

FOLLOWUS
College of Pharmacy, Heze University, Heze 274015, China
lys832000@163.com
收稿:2026-01-26,
录用:2026-03-25,
网络首发:2026-10-19,
Scan QR Code
Rui XU, Xinyue GUAN, Jing LIU, 等. Comprehensive analysis of chloroplast genomes from 15 mangrove species (Rhizophoraceae): codon usage, phylogenetic relationships, and evolutionary insights[J/OL]. 海洋湖沼学报(英文), 2026,1-16.
XU Rui,GUAN Xinyue,LIU Jing,et al.Comprehensive analysis of chloroplast genomes from 15 mangrove species (Rhizophoraceae): codon usage, phylogenetic relationships, and evolutionary insights[J].Journal of Oceanology and Limnology,
Rui XU, Xinyue GUAN, Jing LIU, 等. Comprehensive analysis of chloroplast genomes from 15 mangrove species (Rhizophoraceae): codon usage, phylogenetic relationships, and evolutionary insights[J/OL]. 海洋湖沼学报(英文), 2026,1-16. DOI: 10.1007/s00343-026-6037-0.
XU Rui,GUAN Xinyue,LIU Jing,et al.Comprehensive analysis of chloroplast genomes from 15 mangrove species (Rhizophoraceae): codon usage, phylogenetic relationships, and evolutionary insights[J].Journal of Oceanology and Limnology, DOI:.
Mangrove plants
serving as critical blue carbon ecosystems and biodiversity hotspots
play critical roles in coastal protection
water purification
and climate change mitigation. In this paper
we present the first comprehensive analysis of chloroplast genomes from 15 mangrove species within the Rhizophoraceae family
with particular emphasis on their codon usage bias (CUB)
phylogenetic connections
and evolutionary dynamics. The total GC contents of protein-coding genes (PCGs) span from 36.79% to 38.13%
with a distribution trend of 50%
>
1
st
-site GC (GC1)
>
2
nd
-site GC (GC2)
>
total GC (GCall)
>
3
rd
-site GC (GC3)
>
synonymous codon 3
rd
GC (GC3s). The average values of effective number of codons (ENC) range from 46.43 to 47.18
reflecting a relatively weak CUB across the genomes. This bias is shaped by both mutational pressure and natural selection
with mutation exerting a more significant influence. We identified 13–19 optimal codons across these species
with ACU
AUU
CAA
CGU
GGU
GUA
UGC
and UUA being the most common optimal codons. Among all the genes analyzed
the
rps14
gene demonstrated the strongest CUB (ENC
<
35)
primarily driven by natural selection that optimizes its expression to ensure the efficient and accurate synthesis of the ribosome
whereas
rps18
gene exhibited clear signals of positive selection across all species against their terrestrial relative by the ratio of non-synonymous and synonymous substitution (Ka/Ks) analysis
suggesti
ng it may be undergoing potential adaptive evolution within Rhizophoraceae mangrove species. Phylogenetic analysis based on common coding sequences (CDSs)
concatenated sequences of
rps14
and
rps18
and relative synonymous codon usage (RSCU) values strongly supported monophyletic groups of four true mangrove genera. This study elucidated the synonymous codon usage patterns within the Rhizophoraceae family
offering valuable insights into their phylogenetic relationships
evolutionary processes
and potential applications in genetic engineering of Rhizophoraceae mangrove species.
Akram H , Hussain S , Mazumdar P et al . 2023 . Mangrove health: a review of functions, threats, and challenges associated with mangrove management practices . Forests , 14 ( 9 ): 1698 , https://doi.org/10.3390/f14091698 https://doi.org/10.3390/f14091698 .
Asaf S , Khan A L , Numan M et al . 2021 . Mangrove tree ( Avicennia marina ): insight into chloroplast genome evolutionary divergence and its comparison with related species from family Acanthaceae . Scientific Reports , 11 ( 1 ): 3586 , https://doi.org/10.1038/s41598-021-83060-z https://doi.org/10.1038/s41598-021-83060-z .
Camiolo S , Melito S , Porceddu A . 2015 . New insights into the interplay between codon bias determinants in plants . DNA Research , 22 ( 6 ): 461 - 470 , https://doi.org/10.1093/dnares/dsv027 https://doi.org/10.1093/dnares/dsv027 .
Chan C , Pham P , Dedon P C et al . 2018 . Lifestyle modifications: coordinating the tRNA epitranscriptome with codon bias to adapt translation during stress responses . Genome Biology , 19 ( 1 ): 228 , https://doi.org/10.1186/s13059-018-1611-1 https://doi.org/10.1186/s13059-018-1611-1 .
Chen J , Ma W Q , Hu X W et al . 2023 . Synonymous codon usage bias in the chloroplast genomes of 13 oil-tea Camellia samples from South China . Forests , 14 ( 4 ): 794 , https://doi.org/10.3390/f14040794 https://doi.org/10.3390/f14040794 .
Clarke R T , Greenacre M J . 1985 . Theory and applications of correspondence analysis . Journal of Animal Ecology , 54 ( 3 ): 1031 , https://doi.org/10.2307/4399 https://doi.org/10.2307/4399 .
Duret L , Mouchiroud D . 1999 . Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis , Drosophila , and Arabidopsi s . Proceedings of the National Academy of Sciences of the United States of America , 96 ( 8 ): 4482 - 4487 , https://doi.org/10.1073/pnas.96.8.4482 https://doi.org/10.1073/pnas.96.8.4482 .
Fages-Lartaud M , Hundvin K , Hohmann-Marriott M F . 2022 . Mechanisms governing codon usage bias and the implications for protein expression in the chloroplast of Chlamydomonas reinhardtii . The Plant Journal , 112 ( 4 ): 919 - 945 , https://doi.org/10.1111/tpj.15970 https://doi.org/10.1111/tpj.15970 .
Fang J , Qin L M , Liu H N et al . 2025 . Analysis of codon usage bias of 30 chloroplast genomes in Ulva (Ulvophyceae, Chlorophyta) . Genes , 16 ( 5 ): 608 , https://doi.org/10.3390/genes16050608 https://doi.org/10.3390/genes16050608 .
Fang Z S , Li D F , Murong H E et al . 2024 . Comparative plastome analysis between endangered mangrove species Acanthus ebracteatus and Acanthus relatives provides insights into its origin and adaptive evolution . Ecology and Evolution , 14 ( 11 ): e 70566 , https://doi.org/10.1002/ece3.70566 https://doi.org/10.1002/ece3.70566 .
Gao W , Chen X D , He J et al . 2024 . Intraspecific and interspecific variations in the synonymous codon usage in mitochondrial genomes of 8 Pleurotus strains . BMC Genomics , 25 ( 1 ): 456 , https://doi.org/10.1186/s12864-024-10374-3 https://doi.org/10.1186/s12864-024-10374-3 .
Geng X S , Huang N , Zhu Y L et al . 2022 . Codon usage bias analysis of the chloroplast genome of cassava . South African Journal of Botany , 151 : 970 - 975 , https://doi.org/10.1016/j.sajb.2022.11.022 https://doi.org/10.1016/j.sajb.2022.11.022 .
Gingold H , Dahan O , Pilpel Y . 2012 . Dynamic changes in translational efficiency are deduced from codon usage of the transcriptome . Nucleic Acids Research , 40 ( 20 ): 10053 - 10063 , https://doi.org/10.1093/nar/gks772 https://doi.org/10.1093/nar/gks772 .
Hameed A , Ahmed M Z , Hussain T et al . 2021 . Effects of salinity stress on chloroplast structure and function . Cells , 10 ( 8 ): 2023 , https://doi.org/10.3390/cells10082023 https://doi.org/10.3390/cells10082023 .
Han K , Shi C C , Li L W et al . 2020 . Lineage-specific evolution of mangrove plastid genomes . The Plant Genome , 13 ( 2 ): e 20019 , https://doi.org/10.1002/tpg2.20019 https://doi.org/10.1002/tpg2.20019 .
Hershberg R , Petrov D A . 2008 . Selection on codon bias . Annual Review of Genetics , 42 : 287 - 299 , https://doi.org/10.1146/annurev.genet.42.110807.091442 https://doi.org/10.1146/annurev.genet.42.110807.091442 .
Howai N . 2023 . Mangrove ecosystem services in Tobago: challenges, uses and future prospects . Farm and Business-The Journal of the Caribbean Agro-Economic Society , 15 ( 1 ): 10 - 21 , https://doi.org/10.22004/ag.econ.339780 https://doi.org/10.22004/ag.econ.339780 .
Hu X , Li Y Q , Meng F X et al . 2024 . Analysis of chloroplast genome characteristics and codon usage bias in 14 species of Annonaceae . Functional & Integrative Genomics , 24 ( 3 ): 109 , https://doi.org/10.1007/s10142-024-01389-w https://doi.org/10.1007/s10142-024-01389-w .
Juncosa A M , Tomlinson P B . 1988 . Systematic comparison and some biological characteristics of Rhizophoraceae and Anisophylleaceae . Annals of the Missouri Botanical Garden , 75 : 1296 - 1318 , https://doi.org/10.2307/2399287 https://doi.org/10.2307/2399287 .
Kelleway J J , Saintilan N , Macreadie P I et al . 2016 . Seventy years of continuous encroachment substantially increases 'blue carbon' capacity as mangroves replace intertidal salt marshes . Global Change Biology , 22 ( 3 ): 1097 - 1109 , https://doi.org/10.1111/gcb.13158 https://doi.org/10.1111/gcb.13158 .
Kirsch W , Seyer P , Herrmann R G . 1986 . Nucleotide sequence of the clustered genes for two P 700 chlorophyll a apoproteins of the photosystem I reaction center and the ribosomal protein S14 of the spinach plastid chromosome . Current Genetics , 10 ( 11 ): 843 - 855 , https://doi.org/10.1007/BF00418531 https://doi.org/10.1007/BF00418531 .
Lee S Y , Primavera J H , Dahdouh-Guebas F et al . 2014 . Ecological role and services of tropical mangrove ecosystems: a reassessment . Global Ecology and Biogeography , 23 ( 7 ): 726 - 743 , https://doi.org/10.1111/geb.12155 https://doi.org/10.1111/geb.12155 .
Lelekami M A , Pahlevani M H , Zaynali Nezhad K et al . 2025 . Transcriptome and network analysis pinpoint ABA and plastid ribosomal proteins as main contributors to salinity tolerance in the rice variety, CSR28 . PLoS One , 20 ( 4 ): e 0321181 , https://doi.org/10.1371/journal.pone.0321181 https://doi.org/10.1371/journal.pone.0321181 .
Li N , Li Y Y , Zheng C C et al . 2016 . Genome-wide comparative analysis of the codon usage patterns in plants . Genes & Genomics , 38 ( 8 ): 723 - 731 , https://doi.org/10.1007/s13258-016-0417-3 https://doi.org/10.1007/s13258-016-0417-3 .
Li T T , Ma Z , Ding T M et al . 2024 . Codon usage bias and phylogenetic analysis of chloroplast genome in 36 gracilariaceae species . Functional & Integrative Genomics , 24 ( 2 ): 45 , https://doi.org/10.1007/s10142-024-01316-z https://doi.org/10.1007/s10142-024-01316-z .
Li X J , Liu L , Ren Q D et al . 2025 . Analysis of synonymous codon usage bias in the chloroplast genome of five Caragana . BMC Plant Biology , 25 ( 1 ): 322 , https://doi.org/10.1186/s12870-025-06351-x https://doi.org/10.1186/s12870-025-06351-x .
Meyer M M . 2021 . Revisiting the relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature . Journal of Molecular Evolution , 89 ( 3 ): 165 - 171 , https://doi.org/10.1007/s00239-020-09974-w https://doi.org/10.1007/s00239-020-09974-w .
Omidbakhshfard M A , Omranian N , Ahmadi F S et al . 2012 . Effect of salt stress on genes encoding translation-associated proteins in Arabidopsis thaliana . Plant Signaling & Behavior , 7 ( 9 ): 1095 - 1102 , https://doi.org/10.4161/psb.21218 https://doi.org/10.4161/psb.21218 .
Orr H A . 1999 . The evolutionary genetics of adaptation: a simulation study . Genetics Research , 74 ( 3 ): 207 - 214 , https://doi.org/10.1017/S0016672399004164 https://doi.org/10.1017/S0016672399004164 .
Parvathy S T , Udayasuriyan V , Bhadana V . 2022 . Codon usage bias . Molecular Biology Reports , 49 ( 1 ): 539 - 565 , https://doi.org/10.1007/s11033-021-06749-4 https://doi.org/10.1007/s11033-021-06749-4 .
Rahman , Lokollo F F , Manuputty G D et al . 2024 . A review on the biodiversity and conservation of mangrove ecosystems in Indonesia . Biodiversity and Conservation , 33 ( 3 ): 875 - 903 , https://doi.org/10.1007/s10531-023-02767-9 https://doi.org/10.1007/s10531-023-02767-9 .
Robles P , Quesada V . 2022 . Unveiling the functions of plastid ribosomal proteins in plant development and abiotic stress tolerance . Plant Physiology and Biochemistry , 189 : 35 - 45 , https://doi.org/10.1016/j.plaphy.2022.07.029 https://doi.org/10.1016/j.plaphy.2022.07.029 .
Rogalski M , Ruf S , Bock R . 2006 . Tobacco plastid ribosomal protein S18 is essential for cell survival . Nucleic Acids Research , 34 ( 16 ): 4537 - 4545 , https://doi.org/10.1093/nar/gkl634 https://doi.org/10.1093/nar/gkl634 .
Ruang-Areerate P , Kongkachana W , Naktang C et al . 2021 . Complete chloroplast genome sequences of five Bruguiera species (Rhizophoraceae): comparative analysis and phylogenetic relationships . PeerJ , 9 : e 12268 , https://doi.org/10.7717/peerj.12268 https://doi.org/10.7717/peerj.12268 .
Sharp P M , Cowe E , Higgins D G et al . 1988 . 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 Research , 16 ( 17 ): 8207 - 8211 , https://doi.org/10.1093/nar/16.17.8207 https://doi.org/10.1093/nar/16.17.8207 .
Shen L W , Chen S Q , Liang M et al . 2024 . Comparative analysis of codon usage bias in chloroplast genomes of ten medicinal species of Rutaceae . BMC Plant Biology , 24 ( 1 ): 424 , https://doi.org/10.1186/s12870-024-04999-5 https://doi.org/10.1186/s12870-024-04999-5 .
Shi C C , Han K , Li L W et al . 2020 . Complete chloroplast genomes of 14 mangroves: phylogenetic and comparative genomic analyses . BioMed Research International , 2020 ( 1 ): 8731857 , https://doi.org/10.1155/2020/8731857 https://doi.org/10.1155/2020/8731857 .
Sidik F , Supriyanto B , Krisnawati H et al . 2018 . Mangrove conservation for climate change mitigation in Indonesia . WIREs Climate Change , 9 ( 5 ): e 529 , https://doi.org/10.1002/wcc.529 https://doi.org/10.1002/wcc.529 .
Singh N K , Tyagi A . 2017 . A detailed analysis of codon usage patterns and influencing factors in Zika virus . Archives of Virology , 162 ( 7 ): 1963 - 1973 , https://doi.org/10.1007/s00705-017-3324-2 https://doi.org/10.1007/s00705-017-3324-2 .
Soeprobowati T R , Sularto R B , Hadiyanto H et al . 2024 . The carbon stock potential of the restored mangrove ecosystem of Pasarbanggi, Rembang, Central Java. Marine Environmental Research , 193 : 106257 , https://doi.org/10.1016/j.marenvres.2023.106257 https://doi.org/10.1016/j.marenvres.2023.106257 .
Sueoka N . 1999 . 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 , 238 ( 1 ): 53 - 58 , https://doi.org/10.1016/s0378-1119(99)00320-0 https://doi.org/10.1016/s0378-1119(99)00320-0 .
Sueoka N . 2001 . Near homogeneity of PR2-bias fingerprints in the human genome and their implications in phylogenetic analyses . Journal of Molecular Evolution , 53 ( 4-5 ): 469 - 476 , https://doi.org/10.1007/s002390010237 https://doi.org/10.1007/s002390010237 .
Tyagi S , Jung J A , Kim J S et al . 2020 . Comparative analysis of the complete chloroplast genome of mainland Aster spathulifolius and other Aster species . Plants , 9 ( 5 ): 568 , https://doi.org/10.3390/plants9050568 https://doi.org/10.3390/plants9050568 .
Tyagi S , Kabade P G , Gnanapragasam N et al . 2023 . Codon usage provide insights into the adaptation of rice genes under stress condition . International Journal of Molecular Sciences , 24 ( 2 ): 1098 , https://doi.org/10.3390/ijms24021098 https://doi.org/10.3390/ijms24021098 .
Van Vliet G J C M . 1976 . Wood anatomy of the Rhizophoraceae . Leiden Botanical Series , 3 ( 1 ): 20 - 75 , https://repository.naturalis.nl/pub/508220 https://repository.naturalis.nl/pub/508220 .
Wang C W , Wong S L , Liao T S et al . 2022a . Photosynthesis in response to salinity and submergence in two Rhizophoraceae mangroves adapted to different tidal elevations . Tree Physiology , 42 ( 5 ): 1016 - 1028 , https://doi.org/10.1093/treephys/tpab167 https://doi.org/10.1093/treephys/tpab167 .
Wang L Y , Xing H X , Yuan Y C et al . 2018 . Genome-wide analysis of codon usage bias in four sequenced cotton species . PLoS One , 13 ( 3 ): e 0194372 , https://doi.org/10.1371/journal.pone.0194372 https://doi.org/10.1371/journal.pone.0194372 .
Wang X M , Chen Z T , Sui N . 2024 . Sensitivity and responses of chloroplasts to salt stress in plants. Frontiers in Plant Science , 15 : 1374086 , https://doi.org/10.3389/fpls.2024.1374086 https://doi.org/10.3389/fpls.2024.1374086 .
Wang Z J , Cai Q W , Wang Y et al . 2022b . Comparative analysis of codon bias in the chloroplast genomes of Theaceae species. Frontiers in Genetics , 13 : 824610 , https://doi.org/10.3389/fgene.2022.824610 https://doi.org/10.3389/fgene.2022.824610 .
Wright F . 1990 . The 'effective number of codons' used in a gene . Gene , 87 ( 1 ): 23 - 29 , https://doi.org/10.1016/0378-1119(90)90491-9 https://doi.org/10.1016/0378-1119(90)90491-9 .
Wu P , Xiao W Q , Luo Y Y et al . 2023 . Comprehensive analysis of codon bias in 13 Ganoderma mitochondrial genomes. Frontiers in Microbiology , 14 : 1170790 , https://doi.org/10.3389/fmicb.2023.1170790 https://doi.org/10.3389/fmicb.2023.1170790 .
Wu X K , Xu M Z , Yang J R et al . 2024 . Genome-wide impact of codon usage bias on translation optimization in Drosophila melanogaster . Nature Communications , 15 ( 1 ): 8329 , https://doi.org/10.1038/s41467-024-52660-4 https://doi.org/10.1038/s41467-024-52660-4 .
Xu S H , He Z W , Zhang Z et al . 2017 . The origin, diversification and adaptation of a major mangrove clade (Rhizophoreae) revealed by whole-genome sequencing . National Science Review , 4 ( 5 ): 721 - 734 , https://doi.org/10.1093/nsr/nwx065 https://doi.org/10.1093/nsr/nwx065 .
Xu T , Lee K , Gu L L et al . 2013 . Functional characterization of a plastid-specific ribosomal protein PSRP2 in Arabidopsis thaliana under abiotic stress conditions . Plant Physiology and Biochemistry , 73 : 405 - 411 , https://doi.org/10.1016/j.plaphy.2013.10.027 https://doi.org/10.1016/j.plaphy.2013.10.027 .
Xue Y , Qin S W , Xianyu Z C et al . 2025 . Comparative plastome analysis reveals evolutionary dynamics and codon usage patterns in Bidens (Asteraceae) . Functional & Integrative Genomics , 25 ( 1 ): 175 , https://doi.org/10.1007/s10142-025-01699-7 https://doi.org/10.1007/s10142-025-01699-7 .
Yuan J G , Gu W , Yang H J et al . 2025 . Comparative and phylogenetic analyses of the chloroplast genomes of mangrove plants . Scientific Reports , 15 ( 1 ): 3915 , https://doi.org/10.1038/s41598-024-81894-x https://doi.org/10.1038/s41598-024-81894-x .
Zhang D , Gao F L , Jakovlić I et al . 2020 . PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies . Molecular Ecology Resources , 20 ( 1 ): 348 - 355 , https://doi.org/10.1111/1755-0998.13096 https://doi.org/10.1111/1755-0998.13096 .
Zhang P P , Xu W B , Lu X et al . 2021 . Analysis of codon usage bias of chloroplast genomes in Gynostemma species . Physiology and Molecular Biology of Plants , 27 ( 12 ): 2727 - 2737 , https://doi.org/10.1007/s12298-021-01105-z https://doi.org/10.1007/s12298-021-01105-z .
Zhang Y , Yang Y C , He M et al . 2023 . Comparative chloroplast genome analyses provide insights into evolutionary history of Rhizophoraceae mangroves . PeerJ , 11 : e 16400 , https://doi.org/10.7717/peerj.16400 https://doi.org/10.7717/peerj.16400 .
Zhang Z . 2022 . KaKs_Calculator 3.0: calculating selective pressure on coding and non-coding sequences . Genomics, Proteomics & Bioinformatics , 20 ( 3 ): 536 - 540 , https://doi.org/10.1016/j.gpb.2021.12.002 https://doi.org/10.1016/j.gpb.2021.12.002 .
Zhao S , Deng L H , Chen F . 2020 . Codon usage bias of chloroplast genome in Kandelia obovata . Journal of Forest and Environment , 40 ( 5 ): 534 - 541 , https://doi.org/10.13324/j.cnki.jfcf.2020.05.011. https://doi.org/10.13324/j.cnki.jfcf.2020.05.011. (in Chinese with English abstract)
Zhao Y , Zhang S C . 2024 . Comparative analysis of codon usage bias in six Eimeria genomes . International Journal of Molecular Sciences , 25 ( 15 ): 8398 , https://doi.org/10.3390/ijms25158398 https://doi.org/10.3390/ijms25158398 .
Zhong C R , He S M , Fang Z S . 2024 . Analysis on codon usage bias of chloroplast genomes of three species of mangroves in Combretaceae . Journal of Plant Resources and Environment , 33 ( 2 ): 1 - 12 , https://doi.org/10.3969/j.issn.1674-7895.2024.02.01. https://doi.org/10.3969/j.issn.1674-7895.2024.02.01. (in Chinese with English abstract)
Zou D J , Guo B R , Liu J Q et al . 2026 . Characterization of codon usage bias in the chloroplast genome of Salix matsudana . Journal of Southwest Forestry University , 46 ( 1 ): 74 - 80 , https://doi.org/10.11929/j.swfu.202503017. https://doi.org/10.11929/j.swfu.202503017. (in Chinese with English abstract)
0
浏览量
0
Downloads
0
CSCD
关联资源
相关文章
相关作者
相关机构

京公网安备11010802024621