Phylogenetic analyses of the genes involved in carotenoid biosynthesis in algae

WANG Shanshan; ZHANG Lei; CHI Shan; WANG Guoliang; WANG Xumin; LIU Tao; TANG Xuexi

doi:10.1007/s13131-018-1178-4

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Article Navigation > Acta Oceanologica Sinica > 2018 > 37(4): 89-101

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

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Phylogenetic analyses of the genes involved in carotenoid biosynthesis in algae

doi: 10.1007/s13131-018-1178-4

1.
College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
2.
CAS Key Laboratory of Genome Sciences and Information/Beijing Key Laboratory of Genome and Precision Medicine Technologies, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China

Received Date: 2017-01-17

Abstract

Abstract

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.
- carotenoid biosynthesis,
- algae,
- phylogenetic analysis,

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References

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

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