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Coral symbionts evolved a functional polycistronic flavodiiron gene

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Abstract

Photosynthesis in cyanobacteria, green algae, and basal land plants is protected against excess reducing pressure on the photosynthetic chain by flavodiiron proteins (FLV) that dissipate photosynthetic electrons by reducing O2. In these organisms, the genes encoding FLV are always conserved in the form of a pair of two-type isozymes (FLVA and FLVB) that are believed to function in O2 photo-reduction as a heterodimer. While coral symbionts (dinoflagellates of the family Symbiodiniaceae) are the only algae to harbor FLV in photosynthetic red plastid lineage, only one gene is found in transcriptomes and its role and activity remain unknown. Here, we characterized the FLV genes in Symbiodiniaceae and found that its coding region is composed of tandemly repeated FLV sequences. By measuring the O2-dependent electron flow and P700 oxidation, we suggest that this atypical FLV is active in vivo. Based on the amino-acid sequence alignment and the phylogenetic analysis, we conclude that in coral symbionts, the gene pair for FLVA and FLVB have been fused to construct one coding region for a hybrid enzyme, which presumably occurred when or after both genes were inherited from basal green algae to the dinoflagellate. Immunodetection suggested the FLV polypeptide to be cleaved by a post-translational mechanism, adding it to the rare cases of polycistronic genes in eukaryotes. Our results demonstrate that FLV are active in coral symbionts with genomic arrangement that is unique to these species. The implication of these unique features on their symbiotic living environment is discussed.

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References

  • Alboresi A, Storti M, Cendron L, Morosinotto T (2019a) Role and regulation of class-C flavodiiron proteins in photosynthetic organisms. Biochem J 476:2487–2498

    CAS  PubMed  Google Scholar 

  • Alboresi A, Storti M, Morosinotto T (2019b) Balancing protection and efficiency in the regulation of photosynthetic electron transport across plant evolution. New Phytol 221:105–109

    CAS  PubMed  Google Scholar 

  • Allahverdiyeva Y, Ermakova M, Eisenhut M, Zhang P, Richaud P, Hagemann M, Cournac L, Aro EM (2011) Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. J Biol Chem 286:24007–24014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Allahverdiyeva Y, Isojarvi J, Zhang P, Aro EM (2015) Cyanobacterial oxygenic photosynthesis is protected by flavodiiron proteins. Life 5:716–743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, Cournac L, Aro EM (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc Natl Acad Sci USA 110:4111–4116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anisimova M, Gil M, Dufayard J-F, Dessimoz C, Gascuel O (2011) Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol 60:685–699

    PubMed  PubMed Central  Google Scholar 

  • Bachvaroff TR, Place AR (2008) From stop to start: Tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae. PLoS One 3:e2929

    PubMed  PubMed Central  Google Scholar 

  • Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer ELL, Studholme DJ, Yeats C, Eddy SR (2004) The Pfam protein families database. Nucleic Acids Res 32:D138–D141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bersanini L, Allahverdiyeva Y, Battchikova N, Heinz S, Lespinasse M, Ruohisto E, Mustila H, Nickelsen J, Vass I, Aro E-M (2017) Dissecting the photoprotective mechanism encoded by the flv4-2 operon: a distinct contribution of Sll0218 in photosystem II stabilization. Plant Cell Environ 40:378–389

    CAS  PubMed  Google Scholar 

  • Brown KA, Guo Z, Tokmina-Lukaszewska M, Scott LW, Lubner CE, Smolinski S, Mulder DW, Bothner B, King PW (2019) The oxygen reduction reaction catalyzed by Synechocystis sp. PCC 6803 flavodiiron proteins. Sustain Energy Fuels 3:3191–3200

    CAS  Google Scholar 

  • Burlacot A, Richaud P, Gosset A, Li-Beisson Y, Peltier G (2020) Algal photosynthesis converts nitric oxide into nitrous oxide. Proc Natl Acad Sci USA 117:2704–2709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burlacot A, Sawyer A, Cuiné S, Auroy-Tarrago P, Blangy S, Happe T, Peltier G (2018) Flavodiiron-mediated O2 photoreduction links H2 production with CO2 fixation during the anaerobic induction of photosynthesis. Plant Physiol 177:1639–1649

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaux F, Burlacot A, Mekhalfi M, Auroy P, Blangy S, Richaud P, Peltier G (2017) Flavodiiron proteins promote fast and transient O2 photoreduction in Chlamydomonas. Plant Physiol 174:1825–1836

    CAS  PubMed  PubMed Central  Google Scholar 

  • Curien G, Flori S, Villanova V, Magneschi L, Giustini C, Forti G, Matringe M, Petroutsos D, Kuntz M, Finazzi G (2016) The water to water cycles in microalgae. Plant Cell Physiol 57:1354–1363

    CAS  PubMed  Google Scholar 

  • Dang KV, Pierangelini M, Roberty S, Cardol P (2019) Alternative photosynthetic electron transfers and bleaching phenotypes upon acute heat stress in Symbiodinium and Breviolum spp. (Symbiodiniaceae) in culture. Front Marine Sci. https://doi.org/10.3389/fmars.2019.00656

    Article  Google Scholar 

  • Dietz K-J, Turkan I, Krieger-Liszkay A (2016) Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol 171:1541–1550

    CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Enright AJ, Iliopoulos I, Kyrpides NC, Ouzounis CA (1999) Protein interaction maps for complete genomes based on gene fusion events. Nature 402:86–90

    CAS  PubMed  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360

    CAS  PubMed  Google Scholar 

  • Fang W, Si Y, Douglass S, Casero D, Merchant SS, Pellegrini M, Ladunga I, Liu P, Spalding MH (2012) Transcriptome-wide changes in Chlamydomonas reinhardtii gene expression regulated by carbon dioxide and the CO2-concentrating mechanism regulator CIA5/CCM1. Plant Cell 24:1876–1893

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Noctor G (2020) Redox homeostasis and signaling in a higher-CO2 world. Annu Rev Plant Biol 71:157–182

    CAS  PubMed  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta, Gen Subj 990:87–92

    CAS  Google Scholar 

  • Gerotto C, Alboresi A, Meneghesso A, Jokel M, Suorsa M, Aro E-M, Morosinotto T (2016) Flavodiiron proteins act as safety valve for electrons in Physcomitrella patens. Proc Natl Acad Sci USA 113:12322–12327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    CAS  PubMed  Google Scholar 

  • Hanke GT, Satomi Y, Shinmura K, Takao T, Hase T (2011) A screen for potential ferredoxin electron transfer partners uncovers new, redox dependent interactions. Biochim Biophys Acta Proteins Proteomics 1814:366–374

    CAS  Google Scholar 

  • Hase T, Schürmann P, Knaff DB (2006) The interaction of ferredoxin with ferredoxin-dependent enzymes. In: Golbeck JH (ed) Photosystem I: the light-driven plastocyanin: ferredoxin oxidoreductase. Springer, Netherlands, Dordrecht, pp 477–498

    Google Scholar 

  • Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, Ohad I, Kaplan A (2003) Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13:230–235

    CAS  PubMed  Google Scholar 

  • Hiller RG, Wrench PM, Sharples FP (1995) The light-harvesting chlorophyll a-c-binding protein of dinoflagellates: a putative polyprotein. FEBS Lett 363:175–178

    CAS  PubMed  Google Scholar 

  • Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2017) UFBoot2: Improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522

    PubMed Central  Google Scholar 

  • Ilík P, Pavlovič A, Kouřil R, Alboresi A, Morosinotto T, Allahverdiyeva Y, Aro E-M, Yamamoto H, Shikanai T (2017) Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms. New Phytol 214:967–972

    PubMed  Google Scholar 

  • Inoue K, Fujii T, Yokoyama E, Matsuura K, Hiyama T, Sakurai H (1989) The photoinhibition site of photosystem I in isolated chloroplasts under extremely reducing conditions. Plant Cell Physiol 30:65–71

    CAS  Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607

    CAS  PubMed  Google Scholar 

  • Kleessen S, Irgang S, Klie S, Giavalisco P, Nikoloski Z (2015) Integration of transcriptomics and metabolomics data specifies the metabolic response of chlamydomonas to rapamycin treatment. Plant J 81:822–835

    CAS  PubMed  Google Scholar 

  • Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192:261–268

    CAS  Google Scholar 

  • Kozuleva M, Petrova A, Milrad Y, Semenov A, Ivanov B, Redding KE, Yacoby I (2021) Phylloquinone is the principal Mehler reaction site within photosystem I in high light. Plant Physiol. https://doi.org/10.1093/plphys/kiab221

  • Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346

    CAS  PubMed  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570-2580.e2576

    CAS  PubMed  Google Scholar 

  • Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530–1534

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mustila H, Paananen P, Battchikova N, Santana-Sánchez A, Muth-Pawlak D, Hagemann M, Aro E-M, Allahverdiyeva Y (2016) The flavodiiron protein Flv3 functions as a homo-oligomer during stress acclimation and is distinct from the Flv1/Flv3 hetero-oligomer specific to the O2 photoreduction pathway. Plant Cell Physiol 57:1468–1483

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nikkanen L, Santana Sánchez A, Ermakova M, Rögner M, Cournac L, Allahverdiyeva Y (2020) Functional redundancy between flavodiiron proteins and NDH-1 in Synechocystis sp. PCC 6803. Plant J 103:1460–1476

    CAS  PubMed  Google Scholar 

  • Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125–134

    CAS  PubMed  Google Scholar 

  • Pérez-Pérez ME, Mauriès A, Maes A, Tourasse NJ, Hamon M, Lemaire SD, Marchand CH (2017) The deep thioredoxome in Chlamydomonas reinhardtii: New insights into redox regulation. Mol Plant 10:1107–1125

    PubMed  Google Scholar 

  • Roach T, Na CS, Krieger-Liszkay A (2015) High light-induced hydrogen peroxide production in Chlamydomonas reinhardtii is increased by high CO2 availability. Plant J 81:759–766

    CAS  PubMed  Google Scholar 

  • Roberty S, Bailleul B, Berne N, Franck F, Cardol P (2014) PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol 204:81–91

    CAS  PubMed  Google Scholar 

  • Roberty S, Fransolet D, Cardol P, Plumier J-C, Franck F (2015) Imbalance between oxygen photoreduction and antioxidant capacities in Symbiodinium cells exposed to combined heat and high light stress. Coral Reefs 34:1063–1073

    Google Scholar 

  • Romão CV, Vicente JB, Borges PT, Frazão C, Teixeira M (2016a) The dual function of flavodiiron proteins: oxygen and/or nitric oxide reductases. J Biol Inorg Chem 21:39–52

    PubMed  Google Scholar 

  • Romão CV, Vicente JB, Borges PT, Victor BL, Lamosa P, Silva E, Pereira L, Bandeiras TM, Soares CM, Carrondo MA, Turner D, Teixeira M, Frazão C (2016b) Structure of Escherichia coli flavodiiron nitric oxide reductase. J Mol Biol 428:4686–4707

    PubMed  Google Scholar 

  • Sétif P, Shimakawa G, Krieger-Liszkay A, Miyake C (2020) Identification of the electron donor to flavodiiron proteins in Synechocystis sp. PCC 6803 by in vivo spectroscopy. Biochim Biophys Acta Bioenerg 1861:148256

    PubMed  Google Scholar 

  • Santana-Sanchez A, Solymosi D, Mustila H, Bersanini L, Aro E-M, Allahverdiyeva Y (2019) Flavodiiron proteins 1–to-4 function in versatile combinations in O2 photoreduction in cyanobacteria. eLife 8:e45766

    PubMed  PubMed Central  Google Scholar 

  • Schmitt F-J, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim Biophys Acta Bioenerg 1837:835–848

    CAS  Google Scholar 

  • Sejima T, Takagi D, Fukayama H, Makino A, Miyake C (2014) Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant Cell Physiol 55:1184–1193

    CAS  PubMed  Google Scholar 

  • Shimakawa G, Ishizaki K, Tsukamoto S, Tanaka M, Sejima T, Miyake C (2017a) The liverwort, Marchantia, drives alternative electron flow using a flavodiiron protein to protect PSI. Plant Physiol 173:1636–1647

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shimakawa G, Miyake C (2018) Oxidation of P700 ensures robust photosynthesis. Front Plant Sci 9:1617

    PubMed  PubMed Central  Google Scholar 

  • Shimakawa G, Murakami A, Niwa K, Matsuda Y, Wada A, Miyake C (2019) Comparative analysis of strategies to prepare electron sinks in aquatic photoautotrophs. Photosynth Res 139:401–411

    CAS  PubMed  Google Scholar 

  • Shimakawa G, Shaku K, Miyake C (2016) Oxidation of P700 in photosystem I is essential for the growth of cyanobacteria. Plant Physiol 172:1443–1450

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shimakawa G, Shaku K, Nishi A, Hayashi R, Yamamoto H, Sakamoto K, Makino A, Miyake C (2015) FLAVODIIRON2 and FLAVODIIRON4 proteins mediate an oxygen-dependent alternative electron flow in Synechocystis sp. PCC 6803 under CO2-limited conditions. Plant Physiol 167:472–480

    CAS  PubMed  Google Scholar 

  • Shimakawa G, Watanabe S, Miyake C (2017) A carbon dioxide limitation-inducible protein, ColA, supports the growth of Synechococcus sp. PCC 7002. Marine Drugs 15:390

    PubMed Central  Google Scholar 

  • Shoguchi E, Beedessee G, Hisata K, Tada I, Narisoko H, Satoh N, Kawachi M, Shinzato C (2020) A new dinoflagellate genome illuminates a conserved gene cluster involved in sunscreen biosynthesis. Genom Biol Evol. https://doi.org/10.1093/gbe/evaa235

    Article  Google Scholar 

  • Shoguchi E, Beedessee G, Tada I, Hisata K, Kawashima T, Takeuchi T, Arakaki N, Fujie M, Koyanagi R, Roy MC (2018) Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes. BMC Genomics 19:458

    PubMed  PubMed Central  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    CAS  PubMed  Google Scholar 

  • Steenwyk JL, Buida TJ III, Li Y, Shen X-X, Rokas A (2020) ClipKIT: a multiple sequence alignment trimming software for accurate phylogenomic inference. PLoS Biol 18:e3001007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi D, Ishizaki K, Hanawa H, Mabuchi T, Shimakawa G, Yamamoto H, Miyake C (2017) Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I. Physiol Plant 161:56–74

    CAS  PubMed  Google Scholar 

  • Takishita K, Patron NJ, Ishida K-I, Maruyama T, Keeling PJ (2005) A transcriptional fusion of genes encoding glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and enolase in dinoflagellates. J Eukaryotic Microbiol 52:343–348

    CAS  Google Scholar 

  • Tulin F, Cross FR (2015) Cyclin-dependent kinase regulation of diurnal transcription in Chlamydomonas. Plant Cell 27:2727–2742

    CAS  PubMed  PubMed Central  Google Scholar 

  • Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59:1069–1080

    CAS  PubMed  Google Scholar 

  • Vicente JB, Gomes CM, Wasserfallen A, Teixeira M (2002) Module fusion in an A-type flavoprotein from the cyanobacterium Synechocystis condenses a multiple-component pathway in a single polypeptide chain. Biochem Biophys Res Commun 294:82–87

    CAS  PubMed  Google Scholar 

  • Waller RF, Slamovits CH, Keeling PJ (2006) Lateral gene transfer of a multigene region from cyanobacteria to dinoflagellates resulting in a novel plastid-targeted fusion protein. Mol Biol Evol 23:1437–1443

    CAS  PubMed  Google Scholar 

  • Yamamoto H, Takahashi S, Badger MR, Shikanai T (2016) Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nat Plants 2:16012

    CAS  PubMed  Google Scholar 

  • Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors gratefully thank Dr. Anja Krieger-Liszkay (CNRS Paris-Saclay, France) for the kind advices in writing the manuscript. The authors thank Dr. Gilles Peltier (CEA Cadarache, France) for kindly providing FLVA antibody.

Funding

This work was supported by the Japan Society for the Promotion of Science (JSPS; Grant No. 20J00105 to G.S.).

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Author notes

  1. Adrien Burlacot

    Present address: Department of Plant and Microbial Biology, Howard Hughes Medical Institute, University of California, 111 Koshland Hall, Berkeley, CA, 94720-3102, USA

Authors and Affiliations

  1. Research Center for Solar Energy Chemistry, Osaka University, 1-3 Machikaneyama, Toyonaka, Osaka, 560-8531, Japan

    Ginga Shimakawa & Shuji Nakanishi

  2. Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa, 904-0495, Japan

    Eiichi Shoguchi

  3. Aix Marseille University, CEA, CNRS, Institut de Biosciences Et Biotechnologies Aix-Marseille, CEA Cadarache, 13108, Saint Paul-Lez-Durance, France

    Adrien Burlacot

  4. Division of Integrated Life Science, Graduate School of Biostudies, Kyoto University, Sakyo, Kyoto, 606-8502, Japan

    Kentaro Ifuku, Yufen Che & Minoru Kumazawa

  5. Graduate School of Engineering Science, Osaka University, 1-3 Machikaneyama, Toyonaka, Osaka, 560-8631, Japan

    Kenya Tanaka & Shuji Nakanishi

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  1. Ginga Shimakawa
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Contributions

GS conceived the research plan; GS performed all the physiological experiments; GS, ES, KI, and MK performed bioinformatic analyses; GS, KI, and YC performed immunoblotting with the support by AB; KT and SN provided technical assistance to GS; all the authors analyzed the data; GS and AB drafted the manuscript with support by all other authors.

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Correspondence to Ginga Shimakawa.

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Nucleotide and amino-acid sequences data studied in this study can be found on the database of National Center for Biotechnology Information (NCBI, https://www.ncbi.nlm.nih.gov), JGI Genome Portal (https://genome.jgi.doe.gov), OIST Marine Genomics Unit (https://marinegenomics.oist.jp), CyanoBase (http://genome.microbedb.jp/cyanobase), and MarpolBase (https://marchantia.info) following the accession numbers: Escherichia FDP (WP_000029589), S6803 FLV1 (Sll1521), FLV2 (Sll0219), FLV3 (Sll0550), and FLV4 (Sll0217), S7942 FLV1 (1810) and FLV3 (1809), S7002 FLV1 (A1743) and FLV3 (A1321), Chlamydomonas FLVA (Cre12.g531900) and FLVB (Cre16.g691800), Coccomyxa FLVA (54807) and FLVB (45048), Micromonas FLVA (90715) and FLVB (58403), Ostreococcus FLVA (e_gw1.02.00.129) and FLVB (fgenesh1_pm.C_Chr_02.0001000066), Marchantia FLVA (Mapoly0005s0210) and FLVB (Mapoly0103s0039), Physcomitrella FLVA (Pp3c14_14450V3) and FLVB (Pp3c1_26720V3), Selaginella FLVA (143660) and FLVB (448328), Symbiodinium FLV (s632_g30), Cladocopium FLV (comp44467), and Durusdinium FLV (TRINITY_DN39309).

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Shimakawa, G., Shoguchi, E., Burlacot, A. et al. Coral symbionts evolved a functional polycistronic flavodiiron gene. Photosynth Res 151, 113–124 (2022). https://doi.org/10.1007/s11120-021-00867-7

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