z F, Hu Z H, Lin G Z, Gong X Q, Zhang H Q, Nasrallah J B, Chai J J. Structural basis for specific self-incompatibility response in Brassica. Cell Res, 2016, 26:1320-1329.
doi: 10.1038/cr.2016.129
[35] Sato K, Nishio T, Kimura R, Kusaba M, Suzuki T, Hatakeyama K, Ockendon D J, Satta Y. Coevolution of the S-Locus genes SRK, SLG and SP11/SCR in Brassica oleracea and B. rapa. Genetics, 2002, 162:931-940.
doi: 10.1093/genetics/162.2.931
[36] Kim D S, Kim S. Identification of the S locus core sequences determining self-incompatibility and S multigene family from draft genome sequences of radish (Raphanus sativus L.). Euphytica, 2018, 214:16.
doi: 10.1007/s10681-017-2101-3
[37] Sharp P M, Li W H. An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol, 1986, 24:28-38.
pmid: 3104616
[38] Nasrullah I, Butt A M, Tahir S, Idrees M, Tong Y G. Genomic analysis of codon usage shows influence of mutation pressure, natural selection, and host features on Marburg virus evolution. BMC Evol Biol, 2015, 15:174.
doi: 10.1186/s12862-015-0456-4 pmid: 26306510
[39] Wang L Y, Xing H X, Yuan Y C, Wang X L, Saeed M, Tao J C, Feng W, Zhang G H, Song X L, Sun X Z. Genome-wide analysis of codon usage bias in four sequenced cotton species. PLoS One, 2018, 13:e0194372.
[40] Wong E H, Smith D K, Rabadan R, Peiris M, Poon L L. Codon usage bias and the evolution of influenza A viruses. codon usage biases of influenza virus. BMC Evol Biol, 2010, 10:253.
doi: 10.1186/1471-2148-10-253
[41] Singh R K, Pandey S P. Phylogenetic and evolutionary analysis of plant ARGONAUTES. Methods Mol Biol, 2017, 1640:267-294.
doi: 10.1007/978-1-4939-7165-7_20 pmid: 28608350
[42] Taylor T L, Dimitrov K M, Afonso C L. Genome-wide analysis reveals class and gene specific codon usage adaptation in avian paramyxoviruses 1. Infect Genet Evol, 2017, 50:28-37.
doi: S1567-1348(17)30046-1 pmid: 28189889
[43] Wright F. The ‘effective number of codons’ used in a gene. Gene, 1990, 87:23-29.
pmid: 2110097
[44] Comeron J M, Aguade M. An evaluation of measures of synonymous codon usage bias. J Mol Evol, 1998, 47:268-274.
pmid: 9732453
[45] Liu Q, Feng Y, Zhao X, Dong H, Xue Q. Synonymous codon usage bias in Oryza sativa. Plant Sci, 2004, 167:101-105.
doi: 10.1016/j.plantsci.2004.03.003
[46] Sueoka N. Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA, 1988, 85:2653-2657.
doi: 10.1073/pnas.85.8.2653
[47] 吴彦庆, 赵大球, 陶俊. 芍药花色调控基因的密码子使用模式及其影响因素分析. 中国农业科学, 2016, 49:2368-2378.
Wu Y Q, Zhao D Q, Tao J. Analysis of codon usage pattern of Paeonia lactiflora genes regulating flower color and its influence factors. Sci Agric Sin, 2016, 49:2368-2378 (in Chinese with English abstract).
[48] Chakraborty S, Deb B, Barbhuiya P A, Uddin A. Analysis of codon usage patterns and influencing factors in Nipah virus. Virus Res, 2019, 263:129-138.
doi: S0168-1702(18)30756-1 pmid: 30664908
[49] Sueoka N. Intrastrand parity rules of DNA base composition and usage biases of synonymous codons. J Mol Evol, 1995, 40:318-325.
pmid: 7723058
[50] Sueoka N. Translation-coupled violation of Parity Rule 2 in human genes is not the cause of heterogeneity of the DNA G+C content of third codon position. Gene, 1999, 238:53-58.
doi: 10.1016/S0378-1119(99)00320-0
[51] He Z, Gan H F, Liang X Y. Analysis of synonymous codon usage bias in potato virus M and its adaption to hosts. Viruses, 2019, 11:752.
doi: 10.3390/v11080752
[52] Paul P, Malakar A K, Chakraborty S. Compositional bias coupled with selection and mutation pressure drives codon usage in Brassica campestris genes. Food Sci Biotechnol, 2018, 27:725-733.
doi: 10.1007/s10068-017-0285-x
[53] Kumar N, Kulkarni D D, Lee B, Kaushik R, Bhatia S, Sood R, Pateriya A K, Bhat S, Singh V P. Evolution of codon usage bias in henipaviruses is governed by natural selection and is host- specific. Viruses, 2018, 10:64.
doi: 10.3390/v10020064
[54] Liu X S, Zhang Y G, Fang Y Z, Wang Y L. Patterns and influencing factor of synonymous codon usage in porcine circovirus. Virol J, 2012, 9:68.
doi: 10.1186/1743-422X-9-68
[55] Brule C E, Grayhack E J. Synonymous codons: choose wisely for expression. Trends Genet, 2017, 33:283-297.
doi: 10.1016/j.tig.2017.02.001
[56] Bellgard M, Schibeci D, Trifonov E, Gojobori T. Early detection of G+C differences in bacterial species inferred from the comparative analysis of the two completely sequenced Helicobacter pylori strains. J Mol Evol, 2001, 53:465-468.
pmid: 11675606
[57] Zhou J H, Ding Y Z, He Y, Chu Y F, Zhao P, Zhao P, Ma L Y, Wang X J, Li X R, Liu Y S. The effect of multiple evolutionary selections on synonymous codon usage of genes in the Mycoplasma bovis genome. PLoS One, 2014, 9:e108949.
[58] Murray E E, Lotzer J, Eberle M. Codon usage in plant genes. Nucleic Acids Res, 1989, 17:477-498.
pmid: 2644621
[59] Kawabe A. Miyashita N T. Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet Syst, 2003, 78:342-352.
[60] Uddin A, Paul N, Chakraborty S. The codon usage pattern of genes involved in ovarian cancer. Ann N Y Acad Sci, 2019, 1440:67-78.
doi: 10.1111/nyas.2019.1440.issue-1
[61] Luo W, Tian L, Gan Y D, Chen E L, Shen X J, Pan J B, Irwin D M, Chen R A, Shen Y Y. The fit of codon usage of human- isolated avian influenza A viruses to human. Infection,Genet Evol, 2020, 81:104181.
doi: 10.1016/j.meegid.2020.104181
[62] Yu X L, Liu J X, Li H Z, Liu B Y, Zhao B Q, Ning Z Y. Comprehensive analysis of synonymous codon usage bias for complete genomes and E2 gene of atypical porcine pestivirus. Biochem Genet, 2021, 59:799-812.
doi: 10.1007/s10528-021-10037-y
[63] Yu X L, Liu J X, Li H Z, Liu B Y, Zhao B Q, Ning Z Y. Comprehensive analysis of synonymous codon usage patterns and influencing factors of porcine epidemic diarrhea virus. Arch Virol, 2021, 166:157-165.
doi: 10.1007/s00705-020-04857-3
[64] Butt A M, Nasrullah I, Qamar R, Tong Y. Evolution of codon usage in Zika virus genomes is host and vector specific. Emerg Microbes Infect, 2016, 5:e107.
[65] Kumar N, Bera B C, Greenbaum B D, Bhatia S, Sood R, Selvaraj P, Anand T, Tripathi B N, Virmani N. Revelation of influencing factors in overall codon usage bias of equine influenza viruses. PLoS One, 2016, 11:e0154376.
[66] Wang X, Xu W H, Fan K W, Chiu H C, Huang C Q. Codon usage bias in the H gene of canine distemper virus. Microbial Pathog, 2020, 149:104511.
doi: 10.1016/j.micpath.2020.104511
[67] Chen Y, Shi Y, Deng H, Gu T, Xu J, Ou J, Jiang Z, Jiao Y, Zou T, Wang C. Characterization of the porcine epidemic diarrhea virus codon usage bias. Infect Genet Evol, 2014, 28:95-100.
doi: 10.1016/j.meegid.2014.09.004 pmid: 25239728
[68] Zhang X, Cai Y, Zhai X, Liu J, Zhao W, Ji S, Su S, Zhou J. Comprehensive analysis of codon usage on rabies virus and other lyssaviruses. Int J Mol Sci, 2018, 19:2397.
doi: 10.3390/ijms19082397
[69] Cristina J, Fajardo A, Soñora M, Moratorio G, Musto H. A detailed comparative analysis of codon usage bias in Zika virus. Virus Res, 2016, 223:147-152.
doi: 10.1016/j.virusres.2016.06.022 pmid: 27449601
[70] Deb B, Uddin A, Chakraborty S. Composition, codon usage pattern, protein properties, and influencing factors in the genomes of members of the family Anelloviridae. Arch Virol, 2021, 166:461-474.
doi: 10.1007/s00705-020-04890-2
[71] Zhang W J, Jie Z, Li Z F, Wang L, Xun G, Zhong Y. Comparative analysis of codon usage patterns among mitochondrion, chloroplast and nuclear genes in Triticum aestivum L. J Integr Plant Biol, 2007, 49:246-254.
doi: 10.1111/jipb.2007.49.issue-2
[72] Liu X Y, Li Y, Ji K K, Zhu J, Ling P, Zhou T, Fan L Y, Xie S Q. Genome-wide codon usage pattern analysis reveals the correlation between codon usage bias and gene expression in Cuscuta australis. Genomics, 2020, 112:2695-2702.
doi: 10.1016/j.ygeno.2020.03.002
[73] Chen H X, Sun S C, Norenburg J L, Sundberg P. Mutation and selection cause codon usage and bias in mitochondrial genomes of ribbon worms (Nemertea). PLoS One, 2014, 9:e85631.
[74] Bera B C, Virmani N, Kumar N, Anand T, Pavulraj S, Rash A, Elton D, Rash N, Bhatia S, Sood R, Singh R K, Tripathi B N. Genetic and codon usage bias analyses of polymerase genes of equine influenza virus and its relation to evolution. BMC Genomics, 2017, 18:652.
doi: 10.1186/s12864-017-4063-1
[75] De Amicis F, Marchetti S. Intercodon dinucleotides affect codon choice in plant genes. Nucleic Acids Res, 2000, 28:3339-3345.
pmid: 10954603
[76] Sharp P M, Cowe E, Higgins D G, Shields D C, Wolfe K H, Wright F. Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens: a review of the considerable within species diversity. Nucleic Acids Res, 1988, 16:8207-8211.
pmid: 3138659
[77] Zhou H, Wang H, Huang I F, Naylor M, Clifford P. Heterogeneity in codon usages of sobemovirus genes. Arch Virol, 2005, 150:1591-1605.
doi: 10.1007/s00705-005-0510-4 pmid: 15834656
[78] Miwa H, Odrzykoski I J, Matsui A, Hasegawa M, Murakami N. Adaptive evolution of rbcL in Conocephalum (Hepaticae, bryophytes). Gene, 2009, 441:169-175.
doi: 10.1016/j.gene.2008.11.020
[79] Zhao Y C, Zheng H, Xu A Y, Yan D, H Jiang Z J, Qi Q, Sun J C. Analysis of codon usage bias of envelope glycoprotein genes in nuclear polyhedrosis virus (NPV) and its relation to evolution. BMC Genomics, 2016, 17:677.
doi: 10.1186/s12864-016-3021-7
[80] Christianson M. Codon usage patterns distort phylogenies from or of DNA sequences. Am J Bot, 2005, 92:1221-1233.
doi: 10.3732/ajb.92.8.1221 pmid: 21646144
[81] Liu H, He R, Zhang H, Huang Y, Tian M, Zhang J. Analysis of synonymous codon usage in Zea mays. Mol Biol Rep, 2010, 37:677-684.
doi: 10.1007/s11033-009-9521-7
[82] Fraser H B, Hirsh A E, Wall D P, Eisen M B. Coevolution of gene expression among interacting proteins. Proc Natl Acad Sci USA, 2004, 101:9033-9038.
doi: 10.1073/pnas.0402591101
[83] 朱利泉, 周燕. 甘蓝自交不亲和性信号传导元件与传导过程. 作物学报, 2015, 41:1-14.
doi: 10.3724/SP.J.1006.2015.00001
Zhu L Q, Zhou Y. Protein elements and signal transduction process of self-incompatibility in Brassica oleracea. Acta Agron Sin, 2015, 41:1-14 (in Chinese with English abstract).
[84] Lithwick G, Margalit H. Relative predicted protein levels of functionally associated proteins are conserved across organisms. Nucleic Acids Res, 2005, 33:1051-1057.
pmid: 15718304
[85] Dilucca M, Cimini G, Forcelloni S, Giansanti A. Co-evolution between codon usage and protein-protein interaction in bacteria. Gene, 2021, 778:145475.
doi: 10.1016/j.gene.2021.145475
[86] Najafabadi H S, Goodarzi H. Salavati R. Universal function-specificity of codon usage. Nucleic Acids Res, 2009, 37:7014-7023.
doi: 10.1093/nar/gkp792 pmid: 19773421
[87] He W, Zhang H, Zhang Y, Wang R, Lu S, Ji Y, Liu C, Yuan P, Su S. Codon usage bias in the N gene of rabies virus. Infect Genet Evol, 2017, 54:458-465.
doi: 10.1016/j.meegid.2017.08.012
[88] Luo W, Li Y, Yu S, Shen X, Tian L, Irwin D M, Shen Y. Better fit of codon usage of the polymerase and nucleoprotein genes to the chicken host for H7N9 than H9N2 AIVs. J Infect, 2019, 79:174-187.
[89] Greenbaum B D, Levine A J, Bhanot G, Rabadan R. Patterns of evolution and host gene mimicry in influenza and other RNA viruses. PLoS Pathog, 2008, 4:e1000079.
[1] XIE Qin-Qin, ZUO Tong-Hong, HU Deng-Ke, LIU Qian-Ying, ZHANG Yi-Zhong, ZHANG He-Cui, ZENG Wen-Yi, YUAN Chong-Mo, ZHU Li-Quan. Molecular cloning and expression analysis of BoPUB9 in self-incompatibility Brassica oleracea [J]. Acta Agronomica Sinica, 2022, 48(1): 108-120.
[2] ZUO Xiang-Jun, FANG Peng-Peng, LI Jia-Na, QIAN Wei, MEI Jia-Qin. Characterization of aphid-resistance of a hairy wild Brassica oleracea taxa, B. incana [J]. Acta Agronomica Sinica, 2021, 47(6): 1109-1113.
[3] Tong-Hong ZUO, He-Cui ZHANG, Qian-Ying LIU, Xiao-Ping LIAN, Qin-Qin XIE, Deng-Ke HU, Yi-Zhong ZHANG, Yu-Kui WANG, Xiao-Jing BAI, Li-Quan ZHU. Molecular cloning and expression analysis of BoGSTL21 in self-incompatibility Brasscia oleracea [J]. Acta Agronomica Sinica, 2020, 46(12): 1850-1861.
[4] WANG Yu-Kui,ZHANG He-Cui,BAI Xiao-Jing,LIAN Xiao-Ping,SHI Song-Mei,LIU Qian-Ying,ZUO Tong-Hong,ZHU Li-Quan. Characteristics and expression analysis of BoPINs family genes in Brassica oleracea [J]. Acta Agronomica Sinica, 2019, 45(8): 1270-1278.
[5] Fang YUE,Lei WANG,Yan-Gui CHEN,Xiao-Xia XIN,Qin-Fei LI,Jia-Qin MEI,Zhi-Yong XIONG,Wei QIAN. A new method of synthesizing Brassica napus by crossing B. oleracea with the allohexaploid derived from hybrid between B. napus and B. rapa [J]. Acta Agronomica Sinica, 2019, 45(2): 188-195.
[6] Xiao-Jing BAI,Xiao-Ping LIAN,Yu-Kui WANG,He-Cui ZHANG,Qian-Ying LIU,Tong- Hong ZUO,Yi-Zhong ZHANG,Qin-Qin XIE,Deng-Ke HU,Xue-Song REN,Jing ZENG,Shao-Lan LUO,Min PU,Li-Quan ZHU. Cloning and analysis of BoCDPK14 in self-incompatibility Brasscia olerace [J]. Acta Agronomica Sinica, 2019, 45(12): 1773-1783.
[7] Shao-Lan LUO,Xiao-Ping LIAN,Min PU,Xiao-Jing BAI,Yu-Kui WANG,Jing ZENG,Song-Mei SHI,He-Cui ZHANG,Li-Quan ZHU. Molecular Cloning, Location and Expression Analysis of Brasscia oleracea Zinc Finger Protein Transcription Factor BoC2H2 [J]. Acta Agronomica Sinica, 2018, 44(11): 1650-1660.
[8] Yun-Fei LIANG, Lin-Cheng ZHANG, Quan-Ming PU, Zhen-Ze LEI, Song-Mei SHI, Yu-Peng JIANG, Xue-Song REN, Qi-Guo GAO. Cloning of BoLH27 Gene from Cabbage and Phenotype Analysis of Transgenic Cabbage [J]. Acta Agronomica Sinica, 2018, 44(03): 397-404.
[9] WANG Rui-Yun,JI Xu,LU Ping,LIU Min-Xuan,XU Yue,WANG Lun,WANG Hai-Gang,QIAO Zhi-Jun. Analysis of Genetic Diversity in Common Millet (Panicum miliaceum) Using Fluorescent SSR in China [J]. Acta Agron Sin, 2017, 43(04): 530-548.
[10] HU Yi-Bo, YANG Xiu-Shi, LU Ping*,REN Gui-Xing*. Diversity and Correlation of Quality Traits in Quinoa Germplasms from North China [J]. Acta Agron Sin, 2017, 43(03): 464-470.
[11] XU Ning,CHEN Bing-Xu,WANG Ming-Hai,BAO Shu-Ying,WANG Gui-Fang,GUO Zhong-Xiao. Identification of Alkali Tolerance of Mungbean Germplasm Resources during Germination [J]. Acta Agron Sin, 2017, 43(01): 112-121.
[12] WU Qi,ZHOU Yu-Fei,GAO Yue,ZHANG Jiao,CHEN Bing-Ru,XU Wen-Juan,HUANG Rui-Dong. Screening and Identification for Drought Resistance during Germination in Sorghum Cultivars [J]. Acta Agron Sin, 2016, 42(08): 1233-1246.
[13] ZHANG Yang,HU Zhong-Ying,ZHAO Yue-Ming,LI Na,XIE Li-Nan. DNA Methylation Dynamic Analysis of Self Compatible Line and Self-Incompatible Line of Brassica oleracea var. acephala at Seed Germination Stage [J]. Acta Agron Sin, 2016, 42(04): 532-539.
[14] LIU Ying,ZHANG Qiao-Feng,FU Bi-Sheng,CAI Shi-Bin,JIANG Yan-Jie,ZHANG Zhi-Liang,DENG Yuan-Yu,WU Ji-Zhong,DAI Ting-Bo. Genetic Diversity of Wheat Germplasm Resistant to Sharp Eyespot and Genotyping of Resistance Loci Using SSR Markers [J]. Acta Agron Sin, 2015, 41(11): 1671-1681.
[15] LI Long,WANG Lan-Fen,WU Jing,JING Rui-Lian,WANG Shu-Min*. Identification of Drought Resistence at Seedlings Stage in Common Bean (Phaseolus vulgaris L.) Varieties [J]. Acta Agron Sin, 2015, 41(06): 963-971.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!