Codon Usage of Chloroplast Gene rbcL in Laurencia sensu lato (Rhodophyta) species

Source:
By:Ruben Cabrera, Jhoana Díaz-Larrea, Arsenio J. Areces, Laura Nuñez García, J. Ricardo Cruz-Aviña, Gabriela Vázquez Silva

DOI: https://doi.org/10.30564/jms.v3i4.3542

Abstract:

Recent advances in molecular biology make it possible to sequence not only genes or genomes, but also to understand codon dynamics. For the organelle genes of these organisms, a small set of preferred codons are used for encoding proteins. For the first time, this paper treats the divergence of synonymous codon usage and its bias in the rbcL gene within the Laurencia complex of red algae. We observed that the synonymous codon preference biases in rbcL are large and differ among species. A clear distinction in codon usage between genera is evident: the genera Dasya and Delesseria use a set that fluctuated between 53 and 58 codons. Whereas, in the genera Ceramium, Chondrophycus, Chlamydomonas, Chlorella, Laurencia s.s, Osmundea, and Palisada codon usage indicates a higher restriction fluctuating between 40 to 51 codons. Laurencia complex genera and other representative algae showed a defined composition pattern, with lower percentage values of NNC/G (7-24.9%). Dasya and Delesseria showed a selective pattern tendency because of high percentage values of NNC/G (54-55%). The estimated codon bias parameters were tested to infer systematic relationships and match suitable codons with the NNC / G codon percentages. Cluster analysis based on Codon Usage supports phylogenetic relationships between Chondrophycus, Palisada, Laurencia, Osmundea, and Yuzurua species.

References:

[1]Wang L, Roossinck MJ. 2006. Comparative analysis of expressed sequences reveals a conserved pattern of optimal codon usage in plants. Plant Molecular Biology. 61, 699-710. [2]Wang FP, Li H. 2009. Codon-pair usage and genome evolution. Gene, 433, 8-15. [3]Heitzer M, Eckert A, Fuhrmann M, Griesbeck C. 2007. Influence of codon bias on the expression of foreign genes in microalgae. In: León, R., Galvan A. and Fernandez, E. (Eds.). Transgenic microalgae as green cell factories. Landes Bioscience and Springer Science Business Media. [4]Grantham R. 1980. Workings of the genetic code. Trends Biochemical Sciences. 5, 327-31. [5]Henry I, Sharp PM. 2007. Predicting gene expression level from codon usage bias. Molecular Biology and Evolution. 24(1): 10-12. [6]Lawrence JG, Ochman H. 1998. Molecular archaeology of the Escherichia coli genome. Proceedings National Academy of Sciences. 95, 9413-9417. [7]Christianson ML. 2005. Codon usage patterns distort phylogenies from or of DNA sequences. American Journal of Botany. 92(8): 1221-1233. [8]Van der Linden MG, de Farias S.T. 2006. Correlation between codon usage and thermostability. Extremophiles. 10, 479-481. [9]De Boer HA, Kastein RA. 1986. Biased codon usage: an exploration of its role in optimization of translation. In: W. Reznikoo, L. Gold, (Eds), Maximizing gene expression. Butterwoths, Boston, pp. 225-285. [10]Comeron JM, Aguadé, M. 1998. An evaluation of measures of synonymous codon usage bias. Journal of Molecular Evolution 47, 268-274. [11]Morton BR. 1996. Selection on the codon bias of the Chlamydomonas reinhardtii chloroplast genes and the plant psbA gene. Journal of Molecular Evolution 43, 28-31. [12]Yoshinaga K, Ohta T, Suzuki Y, Sugiura M. 1988. Chlorella chloroplast DNA sequence containing a gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase and a part of a possible gene for the ß`subunit of RNA polymerase. Plant Molecular Biology. 10, 245-250. [13]Collén PN, Collén J, Reis MS, Pedersén MJ, Setubal C, Varani AM, Colepicolo P, Oliveira MC. 2012. Analysis of expressed sequence tags from the agarophyte Gracilaria tenuistipitata (Rhodophyta). Journal of Applied Phycology 24, 641–647 (DOI 10.1007/ s10811-011-9681-4). [14]Lee H, Lee HK, An G, Lee YK. 2007. Analysis of expressed sequence tags from the red alga Griffithsia okiensis. The Journal of Microbiology. 45(6), 541- 546. [15]Nikaido I, Asamizu E, Nakajima M, Nakamura Y, Saga N, Tabata S. 2000. Generation of 10,154 expressed sequence tags from a leafy gametophyte of a marine red alga, Porphyra yezoensis. DNA Research. 7, 223-227. [16]Bernardi G, Bernardi G. 1985. Codon usage and genome composition. Journal of Molecular Evolution. 22, 363-365. [17]Ikemura, T. 1985. Codon usage and tRNA content in unicellular and multicellular organisms. Molecular Biology and Evolution. 2, 13-35. [18]Okayasu T, Sorimachi K. 2009. Organisms can essentially be classified according to two codon patterns. Amino Acids. 36, 261-271. [19]Morton BR. 1998. Selection on the codon bias of chloroplast and cyanelle genes in different plant and algal lineages. Journal of Molecular Evolution. 46, 449-459. [20]Kanaya S, Yamada Y, Kudo Y, Ikemura T. 1999. Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene. 238, 143-155. [21]Ohyama K, Fukuzawa H, Kohchi T, Sano T, Sano S, Shirai H. 1988. Structure and organization of Marchantia polymorpha chloroplast genome. I. Cloning and gene identification. Journal of Molecular Biology. 203, 281-298. [22]Wakasugi T, Ohme M, Shinozaki K, Sugiura M. 1986. Structures of tobacco chloroplast genes for tRNAIle (CAU), tRNALeu (CAA), tRNACys (GCA), tRNASer (UGA) and tRNAThr (GGU): a compilation of tRNA genes from tobacco chloroplasts. Plant Molecular Biology. 7, 385-392. [23]Pfitzinger H, Guillemaunt P, Weil JH, Pillary DTN. 1987. Adjustment of the tRNA population to the codon usage in chloroplasts. Nucleic Acids Research.15, 1377-1386. [24]Wells D, Bains W, Kedes L. 1986. Codon usage in histone gene families of higher eukaryotes reflects functional rather than phylogenetic relationships. Journal of Molecular Evolution. 23, 224-241. [25]Sharp PM, Tuohy TMF, Mosursky KR. 1986. Codon usage in yeast: Cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acid Research. 14, 5125-5143. [26]Long M, Gillespie JH. 1991. Codon usage divergence of homologous vertebrate genes and codon usage clock. Journal of Molecular Evolution. 32, 6-15. [27]Shields DC, Sharp PM, Higgins DG, Wright F. 1988. “Silent” sites in Drosophila genes are not neutral: Evidence of selection among synonymous codon. Molecular Journal and Evolution. 5, 704-716. [28]Rozas J, Sánchez-Del Barrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 19, 2496-2497. [29]Wright F. 1990. The “effective number of codons” used in a gene. Gene. 87, 23-29. [30]Morton BR. 1993. Chloroplast DNA codon use: evidence for selection at the psbA locus based on tRNA availability. Journal of Molecular Evolution.37, 273- 280. [31]Kellogg EA, Juliano ND. 1997. The structure and function of RUBISCO and their implications for systematic studies. American Journal of Botany 84(3), 413-428. [32]Wall DP, Herbeck JT. 2003. Evolutionary patterns of codon usage in the chloroplast gene rbcL. Journal of Molecular Evolution. 56, 673-688. [33] Hagopian JC, Reis M, Kitajima JP, Bhattacharya D, de Oliveira MC. 2004. Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights into the evolution of rhodoplasts and their relationship to other plastids. Journal of Molecular Evolution. 59, 464-477. [34] Campbell WH, Gowri G. 1990. Codon usage in higher plants, green algae, and cyanobacteria. Plant Physiology. 92, 1-11. [35] Golding GB, Strobeck C. 1982. Expected frequencies of codon use as a function of mutation rates and codon fitnesses. Journal of Molecular Evolution. 18, 379-386. [36] Cassano V, Díaz-Larrea J, Sentíes A, Oliveira MC, Gil-Rodríguez MC, Fujii MT. 2009. Evidence for the conspecificity of Palisada papillosa with P. perforata (Ceramiales, Rhodophyta) from the western and eastern Atlantic Ocean on the basis of morphological and molecular analyses. Phycologia. 48(2), 86-100. [37] Gil-Rodríguez MC, Sentíes A, Díaz-Larrea J, Cassano V, Fujii MT. 2009. Laurencia marilzae sp. nov. (Ceramiales, Rhodophyta) from the Canary Islands, Spain, based on morphological and molecular evidences. Journal of Phycology . 45(1), 264-275. [38] Gil-Rodríguez MC, Cassano V, Aylagas E, Sentíes A, Díaz-Larrea J, Oliveira MC, Fujii MT.2010. Palisada flagellifera (Ceramiales, Rhodophyta) from the Canary Islands, Spain: a new record for the eastern Atlantic Ocean based on morphological and molecular evidence. Botanica Marina. 53, 31-40. [39] Martin-Lescanne J, Rousseau F, de Reviers B, Payri C, Couloux A, Cruaud C, Le Gall L. 2010. Phylogenetic analyses of the Laurencia complex (Rhodomelaceae, Ceramiales) support recognition of five genera: Chondrophycus, Laurencia, Osmundea, Palisada and Yuzurua stat. nov. European Journal of Phycology. 45(1), 51-61. [40] Sentíes A, Díaz-Larrea J, Cassano V, Gil-Rodríguez MC, Fujii MT.2011. Laurencia marilzae (Ceramiales, Rhodophyta) from the Mexican Caribbean: A new record for the tropical western atlantic. Bulletin of Marine Science. 87(3), 681-686. [41] Morton BR, Levin JA. 1997. The atypical codon usage of the plant psbA gene may be the remnant of an ancestral bias. Proceedings of National Academy of Sciencies. 94, 11434-11438.