

FOLLOWUS
1.Key Laboratory of Exploration and Utilization of Aquatic Resources, Ministry of Education, Shanghai Ocean University, Shanghai 201306, China
2.Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai 201306, China
3.College of Marine Science, Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, Beibu Gulf Ocean Development Research Center, Beibu Gulf University, Qinzhou 535011, China
4.Beibu Gulf Marine Ecological Environment Field Observation and Research Station of Guangxi, Qinzhou 535011, China
dhgao@shou.edu.cn
Received:19 June 2024,
Published:01 July 2025
Scan QR Code
CHANG Jianhui,TAN Karsoon,GAO Dahai.Genome-wide evolutionary and comparative analysis of superoxide dismutase gene family in three bladed Bangiales species[J].Journal of Oceanology and Limnology,2025,43(04):1282-1297.
CHANG Jianhui,TAN Karsoon,GAO Dahai.Genome-wide evolutionary and comparative analysis of superoxide dismutase gene family in three bladed Bangiales species[J].Journal of Oceanology and Limnology,2025,43(04):1282-1297. DOI: 10.1007/s00343-024-4164-z.
As a key component of the plant antioxidant enzymatic system
superoxide dismutase (SOD) can efficiently protect cells from oxidative stress and maintain redox homeostasis. Currently
there are few studies related to SOD genes in various taxa of algae
and the specific functions and evolutionary patterns of these family members remain unclear. In this study
comprehensively evolutionary analysis of SOD gene family in the bladed Bangiales was carried out. A total of 9
10
and 12 SOD genes were identified from three species of
Pophyra
umbilicalis
Pyropia
haitanensis
and
Pyropia
yezoensis
respectively. Based on phylogenetic analysis
SOD gene members within the same subfamily exhibited similar motif patterns as well as conserved domains
which could be attribute to Cu/Zn-SOD and Fe/Mn-SOD. The promoter regions of SOD genes were rich in hormone-responsive
stress-responsive
and growth cis-acting elements
with variations and similarities observed among different species of other red algae and subfamilies. According to subcellular location prediction
it is suggested that Cu/Zn-SOD was predominantly located in chloroplasts
while Fe/Mn-SOD was primarily located in mitochondria. Also
the two subfamilies differed significantly in the two-/three-dimensional protein structures. In terms of gene evolution
the strongest collinearity relationship was shown be
tween
Pyropia
haitanensis
and
Pyropia
yezoensis
with all the 1꞉1 orthologous gene pair being subjected to a purifying selection (
Ka
/
Ks
<
1
Ka
: non-synonymy rate;
Ks
: synonymy rate). Moreover
12 SOD genes underwent positive selection during the evolutionary process. Furthermore
gene expression analysis based on transcriptomic data from
Pyropia
haitanensis
showed that the expression patterns of SOD genes varied under different stress conditions. Together
this study revealed the evolutionary pattern of SOD genes in three bladed Bangiales species
which will lay the foundation for subsequent studies on the function of SOD genes.
Alscher R G , Erturk N , Heath L S . 2002 . Role of superoxide dismutases (SODs) in controlling oxidative stress in plants . Journal of Experimental Botany , 53 ( 372 ): 1331 - 1341 , https://doi.org/10.1093/jexbot/53.372.1331 https://doi.org/10.1093/jexbot/53.372.1331 .
Bailey T L , Johnson J , Grant C E et al . 2015 . The MEME suite . Nucleic Acids Research , 43 ( W1 ): W39 - W49 , https://doi.org/10.1093/nar/gkv416 https://doi.org/10.1093/nar/gkv416 .
Blaby-Haas C E , Merchant S S . 2013 . Iron sparing and recycling in a compartmentalized cell . Current Opinion in Microbiology , 16 ( 6 ): 677 - 685 , https://doi.org/10.1016/j.mib.2013.07.019 https://doi.org/10.1016/j.mib.2013.07.019 . https://do 10.1016/j.mib.2013.07.019 http://dx.doi.org/10.1016/j.mib.2013.07.019
Cao M , Xu K P , Yu X Z et al . 2020 . A chromosome-level genome assembly of Pyropia haitanensis (Bangiales, Rhodophyta) . Molecular Ecology Resources , 20 ( 1 ): 216 - 227 , https://doi.org/10.1111/1755-0998.13102 https://doi.org/10.1111/1755-0998.13102 .
Chen C J , Chen H , Zhang Y et al . 2020 . TBtools: an integrative toolkit developed for interactive analyses of big biological data . Molecular Plant , 13 ( 8 ): 1194 - 1202 , https://doi.org/10.1016/j.molp.2020.06.009 https://doi.org/10.1016/j.molp.2020.06.009 .
Duvaud S , Gabella C , Lisacek F et al . 2021 . Expasy, the Swiss bioinformatics resource portal, as designed by its users . Nucleic Acids Research , 49 ( W1 ): W216 - W227 , https://doi.org/10.1093/nar/gkab225 https://doi.org/10.1093/nar/gkab225 .
Dvořák P , Krasylenko Y , Zeiner A et al . 2021 . Signaling toward reactive oxygen species-scavenging enzymes in plants. Frontiers in Plant Science , 11 : 618835 , https://doi.org/10.3389/fpls.2020.618835 https://doi.org/10.3389/fpls.2020.618835 .
Feng K , Yu J H , Cheng Y et al . 2016 . The SOD gene family in tomato: identification, phylogenetic relationships, and expression patterns. Frontiers in Plant Science , 7 : 1279 , https://doi.org/10.3389/fpls.2016.01279 https://doi.org/10.3389/fpls.2016.01279 .
Frye K A , Sendra K M , Waldron K J et al . 2022 . Old dogs, new tricks: new insights into the iron/manganese superoxide dismutase family. Journal of Inorganic Biochemistry , 230 : 111748 , https://doi.org/10.1016/j.jinorgbio.2022.111748 https://doi.org/10.1016/j.jinorgbio.2022.111748 .
Gao F L , Chen C J , Arab D A et al . 2019 . EasyCodeML: a visual tool for analysis of selection using CodeML . Ecology and Evolution , 9 ( 7 ): 3891 - 3898 , https://doi.org/10.1002/ece3.5015 https://doi.org/10.1002/ece3.5015 .
Geourjon C , Deléage G . 1995 . SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments . Bioinformatics , 11 ( 6 ): 681 - 684 , https://doi.org/10.1093/bioinformatics/11.6.681 https://doi.org/10.1093/bioinformatics/11.6.681 .
Guan X W , Wang D M , Chen R et al . 2023 . Genome-wide identification and characterization of SOD gene family in Pyropia yezoensis during temperature stresses . Periodical of Ocean University of China , 53 ( 2 ): 60 - 68 , https://doi.org/10.16441/j.cnki.hdxb.20210442. https://doi.org/10.16441/j.cnki.hdxb.20210442. (in Chinese with English abstract)
Hall B G . 2013 . Building phylogenetic trees from molecular data with MEGA . Molecular Biology and Evolution , 30 ( 5 ): 1229 - 1235 , https://doi.org/10.1093/molbev/mst012 https://doi.org/10.1093/molbev/mst012 .
Hasanuzzaman M , Borhannuddin Bhuyan M H M , Parvin K et al . 2020 . Regulation of ROS metabolism in plants under environmental stress: a review of recent experimental evidence . International Journal of Molecular Sciences , 21 ( 22 ): 8695 , https://doi.org/10.3390/ijms21228695 https://doi.org/10.3390/ijms21228695 .
Horton P , Park K J , Obayashi T et al . 2007 . WoLF PSORT: protein localization predictor . Nucleic Acids Research , 35 ( W2 ): W585 - W587 , https://doi.org/10.1093/nar/gkm259 https://doi.org/10.1093/nar/gkm259 .
Hu B , Jin J P , Guo A Y et al . 2015 . GSDS 2.0: an upgraded gene feature visualization server . Bioinformatics , 31 ( 8 ): 1296 - 1297 , https://doi.org/10.1093/bioinformatics/btu817 https://doi.org/10.1093/bioinformatics/btu817 .
Hu S H , Jinn T L . 2022 . Impacts of Mn, Fe, and oxidative stressors on MnSOD activation by AtMTM1 and AtMTM2 in Arabidopsis . Plants (Basel) , 11 ( 5 ): 619 , https://doi.org/10.3390/plants11050619 https://doi.org/10.3390/plants11050619 .
Huang L B , Peng L N , Yan X H . 2021 . Multi-omics responses of red algae Pyropia haitanensis to intertidal desiccation during low tides. Algal Research , 58 : 102376 , https://doi.org/10.1016/j.algal.2021.102376 https://doi.org/10.1016/j.algal.2021.102376 .
Huo C S , He L S , Yu T et al . 2022 . The superoxide dismutase gene family in Nicotiana tabacum : genome-wide identification, characterization, expression profiling and functional analysis in response to heavy metal stress. Frontiers in Plant Science , 13 : 904105 , https://doi.org/10.3389/fpls.2022.904105 https://doi.org/10.3389/fpls.2022.904105 .
Ismaiel M M S , El-Ayouty Y M , Loewen P C et al . 2014 . Characterization of the iron-containing superoxide dismutase and its response to stress in cyanobacterium Spirulina ( Arthrospira ) platensis . Journal of Applied Phycology , 26 ( 4 ): 1649 - 1658 , https://doi.org/10.1007/s10811-013-0233-y https://doi.org/10.1007/s10811-013-0233-y .
Ismaiel M M S , Piercey-Normore M D . 2023 . Antioxidant enzymes of Pseudochlorella pringsheimii under two stressors: variation of SOD Isoforms activity . Journal of Plant Research , 136 ( 5 ): 755 - 767 , https://doi.org/10.1007/s10265-023-01473-5 https://doi.org/10.1007/s10265-023-01473-5 .
Ji X , Zhou J L , Song C G et al . 2022 . Taxonomy, phylogeny and divergence times of Polyporus (Basidiomycota) and related genera . Mycosphere , 13 ( 1 ): 1 - 52 , https://doi.org/10.5943/mycosphere/13/1/1 https://doi.org/10.5943/mycosphere/13/1/1 .
Jiang S R , An P L , Xia C C et al . 2023 . Genome-wide identification and expression analysis of the SUT family from three species of sapindaceae revealed their role in the accumulation of sugars in fruits . Plants (Basel) , 13 ( 1 ): 95 , https://doi.org/10.3390/plants13010095 https://doi.org/10.3390/plants13010095 .
Khan M , Ali S , Al Azzawi T N I et al . 2023 . The key roles of ROS and RNS as a signaling molecule in plant-microbe interactions . Antioxidants , 12 ( 2 ): 268 , https://doi.org/10.3390/antiox12020268 https://doi.org/10.3390/antiox12020268 .
Kim J K , Yarish C , Hwang E K et al . 2017 . Seaweed aquaculture: cultivation technologies, challenges and its ecosystem services . Algae , 32 ( 1 ): 1 - 13 , https://doi.org/10.4490/algae.2017.32.3.3 https://doi.org/10.4490/algae.2017.32.3.3 . https://do 10.4490/algae.2017.32.3.3 http://dx.doi.org/10.4490/algae.2017.32.3.3
Kitayama K , Kitayama M , Osafune T et al . 1999 . Subcellular localization of iron and manganese superoxide dismutase in Chlamydomonas reinhardtii (Chlorophyceae) . Journal of Phycology , 35 ( 1 ): 136 - 142 , https://doi.org/10.1046/j.1529-8817.1999.3510136.x https://doi.org/10.1046/j.1529-8817.1999.3510136.x .
Lescot M , Déhais P , Thijs G et al . 2002 . PlantCARE, a database of plant cis -acting regulatory elements and a portal to tools for in silico analysis of promoter sequences . Nucleic Acids Research , 30 ( 1 ): 325 - 327 , https://doi.org/10.1093/nar/30.1.325 https://doi.org/10.1093/nar/30.1.325 .
Lin Y L , Lai Z X . 2013 . Superoxide dismutase multigene family in Longan somatic embryos: a comparison of CuZn-SOD, Fe-SOD, and Mn-SOD gene structure, splicing, phylogeny, and expression . Molecular Breeding , 32 ( 3 ): 595 - 615 , https://doi.org/10.1007/s11032-013-9892-2 https://doi.org/10.1007/s11032-013-9892-2 .
Liu H H , He J Y , Chi C F et al . 2015 . Identification and analysis of icCu/Zn-SOD, Mn-SOD and ecCu/Zn-SOD in superoxide dismutase multigene family of Pseudosciaena crocea . Fish & Shellfish Immunology , 43 ( 2 ): 491 - 501 , https://doi.org/10.1016/j.fsi.2015.01.032 https://doi.org/10.1016/j.fsi.2015.01.032 .
Liu J , Xu L J , Shang J et al . 2021 . Genome-wide analysis of the maize superoxide dismutase (SOD) gene family reveals important roles in drought and salt responses . Genetics and Molecular Biology , 44 ( 3 ): e 20210035 , https://doi.org/10.1590/1678-4685-gmb-2021-0035 https://doi.org/10.1590/1678-4685-gmb-2021-0035 .
Mittler R . 2017 . ROS are good . Trends in Plant Science , 22 ( 1 ): 11 - 19 , https://doi.org/10.1016/j.tplants.2016.08.002 https://doi.org/10.1016/j.tplants.2016.08.002 .
Mittler R , Zandalinas S I , Fichman Y et al . 2022 . Reactive oxygen species signalling in plant stress responses . Nature Reviews Molecular Cell Biology , 23 ( 10 ): 663 - 679 , https://doi.org/10.1038/s41580-022-00499-2 https://doi.org/10.1038/s41580-022-00499-2 .
Nan G X , Zhang Y , Li S et al . 2016 . NaCl stress-induced transcriptomics analysis of Salix linearistipularis (syn. Salix mongolica ) . Journal of Biological Research-Thessaloniki , 23 ( 1 ): 1 , https://doi.org/10.1186/s40709-016-0038-7 https://doi.org/10.1186/s40709-016-0038-7 .
Nawrocki E P , Eddy S R . 2013 . Infernal 1.1: 100-fold faster RNA homology searches . Bioinformatics , 29 ( 22 ): 2933 - 2935 , https://doi.org/10.1093/bioinformatics/btt509 https://doi.org/10.1093/bioinformatics/btt509 .
Ou S J , Chen J F , Jiang N . 2018 . Assessing genome assembly quality using the LTR Assembly Index (LAI) . Nucleic Acids Research , 46 ( 21 ): e 126 , https://doi.org/10.1093/nar/gky730 https://doi.org/10.1093/nar/gky730 .
Qin Q Q . 2023 . ROS: important factor in plant stem cell fate regulation. Journal of Plant Physiology , 289 : 154082 , https://doi.org/10.1016/j.jplph.2023.154082 https://doi.org/10.1016/j.jplph.2023.154082 .
Rajput V D , Harish , Singh R K et al . 2021 . Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress . Biology (Basel) , 10 ( 4 ): 267 , https://doi.org/10.3390/biology10040267 https://doi.org/10.3390/biology10040267 .
Rozewicki J , Li S L , Amada K M et al . 2019 . MAFFT-DASH: integrated protein sequence and structural alignment . Nucleic Acids Research , 47 ( W1 ): W5 - W10 , https://doi.org/10.1093/nar/gkz342 https://doi.org/10.1093/nar/gkz342 .
Sahu P K , Jayalakshmi K , Tilgam J et al . 2022 . ROS generated from biotic stress: effects on plants and alleviation by endophytic microbes. Frontiers in Plant Science , 13 : 1042936 , https://doi.org/10.3389/fpls.2022.1042936 https://doi.org/10.3389/fpls.2022.1042936 .
Saibi W , Brini F . 2018 . Superoxide dismutase (SOD) and abiotic stress tolerance in plants : an overview . Superoxide Dismutase : Structure, Synthesis and Applications. In: Magliozzi S ed . p . 101 - 142 .
Shams M , Pokora W , Khadivi A et al . 2024 . Superoxide dismutase in Arabidopsis and Chlamydomonas : diversity, localization, regulation, and role . Plant and Soil , published Online 20 March, 2024 , https://doi.org/10.1007/s11104-024-06618-6 https://doi.org/10.1007/s11104-024-06618-6 .
Terwilliger T C , Poon B K , Afonine P V et al . 2022 . Improved AlphaFold modeling with implicit experimental information . Nature Methods , 19 ( 11 ): 1376 - 1382 , https://doi.org/10.1038/s41592-022-01645-6 https://doi.org/10.1038/s41592-022-01645-6 .
Tounsi S , Jemli S , Feki K et al . 2023 . Superoxide dismutase (SOD) family in durum wheat: promising candidates for improving crop resilience . Protoplasma , 260 ( 1 ): 145 - 158 , https://doi.org/10.1007/s00709-022-01767-w https://doi.org/10.1007/s00709-022-01767-w .
Wang Y , Branicky R , Noë A et al . 2018 . Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling . Journal of Cell Biology , 217 ( 6 ): 1915 - 1928 , https://doi.org/10.1083/jcb.201708007 https://doi.org/10.1083/jcb.201708007 .
Waterhouse A , Bertoni M , Bienert S et al . 2018 . SWISS-MODEL: homology modelling of protein structures and complexes . Nucleic Acids Research , 46 ( W1 ): W296 - W303 , https://doi.org/10.1093/nar/gky427 https://doi.org/10.1093/nar/gky427 .
Wu H L , Kim J K , Huo Y Z et al . 2017 . Nutrient removal ability of seaweeds on Pyropia yezoensis aquaculture rafts in China’s radial sandbanks . Aquatic Botany , 137 : 72 - 79 , https://doi.org/10.1016/j.aquabot.2016.11.011 https://doi.org/10.1016/j.aquabot.2016.11.011 .
Xiong E H , Zheng C Y , Wu X L et al . 2016 . Protein subcellular location: the gap between prediction and experimentation . Plant Molecular Biology Reporter , 34 ( 1 ): 52 - 61 , https://doi.org/10.1007/s11105-015-0898-2 https://doi.org/10.1007/s11105-015-0898-2 .
Xu H S , Guo S M , Zhu L et al . 2020 . Growth, physiological and transcriptomic analysis of the perennial ryegrass Lolium perenne in response to saline stress . Royal Society Open Science , 7 ( 7 ): 200637 , https://doi.org/10.1098/rsos.200637 https://doi.org/10.1098/rsos.200637 .
Yang S S , Lian G J . 2020 . ROS and diseases: role in metabolism and energy supply . Molecular and Cellular Biochemistry , 467 ( 1-2 ): 1 - 12 , https://doi.org/10.1007/s11010-019-03667-9 https://doi.org/10.1007/s11010-019-03667-9 .
Yu B , Wang M , Teng B et al . 2023a . Partially acid-hydrolyzed porphyran improved dextran sulfate sodium-induced acute colitis by modulation of gut microbiota and enhancing the mucosal barrier . Journal of Agricultural and Food Chemistry , 71 ( 19 ): 7299 - 7311 , https://doi.org/10.1021/acs.jafc.2c08564 https://doi.org/10.1021/acs.jafc.2c08564 .
Yu S T , Wang C T , Wang Q et al . 2023b . Identification and analysis of SOD family genes in peanut ( Arachis hypogaea L.) and their potential roles in stress responses . Agronomy (Basel) , 13 ( 8 ): 1959 , https://doi.org/10.3390/agronomy13081959 https://doi.org/10.3390/agronomy13081959 .
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 X , Zhang L T , Chen Y Y et al . 2021 . Genome-wide identification of the SOD gene family and expression analysis under drought and salt stress in barley . Plant Growth Regulation , 94 ( 1 ): 49 - 60 , https://doi.org/10.1007/s10725-021-00695-8 https://doi.org/10.1007/s10725-021-00695-8 .
Zhao Y D , Li M C , Konaté M M et al . 2021 . TPM, FPKM, or normalized counts? A comparative study of quantification measures for the analysis of RNA-seq data from the NCI patient-derived models repository . Journal of Translational Medicine , 19 ( 1 ): 269 , https://doi.org/10.1186/s12967-021-02936-w https://doi.org/10.1186/s12967-021-02936-w .
0
Views
8
Downloads
0
CSCD
Publicity Resources
Related Articles
Related Author
Related Institution
京公网安备11010802024621