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


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)


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"

Gene accession ID
Gene name
Gene accession ID
Gene name
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"

Nucleotide composition and ENC
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"

Amino acid
相对同义密码子RSCU 氨基酸
Amino acid
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"

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
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*
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."

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