Abstract
Ulvophytes are attractive model systems for understanding the evolution of growth, development, and environmental stress responses. They are untapped resources for food, fuel, and high-value compounds. The rapid and abundant growth of Ulva species makes them key contributors to coastal biogeochemical cycles, which can cause significant environmental problems in the form of green tides and biofouling. Until now, the Ulva mutabilis genome is the only Ulva genome to have been sequenced. To obtain further insights into the evolutionary forces driving divergence in Ulva species, we analyzed 3 905 single copy ortholog family from U. mutabilis, Chlamydomonas reinhardtii and Volvox carteri to identify genes under positive selection (GUPS) in U. mutabilis. We detected 63 orthologs in U. mutabilis that were considered to be under positive selection. Functional analyses revealed that several adaptive modifications in photosynthesis, amino acid and protein synthesis, signal transduction and stress-related processes might explain why this alga has evolved the ability to grow very rapidly and cope with the variable coastal ecosystem environments.
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References
Bakewell M A, Shi Peng, Zhang Jianzhi. 2007. More genes underwent positive selection in chimpanzee evolution than in human evolution. Proceedings of the National Academy of Sciences of the United States of America, 104(18): 7489–7494, doi: https://doi.org/10.1073/pnas.0701705104
Biswas S, Akey J M. 2006. Genomic insights into positive selection. Trends in Genetics, 22(8): 437–446, doi: https://doi.org/10.1016/j.tig.2006.06.005
Charlier R H, Morand P, Finkl C W, et al. 2006. Green tides on the Brittany coasts. In: 2006 IEEE US/EU Baltic International Symposium. Klaipeda, Lithuania: IEEE, 1–13
Cocquyt E, Verbruggen H, Leliaert F, et al. 2010. Evolution and cytological diversification of the green seaweeds (Ulvophyceae). Molecular Biology and Evolution, 27(9): 2052–2061, doi: https://doi.org/10.1093/molbev/msq091
De Clerck O, Kao S M, Bogaert K A, et al. 2018. Insights into the evolution of multicellularity from the sea lettuce genome. Current Biology, 28(18): 2921–2933, doi: https://doi.org/10.1016/j.cub.2018.08.015
Di Paolo G, De Camilli P. 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature, 443(7112): 651–657, doi: https://doi.org/10.1038/nature05185
Emms D M, Kelly S. 2015. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biology, 16(1): 157, doi: https://doi.org/10.1186/s13059-015-0721-2
Gao Shan, Gu Wenhui, Xiong Qian, et al. 2015. Desiccation enhances phosphorylation of PS II and affects the distribution of protein complexes in the thylakoid membrane. Physiologia Plantarum, 153(3): 492–502, doi: https://doi.org/10.1111/ppl.12258
Gao Shan, Shen Songdong, Wang Guangce, et al. 2011. PSI-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant and Cell Physiology, 52(5): 885–893, doi: https://doi.org/10.1093/pcp/pcr038
Gao Shan, Zheng Zhenbing, Gu Wenhui, et al. 2014. Photosystem I shows a higher tolerance to sorbitol-induced osmotic stress than photosystem II in the intertidal macro-algae Ulva prolifera (Chlorophyta). Physiologia Plantarum, 152(2): 380–388, doi: https://doi.org/10.1111/ppl.12188
Jensen J D, Bachtrog D. 2010. Characterizing recurrent positive selection at fast-evolving genes in Drosophila miranda and Drosophila pseudoobscura. Genome Biology and Evolution, 2: 371–378, doi: https://doi.org/10.1093/gbe/evq028
Kakinuma M, Coury D A, Kuno Y, et al. 2006. Physiological and biochemical responses to thermal and salinity stresses in a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta). Marine Biology, 149(1): 97–106, doi: https://doi.org/10.1007/s00227-005-0215-y
Kanehisa M, Goto S. 2000. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Research, 28(1): 27–30, doi: https://doi.org/10.1093/nar/28.1.27
Nakamura T, Yamada K D, Tomii K, et al. 2018. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics, 34(14): 2490–2492, doi: https://doi.org/10.1093/bioinformatics/bty121
Neilson J A D, Durnford D G. 2010. Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynthesis Research, 106: 57–71, doi: https://doi.org/10.1007/s11120-010-9576-2
Niinemets Ü, Berry J A, von Caemmerer S, et al. 2017. Photosynthesis: ancient, essential, complex, diverse... and in need of improvement in a changing world. New Phytologist, 213(1): 43–47, doi: https://doi.org/10.1111/nph.14307
Noctor G, Arisi A C M, Jouanin L, et al. 1999. Photorespiratory glycine enhances glutathione accumulation in both the chloroplastic and cytosolic compartments. Journal of Experimental Botany, 50(336): 1157–1167, doi: https://doi.org/10.1093/jxb/50.336.1157
R Development Core Team. 2014. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing
Smetacek V, Zingone A. 2013. Green and golden seaweed tides on the rise. Nature, 504(7478): 84–88, doi: https://doi.org/10.1038/nature12860
Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Research, 34(S2): W609–W612
Swift D G, Dunning L T, Igea J, et al. 2016. Evidence of positive selection associated with placental loss in tiger sharks. BMC Evolutionary Biology, 16(1): 126, doi: https://doi.org/10.1186/s12862-016-0696-y
Teng Linhong, Fan Xiao, Xu Dong, et al. 2017. Identification of genes under positive selection reveals differences in evolutionary adaptation between brown-algal species. Frontiers in Plant Science, 8: 1429, doi: https://doi.org/10.3389/fpls.2017.01429
Van Alstyne K L. 2008. Ecological and physiological roles of dimethylsulfoniopropionate and its products in marine macroalgae. In: Amsler C D, ed. Algal Chemical Ecology. Berlin, Heidelberg: Springer, 173–194
Vesty E F, Kessler R W, Wichard T, et al. 2015. Regulation of gametogenesis and zoosporogenesis in Ulva linza (Chlorophyta): comparison with Ulva mutabilis and potential for laboratory culture. Frontiers in Plant Science, 6: 15
Wichard T, Charrier B, Mineur F, et al. 2015. The green seaweed Ulva: a model system to study morphogenesis. Frontiers in Plant Science, 6: 72
Wingler A, Lea P J, Quick W P, et al. 2000. Photorespiration: metabolic pathways and their role in stress protection. Philosophical Transactions of the Royal Society B: Biological Sciences, 355(1402): 1517–1529, doi: https://doi.org/10.1098/rstb.2000.0712
Xie Chen, Mao Xizeng, Huang Jiaju, et al. 2011. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research, 39(S2): W316–W322
Xie Xiujun, Gu Wenhui, Gao Shan, et al. 2013. Alternative electron transports participate in the maintenance of violaxanthin de-epoxidase activity of Ulva sp. under low irradiance. PLoS One, 8(11): e78211
Yang Ziheng. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8): 1586–1591, doi: https://doi.org/10.1093/molbev/msm088
Yang Ziheng, Reis M D. 2011. Statistical properties of the branch-site test of positive selection. Molecular Biology and Evolution, 28(3): 1217–1228, doi: https://doi.org/10.1093/molbev/msq303
Zhang Junxiang, Yuan Hui, Yang Yong, et al. 2016. Plastid ribosomal protein S5 is involved in photosynthesis, plant development, and cold stress tolerance in Arabidopsis. Journal of Experimental Botany, 67(9): 2731–2744, doi: https://doi.org/10.1093/jxb/erw106
Zhang Xiaowen, Mou Shanli, Cao Shaona, et al. 2015. Roles of the transthylakoid proton gradient and xanthophyll cycle in the non-photochemical quenching of the green alga Ulva linza. Estuarine, Coastal and Shelf Science, 163: 69–74, doi: https://doi.org/10.1016/j.ecss.2014.09.006
Zhang Yongyu, He Peimin, Li Hongmei, et al. 2019. Ulva prolifera green-tide outbreaks and their environmental impact in the Yellow Sea, China. National Science Review, 6(4): 825–838, doi: https://doi.org/10.1093/nsr/nwz026
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The National Key Research and Development Program of China under contract No. 2016YFC1402102; the Central Public-interest Scientific Institution Basal Research Fund, CAFS under contract Nos 2020TD19 and 2020TD27; the Major Scientific and Technological Innovation Project of Shandong Provincial Key Research and Development Program under contract No. 2019JZZY020706; the National Natural Science Foundation of China under contract No. 31770393; the Earmarked Fund for China Agriculture Research System under contract No. CARS-50; the Taishan Scholars Funding of Shandong Province.
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Zhang, J., Zhang, X., Han, W. et al. Identification of genes under positive selection reveals evolutionary adaptation of Ulva mutabilis. Acta Oceanol. Sin. 39, 35–41 (2020). https://doi.org/10.1007/s13131-020-1658-1
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DOI: https://doi.org/10.1007/s13131-020-1658-1