A comparative study of the evolution and codon usage bias in WOX gene family of three Camellia sinensis cultivars

WANG Zhanjun, WU Ziqi, WANG Zhaoxia, OU Zulan, LI Jie, CAI Qianwen, XU Zhongdong, ZHANG Zhaoliang

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2022, Vol. 46 ›› Issue (2) : 71-80.

PDF(1705 KB)
PDF(1705 KB)
JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2022, Vol. 46 ›› Issue (2) : 71-80. DOI: 10.12302/j.issn.1000-2006.202108049

A comparative study of the evolution and codon usage bias in WOX gene family of three Camellia sinensis cultivars

Author information +
History +

Abstract

【Objective】The WOX gene family plays an important molecular regulatory role in model plant tissue culture. Phylogeny studies and research on the codon usage bias in the WOX gene family in non-model plants are helpful for exploring genetic evolution and gene expression characteristics, which serve as a guideline for establishing a transgenic system.【Method】In this study, bioinformatics were used to identify the WOX genes among all coding sequences of three Camellia sinensis cultivars. The evolutionary patterns were analyzed using ClustalX 2.1 and MEGA X software. The codon usage index of the coding sequence of the WOX gene was analyzed, and the codon usage pattern and the source of codon variation were explored using Perl language, Codon W1.4.2, and SPSS 23.0. The main factors affecting codon usage bias were analyzed based on the results of ENc-GC3s, a PR2-plot analysis, and a neutral analysis.【Result】A total of 42 WOX members were identified in this study, of which 11 were CSA, 18 were CSS and 13 were DASZ. The phylogenetic analysis revealed that the evolution of WOX genes of the three Camellia sinensis cultivars is highly conserved. The codon bias analysis revealed that the codons of WOX genes preferred to use A/T and end with A/T in the three Camellia sinensis cultivars; the codon usage patterns of WOX genes in CSA and DASZ are similar, indicating that they are closely related. When CSA and CSS are used as transgenic receptors, individual codons in WOX genes of three Camellia sinensis cultivars need to be optimized. Nicotiana tabacum is the best heterologous expression receptor for WOX genes of three Camellia sinensis cultivars. ENc-GC3s mapping the PR2 analysis, and the neutrality analysis indicate that the natural selection is the main reason for the codon usage bias of WOX genes in the three Camellia sinensis cultivars.【Conclusion】This study showed that WOX genes of three Camellia sinensis cultivars are evolutionarily conserved, codons prefer to use A/T and end with A/T, and the codon usage bias is mainly due to the natural selection. The results reveal the optimization information of codons when transforming tea plants, and tobacco is the best heterologous expression receptor.

Key words

Camellia sinensis / WOX gene family / evolutionary analysis / codon usage bias / transgene expression

Cite this article

Download Citations
WANG Zhanjun , WU Ziqi , WANG Zhaoxia , et al . A comparative study of the evolution and codon usage bias in WOX gene family of three Camellia sinensis cultivars[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY. 2022, 46(2): 71-80 https://doi.org/10.12302/j.issn.1000-2006.202108049

References

[1]
XIA E H, ZHANG H B, SHENG J, et al. The tea tree genome provides insights into tea flavor and independent evolution of caffeine biosynthesis[J]. Mol Plant, 2017, 10(6):866-877. DOI: 10.1016/j.molp.2017.04.002.
[2]
WEI C L, YANG H, WANG S B, et al. Draft genome sequence of Camellia sinensis var.sinensis provides insights into the evolution of the tea genome and tea quality[J]. Proc Natl Acad Sci USA, 2018, 115(18):E4151-E4158. DOI: 10.1073/pnas.1719622115.
[3]
ZHANG W Y, ZHANG Y J, QIU H J, et al. Genome assembly of wild tea tree DASZ reveals pedigree and selection history of tea varieties[J]. Nat Commun, 2020, 11(1):3719. DOI: 10.1038/s41467-020-17498-6.
[4]
SINGH K, PAUL A, KUMAR S, et al. Cloning and differential expression of QM like protein homologue from tea[Camellia sinensis (L.) O.Kuntze][J]. Mol Biol Rep, 2009, 36(5):921-927. DOI: 10.1007/s11033-008-9264-x.
[5]
CAO Y P, HAN Y H, MENG D D, et al. Genome-wide analysis suggests the relaxed purifying selection affect the evolution of WOX genes in Pyrus bretschneideri,Prunus persica,Prunus mume,and Fragaria vesca[J]. Front Genet, 2017, 8:78. DOI: 10.3389/fgene.2017.00078.
[6]
WU X L, CHORY J, WEIGEL D. Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development[J]. Dev Biol, 2007, 309(2):306-316. DOI: 10.1016/j.ydbio.2007.07.019.
[7]
GALLOIS J L, NORA F R, MIZUKAMI Y, et al. WUSCHEL induces shoot stem cell activity and developmental plasticity in the root meristem[J]. Genes Dev, 2004, 18(4):375-380. DOI: 10.1101/gad.291204.
[8]
GORDON S P, HEISLER M G, REDDY G V, et al. Pattern formation during de novo assembly of the Arabidopsis shoot meristem[J]. Development, 2007, 134(19):3539-3548. DOI: 10.1242/dev.010298.
[9]
WANG P J, GUO Y C, CHEN X J, et al. Genome-wide identification of WOX genes and their expression patterns under different hormone and abiotic stress treatments in tea plant (Camellia sinensis)[J]. Trees, 2019, 33(4):1129-1142. DOI: 10.1007/s00468-019-01847-0.
[10]
LIU H M, HE R, ZHANG H Y, et al. Analysis of synonymous codon usage in Zea mays[J]. Mol Biol Rep, 2010, 37(2):677-684. DOI: 10.1007/s11033-009-9521-7.
[11]
PERLAK F J, DEATON R W, ARMSTRONG T A, et al. Insect resistant cotton plants[J]. Biotechnology (N Y), 1990, 8(10):939-943. DOI: 10.1038/nbt1090-939.
[12]
张乐, 金龙国, 罗玲, 等. 大豆基因组和转录组的核基因密码子使用偏好性分析[J]. 作物学报, 2011, 37(6):965-974.
ZHANG L, JIN L G, LUO L, et al. Analysis of nuclear gene codon bias on soybean genome and transcriptome[J]. Acta Agron Sin, 2011, 37(6):965-974. DOI: 10.3724/SP.J.1006.2011.00965.
[13]
时慧, 王玉, 杨路成, 等. 茶树抗寒调控转录因子ICE1密码子偏性分析[J]. 园艺学报, 2012, 39(7):1341-1352.
SHI H, WANG Y, YANG L C, et al. Analysis of codon bias of the cold regulated transcription factor ICE1 in tea plant[J]. Acta Hortic Sin, 2012, 39(7):1341-1352. DOI: 10.16420/j.issn.0513-353x.2012.07.002.
[14]
郭秀丽, 王玉, 杨路成, 等. 茶树CBF1基因密码子使用特性分析[J]. 遗传, 2012, 34(12):1614-1623.
GUO X L, WANG Y, YANG L C, et al. Analysis of codon use features of CBF gene in Camellia sinensis[J]. Hereditas, 2012, 34(12):1614-1623. DOI: 10.3724/SP.J.1005.2012.01614.
[15]
PAN L L, WANG Y, HU J H, et al. Analysis of codon use features of stearoyl-acyl carrier protein desaturase gene in Camellia sinensis[J]. J Theor Biol, 2013, 334:80-86. DOI: 10.1016/j.jtbi.2013.06.006.
[16]
ALTSCHUL S F, MADDEN T L, SCHÄFFER A A, et al. Gapped BLAST and PSI-BLAST:a new generation of protein database search programs[J]. Nucleic Acids Res, 1997, 25(17):3389-3402. DOI: 10.1093/nar/25.17.3389.
[17]
TANG F, CHEN N Z, ZHAO M L, et al. Identification and functional divergence analysis of WOX gene family in paper mulberry[J]. Int J Mol Sci, 2017, 18(8):1782. DOI: 10.3390/ijms18081782.
[18]
ARTIMO P, JONNALAGEDDA M, ARNOLD K, et al. ExPASy:SIB bioinformatics resource portal[J]. Nucleic Acids Res, 2012,40(Web Server issue):597-603. DOI: 10.1093/nar/gks400.
[19]
CHOU K C, SHEN H B. Cell-PLoc 2.0:an improved package of web-servers for predicting subcellular localization of proteins in various organisms[J]. Nat Sci, 2010, 2(10):1090-1103. DOI: 10.4236/ns.2010.210136.
[20]
SHIELDS D C, SHARP P M. Synonymous codon usage in Bacillus subtilis reflects both translational selection and mutational biases[J]. Nucleic Acids Res, 1987, 15(19):8023-8040. DOI: 10.1093/nar/15.19.8023.
[21]
ZHOU M, TONG C F, SHI J S. Analysis of codon usage between different poplar species[J]. J Genet Genomics, 2007, 34(6):555-561. DOI: 10.1016/S1673-8527(07)60061-7.
[22]
Romero H, Zavala A, Musto H, Bernardi G. The influence of translational selection on codon usage in fishes from the family Cyprinidae[J]. Gene, 2003, 317:141-147. DOI: 10.1016/S0378-1119(03)00701-7.
[23]
ZHOU M, TONG C F, SHI J S. A preliminary analysis of synonymous codon usage in poplar species[J]. Journal of Plant Physiology & Molecular Biology, 2007, 33(4):285-293. DOI: 10.2471/BLT.13.118778.
[24]
MAJEED A, KAUR H, BHARDWAJ P. Selection constraints determine preference for A/U-ending codons in Taxus contorta[J]. Genome, 2020, 63(4):215-224. DOI: 10.1139/gen-2019-0165.
[25]
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[J]. Gene, 1999, 238(1):53-58. DOI: 10.1016/s0378-1119(99)00320-0.
[26]
FENNOY S L, BAILEY-SERRES J. Synonymous codon usage in Zea mays L.nuclear genes is varied by levels of C and G-ending codons[J]. Nucleic Acids Res, 1993, 21(23):5294-5300. DOI: 10.1093/nar/21.23.5294.
[27]
CHANG Y Y, SONG X B, ZHANG Q X, et al. Genome-wide identification of WOX gene family and expression analysis during rejuvenational rhizogenesis in walnut (Juglans regia L.)[J]. Forests, 2019, 11(1):16. DOI: 10.3390/f11010016.
[28]
VAN DER GRAAFF E, LAUX T, RENSING S A. The WUS homeobox-containing (WOX) protein family[J]. Genome Biol, 2009, 10(12):248. DOI: 10.1186/gb-2009-10-12-248.
[29]
NARDMANN J, WERR W. The shoot stem cell niche in angiosperms:expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono-and dicot evolution[J]. Mol Biol Evol, 2006, 23(12):2492-2504. DOI: 10.1093/molbev/msl125.
[30]
LIU B B, WANG L, ZHANG J, et al. WUSCHEL-related homeobox genes in Populus tomentosa:diversified expression patterns and a functional similarity in adventitious root formation[J]. BMC Genomics, 2014, 15:296. DOI: 10.1186/1471-2164-15-296.
[31]
李晓旭, 刘成, 李伟, 等. 番茄WOX转录因子家族的鉴定及其进化、表达分析[J]. 遗传, 2016, 38(5):444-460.
LI X X, LIU C, LI W, et al. Genome-wide identification,phylogenetic analysis and expression profiling of the WOX family genes in Solanum lycopersicum[J]. Hereditas, 2016, 38(5):444-460. DOI: 10.16288/j.yczz.15-499.
[32]
王占军, 李豹, 姜行舟, 等. 两种茶树全基因组数据的密码子偏好性比较分析[J]. 中国细胞生物学学报, 2018, 40(12):2028-2039.
WANG Z J, LI B, JIANG X Z, et al. Comparative analysis of the codon preference patterns in two species of Camellia sinensis based on genome data[J]. Chin J Cell Biol, 2018, 40(12):2028-2039.
[33]
WANG Z J, WANG G Y, CAI Q W, et al. Genomewide comparative analysis of codon usage bias in three sequenced Jatropha curcas[J]. J Genet, 2021, 100(1):1-13. DOI: 10.1007/s12041-021-01271-9.
[34]
LI N, SUN M H, JIANG Z S, et al. Genome-wide analysis of the synonymous codon usage patterns in apple[J]. J Integr Agric, 2016, 15(5):983. DOI: 10.1016/S2095-3119(16)61333-3.
[35]
SONG H, LIU J, CHEN T, et al. Synonymous codon usage pattern in model legume Medicago truncatula[J]. J Integr Agric, 2018, 17(9):2074-2081. DOI: 10.1016/S2095-3119(18)61961-6.
[36]
ADITAMA R, TANJUNG Z A, SUDANIA W M, et al. Analysis of codon usage bias reveals optimal codons in Elaeis guineensis[J]. Biodiversitas, 2020, 21(11):5311-5337. DOI: 10.13057/biodiv/d211138.
[37]
李晓旭, 郭存, 蒲文宣, 等. 普通烟草WOX转录因子家族的全基因组鉴定及分析[J]. 中国烟草学报, 2021, 27(1):90-100.
LI X X, GUO C, PU W X, et al. Genome-wide identification and systemic analysis of WOX family genes in tobacco[J]. Acta Tabacaria Sin, 2021, 27(1):90-100. DOI: 10.16472/j.chinatobacco.2020.t0039.
PDF(1705 KB)

Accesses

Citation

Detail

Sections
Recommended
The full text is translated into English by AI, aiming to facilitate reading and comprehension. The core content is subject to the explanation in Chinese.

/