Jumping Genes and Shrinking Genomes ‐ Probing the Evolution of Eukaryotic Photosynthesis with Genomics

The advent of comparative genomics has revolutionized the study of the origin and evolution of eukaryotes and their organelles. Genomic analysis has revealed that the endosymbiosis that gave rise to plastids ‐ the light‐harvesting apparatus of photosynthetic eukaryotes ‐ had a profound impact on the genetic composition of the host, far beyond the contribution of cyanobacterial genes for plastid‐specific functions. Here I discuss recent advances in our appreciation of the mosaic nature of the eukaryotic nuclear genome, and the ongoing role endosymbiosis plays in shaping its content. IUBMB Life, 57: 539‐547, 2005

[1]  Hervé Moreau,et al.  DNA LIBRARIES FOR SEQUENCING THE GENOME OF OSTREOCOCCUS TAURI (CHLOROPHYTA, PRASINOPHYCEAE): THE SMALLEST FREE‐LIVING EUKARYOTIC CELL 1 , 2002 .

[2]  Jonathan E. Allen,et al.  Genome sequence of the human malaria parasite Plasmodium falciparum , 2002, Nature.

[3]  W. Martin,et al.  The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis , 1997, Current Genetics.

[4]  Charles F. Delwiche,et al.  Tracing the Thread of Plastid Diversity through the Tapestry of Life , 1999, The American Naturalist.

[5]  G. McFadden,et al.  A Phylogenetic Assessment of the Eukaryotic Light-Harvesting Antenna Proteins, with Implications for Plastid Evolution , 1999, Journal of Molecular Evolution.

[6]  P. Keeling,et al.  Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. , 2003, Molecular biology and evolution.

[7]  B F Lang,et al.  Complete Sequence of the Mitochondrial DNA of the Red Alga Porphyra purpurea: Cyanobacterial Introns and Shared Ancestry of Red and Green Algae , 1999, Plant Cell.

[8]  M. Fraunholz,et al.  Evidence for nucleomorph to host nucleus gene transfer: light-harvesting complex proteins from cryptomonads and chlorarachniophytes. , 2000, Protist.

[9]  C. Delwiche,et al.  Dinoflagellate expressed sequence tag data indicate massive transfer of chloroplast genes to the nuclear genome. , 2004, Protist.

[10]  J. Keithly,et al.  Cryptosporidium parvum appears to lack a plastid genome. , 2000, Microbiology.

[11]  R. Crawford,et al.  Observations on the fine structure of the eyespot and associated organelles in the dinoflagellate glenodinium foliaceum. , 1969, Journal of cell science.

[12]  D. Anderson,et al.  Dinoflagellates: a remarkable evolutionary experiment. , 2004, American journal of botany.

[13]  B. Stoebe,et al.  Gene-cluster analysis in chloroplast genomics. , 1999, Trends in genetics : TIG.

[14]  Dario Leister,et al.  NUMTs in sequenced eukaryotic genomes. , 2004, Molecular biology and evolution.

[15]  G. McFadden,et al.  Jam packed genomes – a preliminary, comparative analysis of nucleomorphs , 2002, Genetica.

[16]  L. Medlin,et al.  Ribosomal RNA Analysis Indicates a Benthic Pennate Diatom Ancestry for the Endosymbionts of the Dinoflagellates Peridinium foliaceum and Peridinium balticum (Pyrrhophyta) , 1997, The Journal of eukaryotic microbiology.

[17]  P. Keeling,et al.  Recycled plastids: a 'green movement' in eukaryotic evolution. , 2002, Trends in genetics : TIG.

[18]  Sabine Cornelsen,et al.  Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Nicholas H. Putnam,et al.  The Genome of the Diatom Thalassiosira Pseudonana: Ecology, Evolution, and Metabolism , 2004, Science.

[20]  T. Cavalier-smith.  Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  Tadashi Maruyama,et al.  Phylogeny of nuclear-encoded plastid-targeted GAPDH gene supports separate origins for the peridinin- and the fucoxanthin derivative-containing plastids of dinoflagellates. , 2004, Protist.

[22]  G. McFadden,et al.  Evolution: Red Algal Genome Affirms a Common Origin of All Plastids , 2004, Current Biology.

[23]  N. Patron,et al.  Complex protein targeting to dinoflagellate plastids. , 2005, Journal of molecular biology.

[24]  M. Chihara,et al.  LEPIDODINIUM VIRIDE GEN. ET SP. NOV. (GYMNODINAIALES, DINOPHYTA), A GREEN DINOFLAGELLATE WITH A CHLOROPHYLL A‐ AND B‐CONTAINING ENDOSYMBIONT 1, 2 , 1990 .

[25]  N. Patron,et al.  Gene Replacement of Fructose-1,6-Bisphosphate Aldolase Supports the Hypothesis of a Single Photosynthetic Ancestor of Chromalveolates , 2004, Eukaryotic Cell.

[26]  D. Roos,et al.  Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. , 2001, Molecular biology and evolution.

[27]  Geoffrey I. McFadden,et al.  Plastid in human parasites , 1996, Nature.

[28]  D. Roos,et al.  Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  T. Ohama,et al.  Evolutionary relationship between dinoflagellates bearing obligate diatom endosymbionts: insight into tertiary endosymbiosis. , 2000, International journal of systematic and evolutionary microbiology.

[30]  P. Keeling,et al.  HSP90, Tubulin and Actin are Retained in the Tertiary Endosymbiont Genome of Kryptoperidinium foliaceum , 2004, The Journal of eukaryotic microbiology.

[31]  W. Martin,et al.  Higher-plant chloroplast and cytosolic fructose-1,6-bisphophosphatase isoenzymes: origins via duplication rather than prokaryote-eukaryote divergence , 1996, Plant Molecular Biology.

[32]  Debashish Bhattacharya,et al.  Photosynthetic eukaryotes unite: endosymbiosis connects the dots. , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[33]  Debashish Bhattacharya,et al.  A molecular timeline for the origin of photosynthetic eukaryotes. , 2004, Molecular biology and evolution.

[34]  D. Bhattacharya,et al.  Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. , 2005, Molecular biology and evolution.

[35]  J. Palmer,et al.  The origin of plastids and their spread via secondary symbiosis , 1997 .

[36]  E. Schnepf,et al.  Cryptophycean‐Like Double Membrane‐Bound Chloroplast in the Dinoflagellate, Dinophysis Ehrenb.: Evolutionary, Phylogenetic and Toxicological Implications , 1988 .

[37]  P. Keeling,et al.  SYMBIOTIC ORIGIN OF A NOVEL ACTIN GENE IN THE CRYPTOPHYTE, PYRENOMONAS HELGOLANDII , 2000, Molecular biology and evolution.

[38]  P. Keeling,et al.  Diversity and evolutionary history of plastids and their hosts. , 2004, American journal of botany.

[39]  C. Delwiche,et al.  Phylogenetic analyses indicate that the 19'Hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. , 2000, Molecular biology and evolution.

[40]  B. Green,et al.  Second- and third-hand chloroplasts in dinoflagellates: Phylogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[41]  T. Cavalier-smith,et al.  Single gene circles in dinoflagellate chloroplast genomes , 1999, Nature.

[42]  G. McFadden.  Plastids and Protein Targeting 1 , 1999, The Journal of eukaryotic microbiology.

[43]  D. Leister,et al.  NUPTs in sequenced eukaryotes and their genomic organization in relation to NUMTs. , 2004, Molecular biology and evolution.

[44]  Jessica C Kissinger,et al.  Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum , 2004, Genome Biology.

[45]  W. Martin,et al.  Gene transfer from organelles to the nucleus: Frequent and in big chunks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. Keeling,et al.  Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[47]  W. Martin,et al.  Chloroplast phosphoglycerate kinase from Euglena gracilis: endosymbiotic gene replacement going against the tide. , 2004, European journal of biochemistry.

[48]  W. Martin,et al.  Higher-plant chloroplast and cytosolic 3-phosphoglycerate kinases: a case of endosymbiotic gene replacement , 2004, Plant Molecular Biology.

[49]  A. Grossman.  Paths toward Algal Genomics , 2005, Plant Physiology.

[50]  Chun-Yuan Huang,et al.  Direct measurement of the transfer rate of chloroplast DNA into the nucleus , 2003, Nature.

[51]  Hervé Philippe,et al.  The origin of red algae and the evolution of chloroplasts , 2000, Nature.

[52]  M. Soares,et al.  Migration of the Plastid Genome to the Nucleus in a Peridinin Dinoflagellate , 2004, Current Biology.

[53]  J. Palmer,et al.  THE SYMBIOTIC BIRTH AND SPREAD OF PLASTIDS: HOW MANY TIMES AND WHODUNIT? , 2003 .

[54]  Christopher J. Tonkin,et al.  Tropical infectious diseases: Metabolic maps and functions of the Plasmodium falciparum apicoplast , 2004, Nature Reviews Microbiology.

[55]  Ping Xu,et al.  Complete Genome Sequence of the Apicomplexan, Cryptosporidium parvum , 2004, Science.

[56]  Enrico Schleiff,et al.  Protein import into chloroplasts , 2004, Nature Reviews Molecular Cell Biology.

[57]  Lucie Maranda,et al.  PHYLOGENETIC EVIDENCE FOR THE CRYPTOPHYTE ORIGIN OF THE PLASTID OF DINOPHYSIS (DINOPHYSIALES, DINOPHYCEAE) 1 , 2003 .

[58]  G. McFadden,et al.  Diatom Genomics: Genetic Acquisitions and Mergers , 2004, Current Biology.

[59]  P. Keeling,et al.  Lateral Transfer and Recompartmentalization of Calvin Cycle Enzymes of Plants and Algae , 2004, Journal of Molecular Evolution.

[60]  K. Steidinger,et al.  PERIDINIUM BALTICUM (LEVANDER) LEMMERMANN, AN UNUSUAL DINOFLAGELLATE WITH A MESOCARYOTIC AND AN EUCARYOTIC NUCLEUS 1 2 3 , 1973 .

[61]  Plant genomes: cyanobacterial genes revealed , 2003, Heredity.

[62]  B. Leander,et al.  Did trypanosomatid parasites have photosynthetic ancestors? , 2004, Trends in microbiology.

[63]  T. Cavalier-smith.  Principles of Protein and Lipid Targeting in Secondary Symbiogenesis: Euglenoid, Dinoflagellate, and Sporozoan Plastid Origins and the Eukaryote Family Tree 1 , 2 , 1999, The Journal of eukaryotic microbiology.

[64]  Michael Reith,et al.  The highly reduced genome of an enslaved algal nucleus , 2001, Nature.

[65]  Fumiko Ohta,et al.  Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D , 2004, Nature.

[66]  W. Martin,et al.  Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes , 2004, Nature Reviews Genetics.

[67]  P. Keeling.  A brief history of plastids and their hosts. , 2004, Protist.

[68]  M. Hasegawa,et al.  Gene transfer to the nucleus and the evolution of chloroplasts , 1998, Nature.

[69]  W. Doolittle.  You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. , 1998, Trends in genetics : TIG.

[70]  R. Bock,et al.  High-frequency gene transfer from the chloroplast genome to the nucleus , 2003, Proceedings of the National Academy of Sciences of the United States of America.