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The cryptomonad nucleomorph

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Abstract

The cryptomonad nucleomorph is a vestigial nucleus of a eukaryotic red alga engulfed by a phagotrophic protist and retained as a photosynthetic endosymbiont. This review recounts the initial discovery and subsequent characterisation of the cryptomonad nucleomorph focusing on the key role of Peter Sitte and his protégés in our understanding of secondary endosymbiosis to create complex plastids, one of the major transition events in the evolution of life on Earth.

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References

  • Bagola K, Mehnert M, Jarosch E, Sommer T (2010) Protein dislocation from the ER. Biochim Biophys Acta 1808:925–936

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M, Maruyama S, Arias MC, Ball SG, Gile GH, Hirakawa Y, Hopkins JF, Kuo A, Rensing SA, Schmutz J, Symeonidi A, Elias M, Eveleigh RJ, Herman EK, Klute MJ, Nakayama T, Obornik M, Reyes-Prieto A, Armbrust EV, Aves SJ, Beiko RG, Coutinho P, Dacks JB, Durnford DG, Fast NM, Green BR, Grisdale CJ, Hempel F, Henrissat B, Hoppner MP, Ishida K, Kim E, Koreny L, Kroth PG, Liu Y, Malik SB, Maier UG, McRose D, Mock T, Neilson JA, Onodera NT, Poole AM, Pritham EJ, Richards TA, Rocap G, Roy SW, Sarai C, Schaack S, Shirato S, Slamovits CH, Spencer DF, Suzuki S, Worden AZ, Zauner S, Barry K, Bell C, Bharti AK, Crow JA, Grimwood J, Kramer R, Lindquist E, Lucas S, Salamov A, McFadden GI, Lane CE, Keeling PJ, Gray MW, Grigoriev IV, Archibald JM (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65

    Article  CAS  PubMed  Google Scholar 

  • Douglas S, Zauner S, Fraunholz M, Beaton M, Penny S, Deng L-T, Wu X, Reith ME, Cavalier-Smith T, Maier U-G (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410:1091–1096

    Article  CAS  PubMed  Google Scholar 

  • Douglas SE, Murphy CA, Spencer DF, Gray MW (1991) Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350:148–151

    Article  CAS  PubMed  Google Scholar 

  • Eschbach S, Hofmann C, Maier U-G, Sitte P, Hansmann P (1991a) A eukaryotic genome of 660kb: electrophoretic karyotype of nucleomorph and cell nucleus of the cryptomonad alga, Pyrenomonas salina. Nucl Acids Res 19:1779–1781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eschbach S, Wolters J, Sitte P (1991b) Primary and secondary structure of the nuclear small subunit ribosomal RNA of the cryptomonad Pyrenomonas salina as inferred from the gene sequence: evolutionary implications. J Mol Evol 32:247–252

    Article  CAS  PubMed  Google Scholar 

  • Fellows JD, Cipriano MJ, Agrawal S, Striepen B (2017) A plastid protein that evolved from ubiquitin and is required for apicoplast protein import in Toxoplasma gondii MBio 8

  • Gillot M, Gibbs S (1980) The cryptomonad nucleomorph: its ultrastructure and evolutionary significance. J Phycol 16:558–568

    Article  Google Scholar 

  • Gould SB, Maier UG, Martin WF (2015) Protein import and the origin of red complex plastids. Curr Biol 25:R515–R521

    Article  CAS  PubMed  Google Scholar 

  • Gould SB, Sommer MS, Hadfi K, Zauner S, Kroth PG, Maier UG (2006) Protein targeting into the complex plastid of cryptophytes. J Mol Evol 62:674–681

    Article  CAS  PubMed  Google Scholar 

  • Greenwood A (1974) The Cryptophyta in relation to phylogeny and photosynthesis. In: Sanders J, Goodchild D (eds) 8th international congress of electron microscopy. Australian Academy of Sciences, Canberra, pp 566–567

    Google Scholar 

  • Greenwood A, Griffiths H, Santore U (1977) Chloroplasts and cell compartments in Cryptophyceae. Br Phycol J 12:119

    Google Scholar 

  • Hansmann P (1988) Ultrastructural localization of RNA in cryptomonads. Protoplasma 146:81–88

    Article  Google Scholar 

  • Hansmann P, Eschbach S (1990) Isolation and preliminary characterization of the nucleus and the nucleomorph of a cryptomonad, Pyrenomonas salina. Eur J Cell Biol 52:373–378

    CAS  PubMed  Google Scholar 

  • Hansmann P, Falk H, Scheer U, Sitte P (1987a) Ultrastructural localization of DNA in two Cryptomonas species by use of a new monoclonal DNA antibody. Eur J Cell Biol 42:152–160

    Google Scholar 

  • Hansmann P, Falk H, Sitte P (1985) Zeitschrift fur Naturforschung 40c:933-935

  • Hansmann P, Maerz M, Sitte P (1987b) Investigations on genomes and nucleic acids in cryptomonads. Endocyt C Res 4:289–295

    Google Scholar 

  • Hempel F, Bullmann L, Lau J, Zauner S, Maier UG (2009) ERAD-derived preprotein transport across the second outermost plastid membrane of diatoms. Mol Biol Evol 26:1781–1790

    Article  CAS  PubMed  Google Scholar 

  • Lane CE, Archibald JM (2006) Novel nucleomorph genome architecture in the cryptomonad genus Hemiselmis. J Eukaryot Microbiol 53:515–521

    Article  CAS  PubMed  Google Scholar 

  • Lane CE, van den Heuvel K, Kozera C, Curtis BA, Parsons BJ, Bowman S, Archibald JM (2007) Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function. Proc Natl Acad Sci U S A 104:19908–19913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ludwig M, Gibbs S (1985) DNA is present in the nucleomorph of cryptomonads: further evidence that the chloroplast evolved from a eukaryotic endosymbiont. Protoplasma 127:9–20

    Article  Google Scholar 

  • Maier U-G, Hofmann C, Eschbach S, Wolters J, Igloi G (1991) Demonstration of nucleomorph-encoded eukaryotic small subunit ribosomal RNA in cryptomonads. Mol Gen Genet 230:155–160

    Article  CAS  PubMed  Google Scholar 

  • Maier UG, Zauner S, Hempel F (2015) Protein import into complex plastids: cellular organization of higher complexity. Eur J Cell Biol 94:340–348

    Article  CAS  PubMed  Google Scholar 

  • McFadden GI (1990a) Evidence that cryptomonad chloroplasts evolved from photosynthetic eukaryotic endosymbionts. J Cell Sci 95:303–308

    CAS  Google Scholar 

  • McFadden GI (1990b) Evolution of algal plastids from eukaryotic endosymbionts. In: Harris N, Wilkinson D (eds) In situ hybridization: applications to developmental biology and medicine. Cambridge University Press, Cambridge, pp 143–156

    Chapter  Google Scholar 

  • McFadden GI (1993) Second-hand chloroplasts: evolution of cryptomonad algae. Adv Bot Res 19:189–230

    Article  Google Scholar 

  • McFadden GI, Gilson PR, Douglas SE (1994) The photosynthetic endosymbiont in cryptomonad cells produces both chloroplast and cytoplasmic-type ribosomes. J Cell Sci 107:649–657

    CAS  PubMed  Google Scholar 

  • McFadden GI, Gilson PR, Douglas SE, Hofmann CJB, Maier U-G (1997) Bonsai genomics: sequencing the smallest eukaryotic genomes. Trends Genet 13:46–49

    Article  CAS  PubMed  Google Scholar 

  • McFadden GI, van Dooren GG (2004) Evolution: red algal genome affirms a common origin of all plastids. Curr Biol 14:R514–R516

    Article  CAS  PubMed  Google Scholar 

  • McKerracher L, Gibbs SP (1983) Cell and nucleomorph division in the alga Cryptomonas. Can J Bot 60:2440–2452

    Article  Google Scholar 

  • Mehnert M, Sommer T, Jarosch E (2010) ERAD ubiquitin ligases: multifunctional tools for protein quality control and waste disposal in the endoplasmic reticulum. Bioessays

  • Moore CE, Curtis B, Mills T, Tanifuji G, Archibald JM (2012) Nucleomorph genome sequence of the cryptophyte alga Chroomonas mesostigmatica CCMP1168 reveals lineage-specific gene loss and genome complexity. Genome Biol Evol 4:1162–1175

    Article  PubMed  PubMed Central  Google Scholar 

  • Morrall S, Grenwood AD (1982) Ultastructure of nucleomorph division in species of Cryptophyceae and its evolutionary implications. J Cell Sci 54:311–328

    Google Scholar 

  • Ralph SA, Foth BJ, Hall N, McFadden GI (2004) Evolutionary pressures on apicoplast transit peptides. Mol Biol Evol 21:2183–2194

    Article  CAS  PubMed  Google Scholar 

  • Reith M (1996) The evolution of plastids and photosynthetic apparatus. In: Ort D, Yocum C (eds) Oxygenic photosynthesis: the light reactions. Kluwer Academic Publishers, Netherlands, pp 643–657

    Google Scholar 

  • Santore U (1982) The distribution of the nucleomorph. Cell Biol Int Rep 6:1055–1063

    Article  CAS  PubMed  Google Scholar 

  • Sitte P, Baltes S (1990) Morphometric analyis of two cryptomonads. Quantitative evaluation of fine-structural changes in an endocytobiotic system. Endocytobiology 6:229–233

    Google Scholar 

  • Sommer MS, Gould SB, Lehmann P, Gruber A, Przyborski JM, Maier UG (2007) Der1-mediated preprotein import into the periplastid compartment of chromalveolates? Mol Biol Evol 24:918–928

    Article  CAS  PubMed  Google Scholar 

  • Tanifuji G, Onodera NT, Wheeler TJ, Dlutek M, Donaher N, Archibald JM (2011) Complete nucleomorph genome sequence of the nonphotosynthetic alga Cryptomonas paramecium reveals a core nucleomorph gene set. Genome Biol Evol 3:44–54

    Article  CAS  PubMed  Google Scholar 

  • Zauner S, Fraunholz M, Wastl J, Penny S, Beaton M, Cavalier-Smith T, Maier U-G, Douglas S (2000) Chloropast protein and centrosomal genes, a tRNA intron, and odd telomeres in an unusually compact eukaryotic genome, the cryptomonad nucleomorph. Proc Natl Acad Sci U S A 97:200–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. School of BioSciences, University of Melbourne, Parkville, VIC, 3010, Australia

    Geoffrey I. McFadden

  2. Botany School, University of Melbourne, Parkville, VIC, Australia

    Geoffrey I. McFadden

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  1. Geoffrey I. McFadden
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Correspondence to Geoffrey I. McFadden.

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Handling Editor: Peter Nick

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McFadden, G.I. The cryptomonad nucleomorph. Protoplasma 254, 1903–1907 (2017). https://doi.org/10.1007/s00709-017-1153-5

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  • DOI: https://doi.org/10.1007/s00709-017-1153-5

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