Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genes
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
PubMed
39696433
PubMed Central
PMC11657870
DOI
10.1186/s12915-024-02089-4
PII: 10.1186/s12915-024-02089-4
Knihovny.cz E-zdroje
- Klíčová slova
- Prototheca, Chlorophyta, Colorless plastids, Plastid genomes,
- MeSH
- fotosyntéza genetika MeSH
- fylogeneze * MeSH
- genom plastidový * MeSH
- molekulární evoluce MeSH
- Prototheca * genetika MeSH
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Plastids are usually involved in photosynthesis, but the secondary loss of this function is a widespread phenomenon in various lineages of algae and plants. In addition to the loss of genes associated with photosynthesis, the plastid genomes of colorless algae are frequently reduced further. To understand the pathways of reductive evolution associated with the loss of photosynthesis, it is necessary to study a number of closely related strains. Prototheca, a chlorophyte genus of facultative pathogens, provides an excellent opportunity to study this process with its well-sampled array of diverse colorless strains. RESULTS: We have sequenced the plastid genomes of 13 Prototheca strains and reconstructed a comprehensive phylogeny that reveals evolutionary patterns within the genus and among its closest relatives. Our phylogenomic analysis revealed three independent losses of photosynthesis among the Prototheca strains and varied protein-coding gene content in their ptDNA. Despite this diversity, all Prototheca strains retain the same key plastid functions. These include processes related to gene expression, as well as crucial roles in fatty acid and cysteine biosynthesis, and membrane transport. CONCLUSIONS: The retention of vestigial genomes in colorless plastids is typically associated with the biosynthesis of secondary metabolites. In contrast, the remarkable conservation of plastid membrane transport system components in the nonphotosynthetic genera Prototheca and Helicosporidium provides an additional constraint against the loss of ptDNA in this lineage. Furthermore, these genes can potentially serve as targets for therapeutic intervention, indicating their importance beyond the evolutionary context.
Zobrazit více v PubMed
Archibald JM. The puzzle of plastid evolution. Curr Biol. 2009;19:R81–8. 10.1016/j.cub.2008.11.067. PubMed
de Vries J, Archibald JM. Endosymbiosis: did plastids evolve from a freshwater cyanobacterium? Curr Biol. 2017;27:R103–5. 10.1016/j.cub.2016.12.006. PubMed
Lim L, McFadden GI. The evolution, metabolism and functions of the apicoplast. Phil Trans R Soc B. 2010;365:749–63. 10.1098/rstb.2009.0273. PubMed PMC
Maciszewski K, Karnkowska A. Should I stay or should I go? Retention and loss of components in vestigial endosymbiotic organelles. Curr Opin Genet Dev. 2019;58–9:33–9. 10.1016/j.gde.2019.07.013. PubMed
Novák Vanclová AMG, Zoltner M, Kelly S, Soukal P, Záhonová K, Füssy Z, Ebenezer TE, Lacová Dobáková E, Eliáš M, Lukeš J, Field MC, Hampl V. Metabolic quirks and the colourful history of the Euglena gracilis secondary plastid. New Phytol. 2020;225:1578–92. 10.1111/nph.16237. PubMed
Hadariová L, Vesteg M, Hampl V, Krajčovič J. Reductive evolution of chloroplasts in non-photosynthetic plants, algae and protists. Curr Genet. 2018;64:365–87. 10.1007/s00294-017-0761-0. PubMed
Gornik SG, Febrimarsa, Cassin AM, MacRae JI, Ramaprasad A, Rchiad Z, McConville MJ, Bacic A, McFadden GI, Pain A, Waller RF. Endosymbiosis undone by stepwise elimination of the plastid in a parasitic dinoflagellate. Proc Natl Acad Sci USA. 2015;112:5767–72. 10.1073/pnas.1423400112. PubMed PMC
Janouškovec J, Gavelis GS, Burki F, Dinh D, Bachvaroff TR, Gornik SG, Bright KJ, Imanian B, Strom SL, Delwiche CF, Waller RF, Fensome RA, Leander BS, Rohwer FL, Saldarriaga JF. Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics. Proc Natl Acad Sci USA. 2017;114:E171–80. 10.1073/pnas.1614842114. PubMed PMC
Allen JF. The CoRR hypothesis for genes in organelles. J Theor Biol. 2017;434:50–7. 10.1016/j.jtbi.2017.04.008. PubMed
Figueroa-Martinez F, Nedelcu AM, Smith DR, Reyes-Prieto A. When the lights go out: the evolutionary fate of free-living colorless green algae. New Phytol. 2014;206:972–82. 10.1111/nph.13279. PubMed PMC
Kayama M, Maciszewski K, Yabuki A, Miyashita H, Karnkowska A, Kamikawa R. Highly reduced plastid genomes of the non-photosynthetic dictyochophyceans Pteridomonas spp. (Ochrophyta, SAR) are retained for tRNA-Glu-based organellar heme biosynthesis. Front Plant Sci. 2020;11:602455. 10.3389/fpls.2020.602455. PubMed PMC
Smith DR. Plastid genomes hit the big time. New Phytol. 2018;219:491–5. 10.1111/nph.15134. PubMed
Smith DR. Lost in the light: Plastid genome evolution in nonphotosynthetic algae. In: Chaw SM, Jansen RK, editors. Advances in Botanical Research. Elsevier Ltd.; 2018. p. 29–53. 10.1016/bs.abr.2017.10.001
Smith DR, Lee RW. A plastid without a genome: evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol. 2014;164:1812–9. 10.1104/pp.113.233718. PubMed PMC
Salomaki ED, Kolísko M. There is treasure everywhere: reductive plastid evolution in Apicomplexa in light of their close relatives. Biomolecules. 2019;9:378. 10.3390/biom9080378. PubMed PMC
Sibbald SJ, Archibald JM. Genomic insights into plastid evolution. Genome Biol Evol. 2020;12:978–90. 10.1093/gbe/evaa096. PubMed PMC
Barrett CF, Sinn BT, Kennedy AH. Unprecedented parallel photosynthetic losses in a heterotrophic orchid genus. Mol Biol Evol. 2019;36:1884–901. 10.1093/molbev/msz111. PubMed PMC
Kim GH, Jeong HJ, Yoo YD, Kim S, Han JH, Han JW, Zuccarello GC. Photosynthetic genes in the heterotrophic dinoflagellate Pfiesteria piscicida (Peridiniales, Alveolata). PLoS ONE. 2013;8:68232. 10.1371/journal.pone.0068232. PubMed PMC
Kamikawa R, Yubuki N, Yoshida M, Taira M, Nakamura N, Ishida KI, Leander BS, Miyashita H, Hashimoto T, Mayama S, Inagaki Y. Multiple losses of photosynthesis in Nitzschia (Bacillariophyceae). Phycological Res. 2015;63:19–28. 10.1111/pre.12072.
Sato S. The apicomplexan plastid and its evolution. Cell Mol Life Sci. 2011;68:1285–96. 10.1007/s00018-011-0646-1. PubMed PMC
de Koning AP, Keeling PJ. Nucleus-encoded genes for plastid-targeted proteins in Helicosporidium: Functional diversity of a cryptic plastid in a parasitic alga. Eukaryot Cell. 2004;3:1198–205. 10.1128/EC.3.5.1198-1205.2004. PubMed PMC
de Koning AP, Keeling PJ. The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured. BMC Biol. 2006;4:12. 10.1186/1741-7007-4-12. PubMed PMC
Sun Y, Pombert JF. Helicosporidia: a genomic snapshot of an early transition to parasitism. Acta Soc Bot Pol. 2014;83:377–85. 10.5586/asbp.2014.039.
Tartar A. The non-photosynthetic algae Helicosporidium spp.: emergence of a novel group of insect pathogens. Insects. 2013;4:375. 10.3390/insects4030375. PubMed PMC
Borza T, Popescu CE, Lee RW. Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii. Eukaryot Cell. 2005;4:253–61. 10.1128/EC.4.2.253-261.2005. PubMed PMC
Guo J, Jian J, Wang L, Xiong L, Lin H, Zhou Z, Sonnenschein EC, Wu W. Genome sequences of two strains of Prototheca wickerhamii provide insight into the protothecosis evolution. Front Cell Infect Microbiol. 2022;12:797017. 10.3389/fcimb.2022.797017. PubMed PMC
Jagielski T, Bakuła Z, Gawor J, Maciszewski K, Kusber WH, Dyląg M, Nowakowska J, Gromadka R, Karnkowska A. The genus Prototheca (Trebouxiophyceae, Chlorophyta) revisited: Implications from molecular taxonomic studies. Algal Res. 2019;43:101639. 10.1016/j.algal.2019.101639.
Jagielski T, Gawor J, Bakuła Z, Decewicz P, Maciszewski K, Karnkowska A. Cytb as a new genetic marker for differentiation of Prototheca species. J Clin Microbiol. 2018;56. 10.1128/JCM.00584-18 PubMed PMC
Bakuła Z, Siedlecki P, Gromadka R, Gawor J, Gromadka A, Pomorski JJ, Panagiotopoulou H, Jagielski T. A first insight into the genome of Prototheca wickerhamii, a major causative agent of human protothecosis. BMC Genomics. 2021;22:168. 10.1186/s12864-021-07491-8. PubMed PMC
Pombert JF, Blouin NA, Lane C, Boucias D, Keeling PJ. A lack of parasitic reduction in the obligate parasitic green alga Helicosporidium. PLoS Genet. 2014;10(5):e1004355. 10.1371/journal.pgen.1004355. PubMed PMC
Yan D, Wang Y, Murakami T, Shen Y, Gong J, Jiang H, Smith DR, Pombert JF, Dai J, Wu Q. Auxenochlorella protothecoides and Prototheca wickerhamii plastid genome sequences give insight into the origins of non-photosynthetic algae. Sci Rep. 2015;5:14465. 10.1038/srep14465. PubMed PMC
Suzuki S, Endoh R, Manabe RI, Ohkuma M, Hirakawa Y. Multiple losses of photosynthesis and convergent reductive genome evolution in the colourless green algae Prototheca. Sci Rep. 2018;8:940. 10.1038/s41598-017-18378-8. PubMed PMC
Figueroa-Martinez F, Nedelcu AM, Smith DR, Reyes-Prieto A. The plastid genome of Polytoma uvella is the largest known among colorless algae and plants and reflects contrasting evolutionary paths to nonphotosynthetic lifestyles. Plant Physiol. 2016;173:932–43. 10.1104/pp.16.01628. PubMed PMC
Pánek T, Barcytė D, Treitli SC, Záhonová K, Sokol M, Ševčíková T, Zadrobílková E, Jaške K, Yubuki N, Čepička I, Eliáš M. A new lineage of non-photosynthetic green algae with extreme organellar genomes. BMC Biol. 2022;20:66. 10.1186/s12915-022-01263-w. PubMed PMC
Molina J, Hazzouri KM, Nickrent D, Geisler M, Meyer RS, Pentony MM, Flowers JM, Pelser P, Barcelona J, Inovejas SA, Uy I, Yuan W, Wilkins O, Michel CI, Locklear S, Concepcion GP, Purugganan MD. Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae). Mol Biol Evol. 2014;31:793–803. 10.1093/molbev/msu051. PubMed PMC
Kamikawa R, Azuma T, Ishii KI, Matsuno Y, Miyashita H. Diversity of organellar genomes in non-photosynthetic diatoms. Protist. 2018;169:351–61. 10.1016/j.protis.2018.04.009. PubMed
Shave CD, Millyard L, May RC. Now for something completely different: Prototheca, pathogenic algae. PLoS Pathog. 2021;17:e1009362. 10.1371/journal.ppat.1009362. PubMed PMC
Sheiner L, Vaidya AB, McFadden GI. The metabolic roles of the endosymbiotic organelles of Toxoplasma and Plasmodium spp. Curr Opin Microbiol. 2013;16:452–8. 10.1016/j.mib.2013.07.003. PubMed PMC
Mukherjee A, Sadhukhan GC. Anti-malarial drug design by targeting apicoplasts: new perspectives. J Pharmacopuncture. 2016;19:7–15. 10.3831/KPI.2016.19.001. PubMed PMC
Dong SS, Wang YL, Xia NH, Liu Y, Liu M, Lian L, Li N, Li LF, Lang XA, Gong YQ, Chen L, Wu E, Zhang SZ. Plastid and nuclear phylogenomic incongruences and biogeographic implications of Magnolia s.l. (Magnoliaceae). J Syst Evol. 2021;60:1–15. 10.1111/jse.12727.
Favre A, Paule J, Ebersbach J. Incongruences between nuclear and plastid phylogenies challenge the identification of correlates of diversification in Gentiana in the European Alpine System. Alp Botany. 2022;132:29–50. 10.1007/s00035-021-00267-6.
Gonçalves DJP, Simpson BB, Ortiz EM, Shimizu GH, Jansen RK. Incongruence between gene trees and species trees and phylogenetic signal variation in plastid genes. Mol Phylogenetic Evol. 2019;138:219–32. 10.1016/j.ympev.2019.05.022. PubMed
Zhang R, Wang YH, Jin JJ, Stull GW, Bruneau A, Cardoso D, Paganucci De Queiroz L, Moore MJ, Zhang SD, Chen SY, Wang J, Li DZ, Yi TS. Exploration of plastid phylogenomic conflict yields new insights into the deep relationships of Leguminosae. Syst Biol. 2020;69:613–22. 10.1093/sysbio/syaa013. PubMed PMC
Jagielski T, Iskra M, Bakuła Z, Rudna J, Roeske K, Nowakowska J, Bielecki J, Krukowski H. Occurrence of Prototheca microalgae in aquatic ecosystems with a description of three new species, Prototheca fontanea, Prototheca lentecrescens, and Prototheca vistulensis. Appl Environ Microbiol. 2022;88:e01092-e1122. 10.1128/aem.01092-22. PubMed PMC
Kunthiphun S, Endoh R, Takashima M, Ohkuma M, Tanasupawat S, Savarajara A. Prototheca paracutis sp. nov., a novel oleaginous achlorophyllous microalga isolated from a mangrove forest. Mycoscience. 2019;60:165–9. 10.1016/j.myc.2019.02.003.
Börner T, Aleynikova AY, Zubo YO, Kusnetsov VV. Chloroplast RNA polymerases: role in chloroplast biogenesis. Biochim Biophys Acta Bioenergetics. 2015;1847:761–9. 10.1016/j.bbabio.2015.02.004. PubMed
Chen J, Yu R, Dai J, Liu Y, Zhou R. The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indica. BMC Plant Biol. 2020;20:199. 10.1186/s12870-020-02415-2. PubMed PMC
Graham SW, Lam VKY, Merckx VSFT. Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes. New Phytol. 2017;214:48–55. 10.1111/nph.14398. PubMed
Mohanta TK, Mishra AK, Khan A, Hashem A, Abd-Allah EF, Al-Harrasi A. Gene loss and evolution of the plastome. Genes. 2020;11:1133. 10.3390/genes11101133. PubMed PMC
Donaher N, Tanifuji G, Onodera NT, Malfatti SA, Chain PSG, Hara Y, Archibald JM. The complete plastid genome sequence of the secondarily nonphotosynthetic alga Cryptomonas paramecium: reduction, compaction, and accelerated evolutionary rate. Genome Biol Evol. 2009;1:439–48. 10.1093/gbe/evp047. PubMed PMC
Kamikawa R, Tanifuji G, Ishikawa SA, Ishii KI, Matsuno Y, Onodera NT, Ishida KI, Hashimoto T, Miyashita H, Mayama S, Inagaki Y. Proposal of a twin arginine translocator system-mediated constraint against loss of ATP synthase genes from nonphotosynthetic plastid genomes. Mol Biol Evol. 2015;32:2598–604. 10.1093/molbev/msv134. PubMed
Logacheva MD, Schelkunov MI, Nuraliev MS, Samigullin TH, Penin AA. The plastid genome of mycoheterotrophic monocot Petrosavia stellaris exhibits both gene losses and multiple rearrangements. Genome Biol Evol. 2014;6:238–46. 10.1093/gbe/evu001. PubMed PMC
de Vries J, Sousa FL, Bölter B, Soll J, Gould SB. YCF1: A Green TIC? Plant Cell. 2015;27:1827–33. 10.1105/tpc.114.135541. PubMed PMC
Smith DR. Can green algal plastid genome size be explained by DNA repair mechanisms? Genome Biol Evol. 2020;12:3797–802. 10.1093/gbe/evaa012. PubMed PMC
Barbrook AC, Santucci N, Plenderleith LJ, Hiller RG, Howe CJ. Comparative analysis of dinoflagellate chloroplast genomes reveals rRNA and tRNA genes. BMC Genomics. 2006;7:297. 10.1186/1471-2164-7-297. PubMed PMC
Severgnini M, Lazzari B, Capra E, Chessa S, Luini M, Bordoni R, Castiglioni B, Ricchi M, Cremonesi P. Genome sequencing of Prototheca zopfii genotypes 1 and 2 provides evidence of a severe reduction in organellar genomes. Sci Rep. 2018;8:14637. 10.1038/s41598-018-32992-0. PubMed PMC
Nakai M. The TIC complex uncovered: The alternative view on the molecular mechanism of protein translocation across the inner envelope membrane of chloroplasts. Biochim Biophys Acta Bioenergetics. 2015;1847:957–67. 10.1016/j.bbabio.2015.02.011. PubMed
Kadirjan-Kalbach D, Yoder DW, Ruckle ME, Larkin RM, Osteryoung KW. FtsHi1/ARC1 is an essential gene in Arabidopsis that links chloroplast biogenesis and division. Plant J. 2012;72:856–67. 10.1111/tpj.12001. PubMed
Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, Andersson B. The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell. 2000;12:419–31. 10.1105/tpc.12.3.419. PubMed PMC
Itoh R, Takano H, Ohta N, Miyagishima S, Kuroiwa H, Kuroiwa T. Two ftsH-family genes encoded in the nuclear and chloroplast genomes of the primitive red alga Cyanidioschyzon merolae. Plant Mol Biol. 1999;41:321–37. 10.1023/A:1006369104530. PubMed
Kikuchi S, Asakura Y, Imai M, Nakahira Y, Kotani Y, Hashiguchi Y, Nakai Y, Takafuji K, Bédard J, Hirabayashi-Ishioka Y, Mori H, Shiina T, Nakai M. A Ycf2-FtsHi heteromeric AAA-ATPase complex is required for chloroplast protein import. Plant Cell. 2018;30:2677–703. 10.1105/tpc.18.00357. PubMed PMC
Liu H, Li A, Rochaix JD, Liu Z. Architecture of chloroplast TOC–TIC translocon supercomplex. Nature. 2023;615:349–57. 10.1038/s41586-023-05744-y. PubMed
Ramundo S, Asakura Y, Salomé PA, Strenkert D, Boone M, Mackinder LCM, Takafuji K, Dinc E, Rahire M, Crèvecoeur M, Magneschi L, Schaad O, Hippler M, Jonikas MC, Merchant S, Nakai M, Rochaix JD, Walter P. Coexpressed subunits of dual genetic origin define a conserved supercomplex mediating essential protein import into chloroplasts. Proc Natl Acad Sci USA. 2020;117:32739–49. 10.1073/pnas.2014294117. PubMed PMC
Jin Z, Wan L, Zhang Y, Li X, Cao Y, Liu H, Fan S, Cao D, Wang Z, Li X, Pan J, Dong MQ, Wu J, Yan Z. Structure of a TOC-TIC supercomplex spanning two chloroplast envelope membranes. Cell. 2020;185:4788–800. 10.1016/j.cell.2022.10.030. PubMed
Baek S, Imamura S, Higa T, Nakai Y, Tanaka K, Nakai M. A distinct class of GTP-binding proteins mediates chloroplast protein import in Rhodophyta. Proc Natl Acad Sci USA. 2022;119:e2208277119. 10.1073/pnas.2208277119. PubMed PMC
Xing J, Pan J, Yi H, Lv K, Gan Q, Wang M, Ge H, Huang X, Huang F, Wang Y, Rochaix JD, Yang W. The plastid-encoded protein Orf2971 is required for protein translocation and chloroplast quality control. Plant Cell. 2022;34:3383–99. 10.1093/plcell/koac180. PubMed PMC
Nadakavukaren MJ, McCracken DA. An ultrastructural survey of the genus Prototheca with special reference to plastids. Mycopathologia. 1977;61:117–9. PubMed
Logacheva MD, Schelkunov MI, Penin AA. Sequencing and analysis of plastid genome in mycoheterotrophic orchid Neottia nidus-avis. Genome Biol Evol. 2011;3:1296–303. 10.1093/gbe/evr102. PubMed PMC
Wickett NJ, Zhang Y, Hansen SK, Roper JM, Kuehl JV, Plock SA, Wolf PG, DePamphilis CW, Boore JL, Goffinet B. Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol. 2008;25:393–401. 10.1093/molbev/msm267. PubMed
Martin W. Gene transfer from organelles to the nucleus: Frequent and in big chunks. Proc Natl Acad Sci USA. 2003;100(15):8612–4. 10.1073/pnas.1633606100. PubMed PMC
Kelly S. The economics of organellar gene loss and endosymbiotic gene transfer. Genome Biol. 2021;22:345. 10.1186/s13059-021-02567-w. PubMed PMC
Howe CJ. Chloroplast genome. In: eLS. Chichester: Wiley; 2016. 10.1002/9780470015902.a0002016.pub3
Wicke S, Müller KF, dePamphilis CW, Quandt D, Wickett NJ, Zhang Y, Renner SS, Schneeweiss GM. Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family. Plant Cell. 2013;25:3711–25. 10.1105/tpc.113.113373. PubMed PMC
Barrett CF, Freudenstein JV, Li J, Mayfield-Jones DR, Perez L, Pires JC, Santos C. Investigating the path of plastid genome degradation in an early-transitional clade of heterotrophic orchids, and implications for heterotrophic angiosperms. Mol Biol Evol. 2014;31:3095–112. 10.1093/molbev/msu252. PubMed
Bellot S, Renner SS. The plastomes of two species in the endoparasite genus Pilostyles (Apodanthaceae) each retain just five or six possibly functional genes. Genome Biol Evol. 2016;8:189–201. 10.1093/gbe/evv251. PubMed PMC
Jagielski T, Gawor J, Bakuła Z, Zuchniewicz K, Żak I, Gromadka R. An optimized method for high quality DNA extraction from microalga Prototheca wickerhamii for genome sequencing. Plant Methods. 2017;13:77. 10.1186/s13007-017-0228-9. PubMed PMC
Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data [Online]. 2010. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ [WWW Document].
Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. 10.1093/bioinformatics/btu170. PubMed PMC
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77. 10.1089/cmb.2012.0021. PubMed PMC
Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: Quality assessment tool for genome assemblies. Bioinformatics. 2013;29:1072–5. 10.1093/bioinformatics/btt086. PubMed PMC
Laetsch DR, Blaxter ML. BlobTools: Interrogation of genome assemblies. F1000Res. 2017;6:1287. 10.12688/f1000research.12232.1.
Karlicki M, Antonowicz S, Karnkowska A. Tiara: deep learning-based classification system for eukaryotic sequences. Bioinformatics. 2022;38:344–50. 10.1093/bioinformatics/btab672. PubMed PMC
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10. 10.1016/S0022-2836(05)80360-2. PubMed
Dierckxsens N, Mardulyn P, Smits G. NOVOPlasty: De novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 2017;45: e18. 10.1093/nar/gkw955. PubMed PMC
Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ, Finn RD, Bateman A. Pfam: The protein families database in 2021. Nucleic Acids Res. 2021;49:D412–9. 10.1093/nar/gkaa913. PubMed PMC
Zimmermann L, Stephens A, Nam SZ, Rau D, Kübler J, Lozajic M, Gabler F, Söding J, Lupas AN, Alva V. A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol. 2018;430:2237–43. 10.1016/j.jmb.2017.12.007. PubMed
Greiner S, Lehwark P, Bock R. OrganellarGenomeDRAW (OGDRAW) version 1.3.1: Expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res. 2019;47:W59-64. 10.1093/nar/gkz238. PubMed PMC
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol. 2013;30:772–80. 10.1093/molbev/mst010. PubMed PMC
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3. 10.1093/bioinformatics/btp348. PubMed PMC
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R, Teeling E. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4. 10.1093/molbev/msaa015. PubMed PMC
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42. 10.1093/sysbio/sys029. PubMed PMC
Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol. 2021;38(10):4647–54. 10.1093/molbev/msab199. PubMed PMC
Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006;34:W609–12. 10.1093/nar/gkl315. PubMed PMC
Xu B, Yang Z. PAMLX: a graphical user interface for PAML. Mol Biol Evol. 2013;30:2723–4. 10.1093/molbev/mst179. PubMed
Maciszewski K, Karnkowska A. Supplementary data for Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genes. 2024. FigShare. 10.6084/m9.figshare.24973665. PubMed PMC