Heme is essential for all organisms. The composition and location of the pathway for heme biosynthesis, have been influenced by past endosymbiotic events and organelle evolution in eukaryotes. Endosymbioses led to temporary redundancy of the enzymes and the genes involved. Genes were transferred to the nucleus from different endosymbiotic partners, and their multiple copies were either lost or retained, resulting in a mosaic pathway. This mosaic is particularly complex in organisms with eukaryote-derived plastids, such as diatoms. The plastids of diatoms are clearly derived from red algae. However, it is not entirely clear whether they were acquired directly from a red algal ancestor or indirectly in higher-order endosymbioses. In the diatom Phaeodactylum tricornutum, most enzymes of the pathway are present in a single copy, but three, glutamyl-tRNA synthetase (GluRS), uroporphyrinogen decarboxylase (UROD) and coproporphyrinogen oxidase (CPOX), are encoded in multiple copies. These are not direct paralogs resulting from gene duplication within the lineage but were acquired horizontally during the plastid endosymbioses. While some iso-enzymes originate from the host cell, others originate either from the genome of the cyanobacterial ancestor of all plastids or from the nuclear genome of the eukaryotic ancestor of the diatom complex plastid, a rhodophyte or an alga containing rhodophyte-derived plastids, a situation known as pseudoparalogy. Using green fluorescent protein-tagged expression and immunogold labeling, we experimentally localized all enzymes of the pathway in P. tricornutum, and confirmed their localization in the plastid, with a few possible exceptions. Our meta-analyses of transcription data showed that the pseudoparalogs are differentially expressed in response to nitrate starvation, blue light, high light, high CO2, and the cell cycle. Taken together, our findings emphasize that the evolution of complex plastids via endosymbiosis has a direct impact not only on the genetics but also on the physiology of resulting organisms.

Department of Computational Quantitative and Synthetic Biology INSERM Sorbonne Université Paris France

Faculty of Science University of South Bohemia České Budějovice Czechia

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czechia

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Agarwal A., Levitan O., Cruz de Carvalho H., Falkowski P. G. (2023). Light-dependent signal transduction in the marine diatom Phaeodactylum tricornutum. Proc. Natl. Acad. Sci U S A. 120 (11), e2216286120. doi: 10.1073/pnas.2216286120 PubMed DOI PMC

Ait-Mohamed O., Novák Vanclová A. M. G., Joli N., Liang Y., Zhao X., Genovesio A., et al. . (2020). PhaeoNet: A holistic RNAseq-based portrait of transcriptional coordination in the model diatom phaeodactylum tricornutum. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.590949 PubMed DOI PMC

Almagro Armenteros J. J., Salvatore M., Emanuelsson O., Winther O., von Heijne G., Elofsson A., et al. . (2019. a). Detecting sequence signals in targeting peptides using deep learning. Life Sci. Alliance 2, e201900429. doi: 10.26508/lsa.201900429 PubMed DOI PMC

Almagro Armenteros J. J., Tsirigos K. D., Sønderby C. K., Petersen T. N., Winther O., Brunak S., et al. . (2019. b). SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat. Biotechnol. 37, 420–423. doi: 10.1038/s41587-019-0036-z PubMed DOI

Armbrust E. V., Berges J. A., Bowler C., Green B. R., Martinez D., Putnam N. H., et al. . (2004). The genome of the diatom thalassiosira pseudonana : ecology, evolution, and metabolism. Sci. (1979) 306, 79–86. doi: 10.1126/science.1101156 PubMed DOI

Ashworth J., Turkarslan S., Harris M., Orellana M. V., Baliga N. S. (2016). Pan-transcriptomic analysis identifies coordinated and orthologous functional modules in the diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum. Mar. Genomics 26, 21–28. doi: 10.1016/j.margen.2015.10.011 PubMed DOI

Azuma T., Pánek T., Tice A. K., Kayama M., Kobayashi M., Miyashita H., et al. . (2022). An enigmatic stramenopile sheds light on early evolution in ochrophyta plastid organellogenesis. Mol. Biol. Evol. 39, msac065. doi: 10.1093/molbev/msac065 PubMed DOI PMC

Beale S. I., Gough S. P., Granick S. (1975). Biosynthesis of delta-aminolevulinic acid from the intact carbon skeleton of glutamic acid in greening barley. Proc. Natl. Acad. Sci. 72, 2719–2723. doi: 10.1073/pnas.72.7.2719 PubMed DOI PMC

Bhaya D., Grossman A. (1991). Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol. Gen. Genet. 229, 400–404. doi: 10.1007/BF00267462 PubMed DOI

Bolser D. M., Staines D. M., Perry E., Kersey P. J. (2017). Ensembl plants: integrating tools for visualizing, mining, and analyzing plant genomic data. Methods Mol. Biol. 1533, 1–31. doi: 10.1007/978-1-4939-6658-5_1 PubMed DOI

Bowler C., Allen A. E., Badger J. H., Grimwood J., Jabbari K., Kuo A., et al. . (2008). The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239–244. doi: 10.1038/nature07410 PubMed DOI

Brzezowski P., Richter A. S., Grimm B. (2015). Regulation and function of tetrapyrrole biosynthesis in plants and algae. Biochim. Biophys. Acta (BBA) - Bioenergetics 1847, 968–985. doi: 10.1016/j.bbabio.2015.05.007 PubMed DOI

Chow K.-S., Singh D. P., Roper J. M., Smith A. G. (1997). A Single Precursor Protein for Ferrochelatase-I fromArabidopsis Is Imported in Vitro into Both Chloroplasts and Mitochondria. J. Biol. Chem. 272, 27565–27571. doi: 10.1074/jbc.272.44.27565 PubMed DOI

Chow K. S., Singh D. P., Walker A. R., Smith A. G. (1998). Two different genes encode ferrochelatase in Arabidopsis: mapping, expression and subcellular targeting of the precursor proteins. Plant J. 15, 531–541. doi: 10.1046/j.1365-313X.1998.00235.x PubMed DOI

Cihlář J., Füssy Z., Horák A., Oborník M. (2016). Evolution of the tetrapyrrole biosynthetic pathway in secondary algae: conservation, redundancy and replacement. PloS One 11, e0166338. doi: 10.1371/journal.pone.0166338 PubMed DOI PMC

Cihlář J., Füssy Z., Oborník M. (2019). “Chapter Eight - Evolution of tetrapyrrole pathway in eukaryotic phototrophs,” in Advances in Botanical Research, ed. Grimm B. (Academic Press; ), 273–309. doi: 10.1016/bs.abr.2018.12.003 DOI

Dailey H. A., Dailey T. A., Wu C.-K., Medlock A. E., Rose J. P., Wang K.-F. (2000). Ferrochelatase at the millennium: structures, mechanisms and [2Fe-2S] clusters. Cell. Mol. Life Sci. 57, 1909–1926. doi: 10.1007/PL00000672 PubMed DOI PMC

Dorrell R. G., Azuma T., Nomura M., Audren de Kerdrel G., Paoli L., Yang S., et al. . (2019). Principles of plastid reductive evolution illuminated by nonphotosynthetic chrysophytes. Proc. Natl. Acad. Sci. 116, 6914–6923. doi: 10.1073/pnas.1819976116 PubMed DOI PMC

Dugdale R. C., Wilkerson F. P. (1998). Silicate regulation of new production in the equatorial Pacific upwelling. Nature 391, 270–273. doi: 10.1038/34630 DOI

Durham B., Millett F. S. (2005). Iron: heme proteins & Electron transport. In Encyclopedia of Inorganic and Bioinorganic Chemistry, Scott R. A. (Ed.). doi: 10.1002/9781119951438.eibc0098 DOI

Falciatore A., Casotti R., Leblanc C., Abrescia C., Bowler C. (1999). Transformation of nonselectable reporter genes in marine diatoms. Mar. Biotechnol. 1, 239–251. doi: 10.1007/PL00011773 PubMed DOI

Ferreira G. C., Andrew T. L., Karr S. W., Dailey H. A. (1988). Organization of the terminal two enzymes of the heme biosynthetic pathway. Orientation of protoporphyrinogen oxidase and evidence for a membrane complex. J. Biol. Chem. 263, 3835–3839. doi: 10.1016/S0021-9258(18)69000-3 PubMed DOI

Filloramo G. V., Curtis B. A., Blanche E., Archibald J. M. (2021). Re-examination of two diatom reference genomes using long-read sequencing. BMC Genomics 22, 379. doi: 10.1186/s12864-021-07666-3 PubMed DOI PMC

Füssy Z., Oborník M. (2018). Complex endosymbioses I: from primary to complex plastids, multiple independent events. Methods Mol. Biol. 1829, 17–35. doi: 10.1007/978-1-4939-8654-5_2 PubMed DOI

Giguere D. J., Bahcheli A. T., Slattery S. S., Patel R. R., Browne T. S., Flatley M., et al. . (2022). Telomere-to-telomere genome assembly of Phaeodactylum tricornutum. PeerJ 10, e13607. doi: 10.7717/peerj.13607 PubMed DOI PMC

Gile G. H., Moog D., Slamovits C. H., Maier U.-G., Archibald J. M. (2015). Dual organellar targeting of aminoacyl-tRNA synthetases in diatoms and cryptophytes. Genome Biol. Evol. 7, 1728–1742. doi: 10.1093/gbe/evv095 PubMed DOI PMC

Gould S. B., Sommer M. S., Kroth P. G., Gile G. H., Keeling P. J., Maier U.-G. (2006). Nucleus-to-nucleus gene transfer and protein retargeting into a remnant cytoplasm of cryptophytes and diatoms. Mol. Biol. Evol. 23, 2413–2422. doi: 10.1093/molbev/msl113 PubMed DOI

Grossman A., Manodori A., Snyder D. (1990). Light-harvesting proteins of diatoms: Their relationship to the chlorophyll a/b binding proteins of higher plants and their mode of transport into plastids. Mol. Gen. Genet. 224, 91–100. doi: 10.1007/BF00259455 PubMed DOI

Gruber A., McKay C., Oborník M., Rocap G. (2023). Multi class intracellular protein targeting predictions in diatoms and other algae with complex plastids: ASAFind 2.0. arXiv. vol. arXiv:2303.02488. doi: 10.48550/arXiv.2303.02488 DOI

Gruber A., Oborník M. (2024). “Evolution of plastids and mitochondria in diatoms,” in Diatom Photosynthesis: From Primary Production to High Value. Eds. Goessling J. W., Serôdio J., Lavaud J. (Scrivener Publishing LLC, Berverly: ), 79–110.

Gruber A., Rocap G., Kroth P. G., Armbrust E. V., Mock T. (2015). Plastid proteome prediction for diatoms and other algae with secondary plastids of the red lineage. Plant J. 81, 519–528. doi: 10.1111/tpj.12734 PubMed DOI PMC

Gschloessl B., Guermeur Y., Cock J. M. (2008). HECTAR: A method to predict subcellular targeting in heterokonts. BMC Bioinf. 9, 393. doi: 10.1186/1471-2105-9-393 PubMed DOI PMC

Guillard R. R. L. (1975). “Culture of Phytoplankton for Feeding Marine Invertebrates,” in Culture of Marine Invertebrate Animals (Springer US, Boston, MA: ), 29–60. doi: 10.1007/978-1-4615-8714-9_3 DOI

Hedtke B., Strätker S. M., Pulido A. C. C., Grimm B. (2023). Two isoforms of Arabidopsis protoporphyrinogen oxidase localize in different plastidal membranes. Plant Physiol. 192, 871–885. doi: 10.1093/plphys/kiad107 PubMed DOI PMC

Hey D., Ortega-Rodes P., Fan T., Schnurrer F., Brings L., Hedtke B., et al. . (2016). Transgenic tobacco lines expressing sense or antisense FERROCHELATASE 1 RNA show modified ferrochelatase activity in roots and provide experimental evidence for dual localization of ferrochelatase 1. Plant Cell Physiol. 57, 2576–2585. doi: 10.1093/pcp/pcw171 PubMed DOI

Huysman M. J. J., Fortunato A. E., Matthijs M., Costa B. S., Vanderhaeghen R., Van den Daele H., et al. . (2013). AUREOCHROME1a-Mediated Induction of the Diatom-Specific Cyclin dsCYC2 Controls the Onset of Cell Division in Diatoms (Phaeodactylum tricornutum). Plant Cell 25, 215–228. doi: 10.1105/tpc.112.106377 PubMed DOI PMC

Jumper J., Evans R., Pritzel A., Green T., Figurnov M., Ronneberger O., et al. . (2021). Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589. doi: 10.1038/s41586-021-03819-2 PubMed DOI PMC

Keeling P. J., Archibald J. M. (2008). Organelle evolution: what’s in a name? Curr. Biol. 18, R345–R347. doi: 10.1016/j.cub.2008.02.065 PubMed DOI

Kobayashi K., Masuda T., Tajima N., Wada H., Sato N. (2014). Molecular phylogeny and intricate evolutionary history of the three isofunctional enzymes involved in the oxidation of protoporphyrinogen IX. Genome Biol. Evol. 6, 2141–2155. doi: 10.1093/gbe/evu170 PubMed DOI PMC

Koch M., Breithaupt C., Kiefersauer R., Freigang J., Huber R., Messerschmidt A. (2004). Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. EMBO J. 23, 1720–1728. doi: 10.1038/sj.emboj.7600189 PubMed DOI PMC

Koonin E. V. (2005). Orthologs, paralogs, and evolutionary genomics. Annu. Rev. Genet. 39, 309–338. doi: 10.1146/annurev.genet.39.073003.114725 PubMed DOI

Kořený L., Oborník M. (2011). Sequence evidence for the presence of two tetrapyrrole pathways in euglena gracilis. Genome Biol. Evol. 3, 359–364. doi: 10.1093/gbe/evr029 PubMed DOI PMC

Kořený L., Oborník M., Horáková E., Waller R. F., Lukeš J. (2022). The convoluted history of haem biosynthesis. Biol. Rev. 97, 141–162. doi: 10.1111/brv.12794 PubMed DOI

Kořený L., Oborník M., Lukeš J. (2013). Make it, take it, or leave it: heme metabolism of parasites. PloS Pathog. 9, e1003088. doi: 10.1371/journal.ppat.1003088 PubMed DOI PMC

Lang M., Apt K. E., Kroth P. G. (1998). Protein transport into “Complex” Diatom plastids utilizes two different targeting signals. J. Biol. Chem. 273, 30973–30978. doi: 10.1074/jbc.273.47.30973 PubMed DOI

Layer G., Jahn D., Deery E., Lawrence A. D., Warren M. J. (2010). Biosynthesis of Heme and Vitamin B12. Comprehensive Natural Products II: Chemistry and Biology. 7, 445–499. doi: 10.1016/B978-008045382-8.00144-1 DOI

Maheswari U., Montsant A., Goll J., Krishnasamy S., Rajyashri K. R., Patell V. M., et al. . (2005). The diatom EST database. Nucleic Acids Res. 33, D344–D347. doi: 10.1093/nar/gki121 PubMed DOI PMC

Mann M., Serif M., Wrobel T., Eisenhut M., Madhuri S., Flachbart S., et al. . (2020). The aureochrome photoreceptor ptAUREO1a is a highly effective blue light switch in diatoms. iScience 23, 101730. doi: 10.1016/j.isci.2020.101730 PubMed DOI PMC

Martino A., Meichenin A., Shi J., Pan K., Bowler C. (2007). Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions 1. J. Phycol. 43, 992–1009. doi: 10.1111/j.1529-8817.2007.00384.x DOI

Masoumi A., Heinemann I. U., Rohde M., Koch M., Jahn M., Jahn D. (2008). Complex formation between protoporphyrinogen IX oxidase and ferrochelatase during haem biosynthesis in Thermosynechococcus elongatus. Microbiol. (N Y) 154, 3707–3714. doi: 10.1099/mic.0.2008/018705-0 PubMed DOI

Masuda T., Suzuki T., Shimada H., Ohta H., Takamiya K. (2003). Subcellular localization of two types of ferrochelatase in cucumber. Planta 217, 602–609. doi: 10.1007/s00425-003-1019-2 PubMed DOI

Matsuo E., Inagaki Y. (2018). Patterns in evolutionary origins of heme, chlorophyll a and isopentenyl diphosphate biosynthetic pathways suggest non-photosynthetic periods prior to plastid replacements in dinoflagellates. PeerJ 6, e5345. doi: 10.7717/peerj.5345 PubMed DOI PMC

Matthijs M., Fabris M., Obata T., Foubert I., Franco-Zorrilla J. M., Solano R., et al. . (2017). The transcription factor bZIP14 regulates the TCA cycle in the diatom Phaeodactylum tricornutum. EMBO J. 36, 1559–1576. doi: 10.15252/embj.201696392 PubMed DOI PMC

McCarthy J. K., Smith S. R., McCrow J. P., Tan M., Zheng H., Beeri K., et al. . (2017). Nitrate reductase knockout uncouples nitrate transport from nitrate assimilation and drives repartitioning of carbon flux in a model pennate diatom. Plant Cell 29, 2047–2070. doi: 10.1105/tpc.16.00910 PubMed DOI PMC

Mense S. M., Zhang L. (2006). Heme: a versatile signaling molecule controlling the activities of diverse regulators ranging from transcription factors to MAP kinases. Cell Res. 16, 681–692. doi: 10.1038/sj.cr.7310086 PubMed DOI

Mirdita M., Schütze K., Moriwaki Y., Heo L., Ovchinnikov S., Steinegger M. (2022). ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682. doi: 10.1038/s41592-022-01488-1 PubMed DOI PMC

Moog D., Stork S., Zauner S., Maier U.-G. (2011). In silico and in vivo investigations of proteins of a minimized eukaryotic cytoplasm. Genome Biol. Evol. 3, 375–382. doi: 10.1093/gbe/evr031 PubMed DOI PMC

Nelson D. M., Tréguer P., Brzezinski M. A., Leynaert A., Quéguiner B. (1995). Production and dissolution of biogenic silica in the ocean: Revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochem. Cycles 9, 359–372. doi: 10.1029/95GB01070 DOI

Nielsen H. (2017). Predicting secretory proteins with signalP. Methods Mol. Biol. 1611, 59–73. doi: 10.1007/978-1-4939-7015-5_6 PubMed DOI

Oborník M., Green B. R. (2005). Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol. Biol. Evol. 22, 2343–2353. doi: 10.1093/molbev/msi230 PubMed DOI

Oudot-Le-Secq M.-P., Grimwood J., Shapiro H., Armbrust E. V., Bowler C., Green B. R. (2007). Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol. Genet. Genomics 277, 427–439. doi: 10.1007/s00438-006-0199-4 PubMed DOI

Pazderník M., Mareš J., Pilný J., Sobotka R. (2019). The antenna-like domain of the cyanobacterial ferrochelatase can bind chlorophyll and carotenoids in an energy-dissipative configuration. J. Biol. Chem. 294, 11131–11143. doi: 10.1074/jbc.RA119.008434 PubMed DOI PMC

Piel R. B., Dailey H. A., Medlock A. E. (2019). The mitochondrial heme metabolon: Insights into the complex(ity) of heme synthesis and distribution. Mol. Genet. Metab. 128, 198–203. doi: 10.1016/j.ymgme.2019.01.006 PubMed DOI PMC

Pronobis M. I., Deuitch N., Peifer M. (2016). The miraprep: A protocol that uses a miniprep kit and provides maxiprep yields. PloS One 11, e0160509. doi: 10.1371/journal.pone.0160509 PubMed DOI PMC

Rastogi A., Maheswari U., Dorrell R. G., Vieira F. R. J., Maumus F., Kustka A., et al. . (2018). Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum genome and evolutionary origin of diatoms. Sci. Rep. 8, 4834. doi: 10.1038/s41598-018-23106-x PubMed DOI PMC

Rastogi A., Vieira F. R. J., Deton-Cabanillas A.-F., Veluchamy A., Cantrel C., Wang G., et al. . (2020). A genomics approach reveals the global genetic polymorphism, structure, and functional diversity of ten accessions of the marine model diatom Phaeodactylum tricornutum . ISME J. 14, 347–363. doi: 10.1038/s41396-019-0528-3 PubMed DOI PMC

Richtová J., Sheiner L., Gruber A., Yang S.-M., Kořený L., Striepen B., et al. . (2021). Using diatom and apicomplexan models to study the heme pathway of chromera velia. Int. J. Mol. Sci. 22, 6495. doi: 10.3390/ijms22126495 PubMed DOI PMC

Sakaino M., Ishigaki M., Ohgari Y., Kitajima S., Masaki R., Yamamoto A., et al. . (2009). Dual mitochondrial localization and different roles of the reversible reaction of mammalian ferrochelatase. FEBS J. 276, 5559–5570. doi: 10.1111/j.1742-4658.2009.07248.x PubMed DOI

Sehnal D., Bittrich S., Deshpande M., Svobodová R., Berka K., Bazgier V., et al. . (2021). Mol* Viewer: modern web app for 3D visualization and analysis of large biomolecular structures. Nucleic Acids Res. 49, W431–W437. doi: 10.1093/nar/gkab314 PubMed DOI PMC

Sharaf A., Gruber A., Jiroutová K., Oborník M. (2019). Characterization of aminoacyl-tRNA synthetases in chromerids. Genes (Basel) 10, 582. doi: 10.3390/genes10080582 PubMed DOI PMC

Sobotka R., Tichy M., Wilde A., Hunter C. N. (2011). Functional assignments for the carboxyl-terminal domains of the ferrochelatase from synechocystis PCC 6803: the CAB domain plays a regulatory role, and region II is essential for catalysis. Plant Physiol. 155, 1735–1747. doi: 10.1104/pp.110.167528 PubMed DOI PMC

Takahashi F, Yamagata D, Ishikawa M, Fukamatsu Y, Ogura Y, Kasahara M, et al. . AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc Natl Acad Sci U S A. (2007) 104(49):19625–30. doi: 10.1073/pnas.0707692104 PubMed DOI PMC

Taketani S., Ishigaki M., Mizutani A., Uebayashi M., Numata M., Ohgari Y., et al. . (2007). Heme synthase (Ferrochelatase) catalyzes the removal of iron from heme and demetalation of metalloporphyrins. Biochemistry 46, 15054–15061. doi: 10.1021/bi701460x PubMed DOI

Teufel F., Almagro Armenteros J. J., Johansen A. R., Gíslason M. H., Pihl S. I., Tsirigos K. D., et al. . (2022). SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat. Biotechnol. 40, 1023–1025. doi: 10.1038/s41587-021-01156-3 PubMed DOI PMC

van Lis R., Atteia A., Nogaj L. A., Beale S. I. (2005). Subcellular localization and light-regulated expression of protoporphyrinogen IX oxidase and ferrochelatase in chlamydomonas reinhardtii . Plant Physiol. 139, 1946–1958. doi: 10.1104/pp.105.069732 PubMed DOI PMC

Villar E., Zweig N., Vincens P., Cruz de Carvalho H., Duchene C., Liu S., et al. . (2024). DiatOmicBase, a gene-centered platform to mine functional omics data across diatom genomes. bioRxiv 2024, 9.12.612655. doi: 10.1101/2024.09.12.612655 DOI

Wang L., Patena W., Van Baalen K. A., Xie Y., Singer E. R., Gavrilenko S., et al. . (2023). A chloroplast protein atlas reveals punctate structures and spatial organization of biosynthetic pathways. Cell 186, 3499–3518.e14. doi: 10.1016/j.cell.2023.06.008 PubMed DOI

Watanabe S., Hanaoka M., Ohba Y., Ono T., Ohnuma M., Yoshikawa H., et al. . (2013). Mitochondrial localization of ferrochelatase in a red alga cyanidioschyzon merolae. Plant Cell Physiol. 54, 1289–1295. doi: 10.1093/pcp/pct077 PubMed DOI

Yang M., Lin X., Liu X., Zhang J., Ge F. (2018). Genome annotation of a model diatom phaeodactylum tricornutum using an integrated proteogenomic pipeline. Mol. Plant 11, 1292–1307. doi: 10.1016/j.molp.2018.08.005 PubMed DOI

Zámocký M., Gasselhuber B., Furtmüller P. G., Obinger C. (2014). Turning points in the evolution of peroxidase-catalase superfamily: molecular phylogeny of hybrid heme peroxidases. Cell Mol. Life Sci. 71, 4681–4696. doi: 10.1007/s00018-014-1643-y PubMed DOI PMC