WANG Shanshan, ZHANG Lei, CHI Shan, WANG Guoliang, WANG Xumin, LIU Tao, TANG Xuexi. Phylogenetic analyses of the genes involved in carotenoid biosynthesis in algae[J]. Acta Oceanologica Sinica, 2018, 37(4): 89-101. doi: 10.1007/s13131-018-1178-4
Citation: WANG Shanshan, ZHANG Lei, CHI Shan, WANG Guoliang, WANG Xumin, LIU Tao, TANG Xuexi. Phylogenetic analyses of the genes involved in carotenoid biosynthesis in algae[J]. Acta Oceanologica Sinica, 2018, 37(4): 89-101. doi: 10.1007/s13131-018-1178-4

Phylogenetic analyses of the genes involved in carotenoid biosynthesis in algae

doi: 10.1007/s13131-018-1178-4
  • Received Date: 2017-01-17
  • Carotenoids play a crucial role in absorbing light energy for photosynthesis, as well as in protecting chlorophyll from photodamage. In contrast to the Streptophyta, few studies have examined carotenoid biosynthetic pathways in algae, owing to a shortage of datasets. As part of the 1000 Plants Project, we sequenced and assembled the transcriptomes of 41 marine macroalgal species, including 22 rhodophytes and 19 phaeophytes, and then combined the datasets with publicly available data from GenBank (National Center for Biotechnology Information) and the U.S. Department of Energy Joint Genome Institute. As a result, we identified 68 and 79 full-length homologs in the Rhodophyta and Phaeophyceae, respectively, of seven inferred carotenoid biosynthetic genes, including the genes for phytoene synthase (PSY), phytoene desaturase (PDS), ζ-carotene desaturase (ZDS), ζ-carotene isomerase (Z-ISO), prolycopene isomerase (crtISO), lycopene β-cyclase (LCYB), and lycopene ε-cyclase (LCYE). We found that the evolutionary history of the algal carotenoid biosynthetic pathway was more complex than that of the same pathway in the Streptophyta and, more specifically, that the evolutionary history involved endosymbiotic gene transfer, gene duplication, and gene loss. Almost all of the eukaryotic algae that we examined had inherited the seven carotenoid biosynthesis genes via endosymbiotic gene transfer. Moreover, PSY, crtISO, and the ancestral lycopene cyclase gene (LCY) underwent duplication events that resulted in multiple gene copies, and the duplication and subsequent divergence of LCYB and LCYE specialized and complicated the cyclization of lycopene. Our findings also verify that the loss of LCYE in both the microphytic rhodophytes and phaeophytes explains the differences in their carotenoid patterns, when compared to the macrophytic rhodophytes. These analyses provide a molecular basis for further biochemical and physiological validation in additional algal species and should help elucidate the origin and evolution of carotenoid biosynthetic pathways.
  • Bartnikas T B, Tosques I E, Laratta W P, et al. 1997. Characterization of the nitric oxide reductase-encoding region in Rhodobacter sphaeroides 2.4.3. J Bacteriol, 179(11): 3534-3540
    Bhattacharya D, Medlin L. 1998. Algal phylogeny and the origin of land plants. Plant Physiol, 116(1): 9-15
    Breitenbach J, Sandmann G. 2005. ζ-Carotene cis isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene. Planta, 220(5): 785-793
    Cavalier-Smith T. 1999. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol, 46(4): 347-366
    Chai Chenglin, Fang Jun, Liu Yang, et al. 2011. ZEBRA2, encoding a carotenoid isomerase, is involved in photoprotection in rice. Plant Mol Biol, 75(3): 211-221
    Chen Qian, Jiang Jianguo, Wang Fei. 2007. Molecular phylogenies and evolution of crt genes in algae. Crit Rev Biotechnol, 27(2): 77-91
    Chen Yu, Li Faqiang, Wurtzel E T. 2010. Isolation and characterization of the Z-ISO gene encoding a missing component of carotenoid biosynthesis in plants. Plant Physiol, 153(1): 66-79
    Cui Hongli, Wang Yinchu, Qin Song. 2011. Molecular evolution of lycopene cyclases involved in the formation of carotenoids in eukaryotic algae. Plant Mol Biol Rep, 29(4): 1013-1020
    Cunningham F X, Gantt E. 1998. Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol, 49: 557-583
    Cunningham F X Jr, Lee H, Gantt E. 2007. Carotenoid biosynthesis in the primitive red alga Cyanidioschyzon merolae. Eukaryot Cell, 6(3): 533-545
    Cunningham F X, Pogson B, Sun Zairen, et al. 1996. Functional analysis of the β and ε lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell, 8(9): 1613-1626
    Cunningham F X, Sun Zairen, Chamovitz D, et al. 1994. Molecular structure and enzymatic function of lycopene cyclase from the cyanobacterium Synechococcus sp strain PCC7942. Plant Cell, 6(8): 1107-1121
    Dogbo O, Laferriére A, D’Harlingue A, et al. 1988. Carotenoid biosynthesis: Isolation and characterization of a bifunctional enzyme catalyzing the synthesis of phytoene. Proc Natl Acad Sci USA, 85(19): 7054-7058
    Douzery E J P, Snell E A, Bapteste E, et al. 2004. The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils?.. Proc Natl Acad Sci USA, 101(43): 15386-15391
    Frigaard N U, Maresca J A, Yunker C E, et al. 2004. Genetic manipulation of carotenoid biosynthesis in the green sulfur bacterium Chlorobium tepidum. J Bacteriol, 186(16): 5210-5220
    Giuliano G, Giliberto L, Rosati C. 2002. Carotenoid isomerase: a tale of light and isomers. Trends Plant Sci, 7(10): 427-429
    Gruszecki W I, Strzałka K. 2005. Carotenoids as modulators of lipid membrane physical properties. Biochim Biophys Acta, 1740(2): 108-115
    Hittinger C T, Carroll S B. 2007. Gene duplication and the adaptive evolution of a classic genetic switch. Nature, 449(7163): 677-681
    Isaacson T, Ohad I, Beyer P, et al. 2004. Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants. Plant Physiol, 136(4): 4246-4255
    Johnson M T J, Carpenter E J, Tian Zhijian, et al. 2012. Evaluating methods for isolating total RNA and predicting the success of sequencing phylogenetically diverse plant transcriptomes. PLoS One, 7(11): e50226
    Keeling P J, Palmer J D. 2008. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet, 9(8): 605-618
    Klassen J L. 2010. Phylogenetic and evolutionary patterns in microbial carotenoid biosynthesis are revealed by comparative genomics. PLoS One, 5(6): e11257
    Krubasik P, Sandmann G. 2000. Molecular evolution of lycopene cyclases involved in the formation of carotenoids with ionone end groups. Biochem Soc Trans, 28(6): 806-810
    Ladygin V G. 2000. Biosynthesis of carotenoids in the chloroplasts of algae and higher plants. Russ J Plant Physl, 47(6): 796-814
    Li Ruiqiang, Li Yingrui, Kristiansen K, et al. 2008a. SOAP: short oligonucleotide alignment program. Bioinformatics, 24(5): 713-714
    Li Faqiang, Murillo C, Wurtzel E T. 2007. Maize Y9 encodes a product essential for 15-cis-ζ-carotene isomerization. Plant Physiol, 144(2): 1181-1189
    Li Tianyong, Ren Lei, Zhou Guan, et al. 2012. A suitable method for extracting total RNA from red algae. Transactions of Oceanology and Limnology (in Chinese),(4): 64-71
    Li Faqiang, Vallabhaneni R, Wurtzel E T. 2008b. PSY3, a new member of the phytoene synthase gene family conserved in the Poaceae and regulator of abiotic stress-induced root carotenogenesis. Plant Physiol, 146(3): 1333-1345
    Li Huanqin, Wang Wenlei, Wang Zhaokai, et al. 2016. De novo transcriptome analysis of carotenoid and polyunsaturated fatty acid metabolism in Rhodomonas sp. J Appl Phycol, 28(3): 1649-1656
    Li Ruiqiang, Zhu Hongmei, Ruan Jue, et al. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res, 20(2): 265-272
    Lichtenthaler H K. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol, 148: 350-382
    Lohr M, Im C S, Grossman A R. 2005. Genome-based examination of chlorophyll and carotenoid biosynthesis in Chlamydomonas reinhardtii. Plant Physiol, 138(1): 490-515
    Lund A, Andersson P, Eriksson J, et al. 2008. Automatic fitting procedures for EPR s pectra of disordered systems: matrix diagonalization and perturbation methods applied to fluorocarbon radicals. Spectrochim Acta Part A, 69(5): 1294-300
    Martin W, Herrmann R G. 1998. Gene transfer from organelles to the nucleus: how much, what happens, and why?.. Plant Physiol, 118(1): 9-17
    Martin W, Rujan T, Richly E, et al. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA, 99(19): 12246-12251
    Masamoto K, Wada H, Kaneko T, et al. 2001. Identification of a gene required for cis-to-trans carotene isomerization in carotenogenesis of the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol, 42(12): 1398-1402
    Matthews P D, Luo Ruibai, Wurtzel E T. 2003. Maize phytoene desaturase and ζ-carotene desaturase catalyse a poly-=Z desaturation pathway: implications for genetic engineering of carotenoid content among cereal crops. J Exp Bot, 54(391): 2215-2230
    McFadden G I. 2001. Primary and secondary endosymbiosis and the origin of plastids. J Phycol, 37(6): 951-959
    McFadden G I. 2001. Chloroplast origin and integration. Plant Physiol, 125(1): 50-53
    Millen R S, Olmstead R G, Adams K L, et al. 2001. Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell, 13(3): 645-658
    Moriya Y, Itoh M, Okuda S, et al. 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res, 35(S2): W182-W185
    Ni Ting, Yue Jipei, Sun Guiling, et al. 2012. Ancient gene transfer from algae to animals: mechanisms and evolutionary significance. BMC Evol Biol, 12: 83
    Nisar N, Li Li, Lu Shan, et al. 2015. Carotenoid metabolism in plants. Mol Plant, 8(1): 68-82
    Park H, Kreunen S S, Cuttriss A J, et al. 2002. Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell, 14(2): 321-332
    Ronquist F, Huelsenbeck J P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12): 1572-1574
    Ruiz-Sola M Á, Rodríguez-Concepción M. 2012. Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book, 10: e0158
    Sandmann G. 1994. Carotenoid biosynthesis in microorganisms and plants. Eur J Biochem, 223(1): 7-24
    Sandmann G. 2002. Molecular evolution of carotenoid biosynthesis from bacteria to plants. Physiol Plant, 116(4): 431-440
    Sandmann G. 2009. Evolution of carotene desaturation: the complication of a simple pathway. Arch Biochem Biophys, 483(2): 169-174
    Sievers F, Wilm A, Dineen D, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol, 7: 539
    Stickforth P, Steiger S, Hess W R, et al. 2003. A novel type of lycopene ε-cyclase in the marine cyanobacterium Prochlorococcus marinus MED4. Arch Microbiol, 179(6): 409-415
    Takaichi S. 2011. Carotenoids in algae: distributions, biosyntheses and functions. Mar Drugs, 9(6): 1101-1118
    Takaichi S, Yokoyama A, Mochimaru M, et al. 2016. Carotenogenesis diversification in phylogenetic lineages of Rhodophyta. J Phycol, 52(3): 329-338
    Tamura K, Peterson D, Peterson N, et al. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol, 28(10): 2731-2739
    Thompson J D, Gibson T J, Plewniak F, et al. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res, 25(24): 4876-4882
    Timmis J N, Ayliffe M A, Huang C Y, et al. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet, 5(2): 123-135
    Tran D, Haven J, Qiu Weigang, et al. 2009. An update on carotenoid biosynthesis in algae: phylogenetic evidence for the existence of two classes of phytoene synthase. Planta, 229(3): 723-729
    Vílchez C, Forján E, Cuaresma M, et al. 2011. Marine carotenoids: biological functions and commercial applications. Mar Drugs, 9(3): 319-333
    Walter M H, Strack D. 2011. Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep, 28(4): 663-692
    Yu Qiuju, Ghisla S, Hirschberg J, et al. 2011. Plant carotene cis-trans isomerase CRTISO: a new member of the FADred-dependent flavoproteins catalyzing non-redox reactions. J Biol Chem, 286(10): 8666-8676
  • Relative Articles

  • Cited by

    Periodical cited type(14)

    1. Cheng-Ling Li, Jia-Qiu Pu, Wei Zhou, et al. Functional Characterization of the First Bona Fide Phytoene Synthase in Red Algae from Pyropia yezoensis. Marine Drugs, 2024, 22(6): 257. doi:10.3390/md22060257
    2. Amirreza Zarekarizi, Linn Hoffmann, David J. Burritt. The potential of manipulating light for the commercial production of carotenoids from algae. Algal Research, 2023, 71: 103047. doi:10.1016/j.algal.2023.103047
    3. Rao Yao, Wen Fu, Ming Du, et al. Carotenoids Biosynthesis, Accumulation, and Applications of a Model Microalga Euglenagracilis. Marine Drugs, 2022, 20(8): 496. doi:10.3390/md20080496
    4. Parminder Kaur Narang, Jyotirmayee Dey, Soumya Ranjan Mahapatra, et al. Genome-based identification and comparative analysis of enzymes for carotenoid biosynthesis in microalgae. World Journal of Microbiology and Biotechnology, 2022, 38(1) doi:10.1007/s11274-021-03188-y
    5. Priyanka Sirohi, Hariom Verma, Sandeep Kumar Singh, et al. Microalgal Carotenoids: Therapeutic Application and Latest Approaches to Enhance the Production. Current Issues in Molecular Biology, 2022, 44(12): 6257. doi:10.3390/cimb44120427
    6. Haimin Chen, Jeffrey Shih-Chieh Chu, Juanjuan Chen, et al. Insights into the Ancient Adaptation to Intertidal Environments by Red Algae Based on a Genomic and Multiomics Investigation of Neoporphyra haitanensis. Molecular Biology and Evolution, 2022, 39(1) doi:10.1093/molbev/msab315
    7. Kunal Seth, Ashwani Kumar, Rajesh P. Rastogi, et al. Bioprospecting of fucoxanthin from diatoms — Challenges and perspectives. Algal Research, 2021, 60: 102475. doi:10.1016/j.algal.2021.102475
    8. Gerhard Sandmann. Diversity and origin of carotenoid biosynthesis: its history of coevolution towards plant photosynthesis. New Phytologist, 2021, 232(2): 479. doi:10.1111/nph.17655
    9. Amit Kumar Gupta, Kunal Seth, Kirti Maheshwari, et al. Biosynthesis and extraction of high-value carotenoid from algae. Frontiers in Bioscience-Landmark, 2021, 26(6) doi:10.52586/4932
    10. Bárbara A. Rebelo, Sara Farrona, M. Rita Ventura, et al. Canthaxanthin, a Red-Hot Carotenoid: Applications, Synthesis, and Biosynthetic Evolution. Plants, 2020, 9(8): 1039. doi:10.3390/plants9081039
    11. Mehmooda Fayyaz, Kit Wayne Chew, Pau Loke Show, et al. Genetic engineering of microalgae for enhanced biorefinery capabilities. Biotechnology Advances, 2020, 43: 107554. doi:10.1016/j.biotechadv.2020.107554
    12. Dinesh Kumar Saini, Hillol Chakdar, Sunil Pabbi, et al. Enhancing production of microalgal biopigments through metabolic and genetic engineering. Critical Reviews in Food Science and Nutrition, 2020, 60(3): 391. doi:10.1080/10408398.2018.1533518
    13. Fanny Lalegerie, Sirine Lajili, Gilles Bedoux, et al. Photo-protective compounds in red macroalgae from Brittany: Considerable diversity in mycosporine-like amino acids (MAAs). Marine Environmental Research, 2019, 147: 37. doi:10.1016/j.marenvres.2019.04.001
    14. Delphine Nègre, Méziane Aite, Arnaud Belcour, et al. Genome–Scale Metabolic Networks Shed Light on the Carotenoid Biosynthesis Pathway in the Brown Algae Saccharina japonica and Cladosiphon okamuranus. Antioxidants, 2019, 8(11): 564. doi:10.3390/antiox8110564

    Other cited types(0)

  • Created with Highcharts 5.0.7Amount of accessChart context menuAbstract Views, HTML Views, PDF Downloads StatisticsAbstract ViewsHTML ViewsPDF Downloads2024-052024-062024-072024-082024-092024-102024-112024-122025-012025-022025-032025-040510152025
    Created with Highcharts 5.0.7Chart context menuAccess Class DistributionFULLTEXT: 30.0 %FULLTEXT: 30.0 %META: 68.8 %META: 68.8 %PDF: 1.2 %PDF: 1.2 %FULLTEXTMETAPDF
    Created with Highcharts 5.0.7Chart context menuAccess Area DistributionBrazil: 2.7 %Brazil: 2.7 %China: 51.2 %China: 51.2 %Gambia: 0.2 %Gambia: 0.2 %Japan: 1.5 %Japan: 1.5 %Korea Republic of: 1.7 %Korea Republic of: 1.7 %Malaysia: 1.0 %Malaysia: 1.0 %Philippines: 0.7 %Philippines: 0.7 %Russian Federation: 11.4 %Russian Federation: 11.4 %United States: 29.5 %United States: 29.5 %BrazilChinaGambiaJapanKorea Republic ofMalaysiaPhilippinesRussian FederationUnited States

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (1387) PDF downloads(562) Cited by(14)
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return