1932

Abstract

Over 100 whole-genome sequences from algae are published or soon to be published. The rapidly increasing availability of these fundamental resources is changing how we understand one of the most diverse, complex, and understudied groups of photosynthetic eukaryotes. Genome sequences provide a window into the functional potential of individual algae, with phylogenomics and functional genomics as tools for contextualizing and transferring knowledge from reference organisms into less well-characterized systems. Remarkably, over half of the proteins encoded by algal genomes are of unknown function, highlighting the volume of functional capabilities yet to be discovered. In this review, we provide an overview of publicly available algal genomes, their associated protein inventories, and their quality, with a summary of the statuses of protein function understanding and predictions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-050718-095841
2019-04-29
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/arplant/70/1/annurev-arplant-050718-095841.html?itemId=/content/journals/10.1146/annurev-arplant-050718-095841&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Abdel-Ghany SE, Müller-Moulé P, Niyogi KK, Pilon M, Shikanai T 2005. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–51
    [Google Scholar]
  2. 2.  Abreu IA, Cabelli DE 2010. Superoxide dismutases—a review of the metal-associated mechanistic variations. Biochim. Biophys. Acta Proteins Proteom. 1804:263–74
    [Google Scholar]
  3. 3.  Ajjawi I, Verruto J, Aqui M, Soriaga LB, Coppersmith J et al. 2017. Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator. Nat. Biotechnol. 35:647–52
    [Google Scholar]
  4. 4.  Allen AE, Dupont CL, Obornik M, Horak A, Nunes-Nesi A et al. 2011. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473:203–7
    [Google Scholar]
  5. 5.  Arakaki Y, Kawai-Toyooka H, Hamamura Y, Higashiyama T, Noga A et al. 2013. The simplest integrated multicellular organism unveiled. PLOS ONE 8:e81641
    [Google Scholar]
  6. 6.  Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O et al. 2016. Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci. Rep. 6:39734
    [Google Scholar]
  7. 7.  Aravind L 2000. Guilt by association: contextual information in genome analysis. Genome Res 10:1074–77
    [Google Scholar]
  8. 8.  Arias-Darraz L, Cabezas D, Colenso CK, Alegría-Arcos M, Bravo-Moraga F et al. 2015. A transient receptor potential ion channel in Chlamydomonas shares key features with sensory transduction-associated TRP channels in mammals. Plant Cell 27:177–88
    [Google Scholar]
  9. 9.  Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D et al. 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86
    [Google Scholar]
  10. 10.  Armstrong W 1980. Aeration in higher plants. Advances in Botanical Research 7 HW Woolhouse 225–332 New York: Academic
    [Google Scholar]
  11. 11.  Arriola MB, Velmurugan N, Zhang Y, Plunkett MH, Hondzo H, Barney BM 2018. Genome sequences of Chlorella sorokiniana UTEX 1602 and Micractinium conductrix SAG 241.80: implications to maltose excretion by a green alga. Plant J 93:566–86
    [Google Scholar]
  12. 12.  Ashburner M, Ball CA, Blake JA, Botstein D, Butler H et al. 2000. Gene ontology: tool for the unification of biology. Nat. Genet. 25:25–29
    [Google Scholar]
  13. 13.  Atkinson HJ, Morris JH, Ferrin TE, Babbitt PC 2009. Using sequence similarity networks for visualization of relationships across diverse protein superfamilies. PLOS ONE 4:e4345
    [Google Scholar]
  14. 14.  Atteia A, Adrait A, Brugière S, Tardif M, van Lis R et al. 2009. A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the α-proteobacterial mitochondrial ancestor. Mol. Biol. Evol. 26:1533–48
    [Google Scholar]
  15. 15.  Baldauf SL 2003. The deep roots of eukaryotes. Science 300:1703–6
    [Google Scholar]
  16. 16.  Baldauf SL 2008. An overview of the phylogeny and diversity of eukaryotes. J. Syst. Evol. 46:263–73
    [Google Scholar]
  17. 17.  Barbier G, Oesterhelt C, Larson MD, Halgren RG, Wilkerson C et al. 2005. Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiol 137:460–74
    [Google Scholar]
  18. 18.  Bhattacharya D, Price DC, Chan CX, Qiu H, Rose N et al. 2013. Genome of the red alga Porphyridium purpureum. Nat. Commun. 4:1941
    [Google Scholar]
  19. 19.  Bienvenut WV, Espagne C, Martinez A, Majeran W, Valot B et al. 2011. Dynamics of post‐translational modifications and protein stability in the stroma of Chlamydomonas reinhardtii chloroplasts. Proteomics 11:1734–50
    [Google Scholar]
  20. 20.  Blaby IK, Blaby-Haas CE, Tourasse N, Hom EF, Lopez D et al. 2014. The Chlamydomonas genome project: a decade on. Trends Plant Sci 19:672–80
    [Google Scholar]
  21. 21.  Blaby-Haas CE, de Crécy-Lagard V 2011. Mining high-throughput experimental data to link gene and function. Trends Biotechnol 29:174–82
    [Google Scholar]
  22. 22.  Blaby-Haas CE, Merchant SS 2012. The ins and outs of algal metal transport. Biochim. Biophys. Acta Mol. Cell Res. 1823:1531–52
    [Google Scholar]
  23. 23.  Blaby-Haas CE, Merchant SS 2017. Regulating cellular trace metal economy in algae. Curr. Opin. Plant Biol. 39:88–96
    [Google Scholar]
  24. 24.  Blaby-Haas CE, Padilla-Benavides T, Stübe R, Argüello JM, Merchant SS 2014. Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis. PNAS 111:E5480–87
    [Google Scholar]
  25. 25.  Blanc G, Agarkova I, Grimwood J, Kuo A, Brueggeman A et al. 2012. The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 13:R39
    [Google Scholar]
  26. 26.  Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J et al. 2010. The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22:2943–55
    [Google Scholar]
  27. 27.  Blanc-Mathieu R, Krasovec M, Hebrard M, Yau S, Desgranges E et al. 2017. Population genomics of picophytoplankton unveils novel chromosome hypervariability. Sci. Adv. 3:e1700239
    [Google Scholar]
  28. 28.  Blanc-Mathieu R, Verhelst B, Derelle E, Rombauts S, Bouget FY et al. 2014. An improved genome of the model marine alga Ostreococcus tauri unfolds by assessing Illumina de novo assemblies. BMC Genom 15:1103
    [Google Scholar]
  29. 29.  Bock R 2017. Witnessing genome evolution: experimental reconstruction of endosymbiotic and horizontal gene transfer. Annu. Rev. Genet. 51:1–22
    [Google Scholar]
  30. 30.  Bogen C, Al-Dilaimi A, Albersmeier A, Wichmann J, Grundmann M et al. 2013. Reconstruction of the lipid metabolism for the microalga Monoraphidium neglectum from its genome sequence reveals characteristics suitable for biofuel production. BMC Genom 14:926
    [Google Scholar]
  31. 31.  Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K et al. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–44
    [Google Scholar]
  32. 32.  Brandenburg F, Schoffman H, Kurz S, Krämer U, Keren N et al. 2017. The Synechocystis MANGANESE EXPORTER Mnx is essential for manganese homeostasis in cyanobacteria. Plant Physiol 173:1798–810
    [Google Scholar]
  33. 33.  Brawley SH, Blouin NA, Ficko-Blean E, Wheeler GL, Lohr M et al. 2017. Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). PNAS 114:E6361–70
    [Google Scholar]
  34. 34.  Breker M, Lieberman K, Cross FR 2018. Comprehensive discovery of cell-cycle-essential pathways in Chlamydomonas reinhardtii. Plant Cell 30:1178–98
    [Google Scholar]
  35. 35.  Brock TD 1975. Salinity and the ecology of Dunaliella from Great Salt Lake. Microbiology 89:285–92
    [Google Scholar]
  36. 36.  Burki F 2017. The convoluted evolution of eukaryotes with complex plastids. Advances in Botanical Research 84 Y Hirakawa 1–30 New York: Academic
    [Google Scholar]
  37. 37.  Burki F, Kaplan M, Tikhonenkov DV, Zlatogursky V, Minh BQ et al. 2016. Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc. R. Soc. B 283:20152802
    [Google Scholar]
  38. 38.  Burns JA, Paasch A, Narechania A, Kim E 2015. Comparative genomics of a bacterivorous green alga reveals evolutionary causalities and consequences of phago-mixotrophic mode of nutrition. Genome Biol. Evol. 7:3047–61
    [Google Scholar]
  39. 39.  Capasso C, Supuran CT 2015. An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: Can bacterial carbonic anhydrases shed new light on evolution of bacteria. ? J. Enzym. Inhib. Med. Chem. 30:325–32
    [Google Scholar]
  40. 40.  Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B et al. 2009. AmiGO: online access to ontology and annotation data. Bioinformatics 25:288–89
    [Google Scholar]
  41. 41.  Carrier G, Baroukh C, Rouxel C, Duboscq-Bidot L, Schreiber N, Bougaran G 2018. Draft genomes and phenotypic characterization of Tisochrysis lutea strains. Toward the production of domesticated strains with high added value. Algal Res 29:1–11
    [Google Scholar]
  42. 42.  Casabianca S, Cornetti L, Capellacci S, Vernesi C, Penna A 2017. Genome complexity of harmful microalgae. Harmful Algae 63:7–12
    [Google Scholar]
  43. 43.  Castenholz RW, McDermott TR 2010. The Cyanidiales: ecology, biodiversity, and biogeography. Red Algae in the Genomic Age J Seckbach, DJ Chapman 357–71 Dordrecht: Springer
    [Google Scholar]
  44. 44.  Cavalier-Smith T 1999. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Eukaryot. Microbiol. 46:347–66
    [Google Scholar]
  45. 45.  Cheng S, Melkonian M, Smith SA, Brockington S, Archibald JM et al. 2018. 10KP: a phylodiverse genome sequencing plan. GigaScience 7:giy013
    [Google Scholar]
  46. 46.  Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE et al. 2010. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–21
    [Google Scholar]
  47. 47.  Collén J, Porcel B, Carré W, Ball SG, Chaparro C et al. 2013. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. PNAS 110:5247–52
    [Google Scholar]
  48. 48.  Cormier A, Avia K, Sterck L, Derrien T, Wucher V et al. 2017. Re-annotation, improved large-scale assembly and establishment of a catalogue of noncoding loci for the genome of the model brown alga Ectocarpus. New Phytol 214:219–32
    [Google Scholar]
  49. 49.  Corteggiani Carpinelli E, Telatin A, Vitulo N, Forcato C, D'Angelo M et al. 2014. Chromosome scale genome assembly and transcriptome profiling of Nannochloropsis gaditana in nitrogen depletion. Mol. Plant 7:323–35
    [Google Scholar]
  50. 50.  Courties C, Vaquer A, Troussellier M, Lautier J, Chrétiennot-Dinet MJ et al. 1994. Smallest eukaryotic organism. Nature 370:255
    [Google Scholar]
  51. 51.  Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG 2005. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93
    [Google Scholar]
  52. 52.  Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M et al. 2012. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65
    [Google Scholar]
  53. 53.  Dagan T, Roettger M, Stucken K, Landan G, Koch R et al. 2012. Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol. Evol. 5:31–44
    [Google Scholar]
  54. 54.  De la Rosa MA, Molina-Heredia FP, Hervás M, Navarro JA 2006. Convergent evolution of cytochrome c6 and plastocyanin. Photosystem I: The Light-Driven Plastocyanin: Ferredoxin Oxidoreductase JH Golbeck 683–96 Advances in Photosynthesis and Respiration Ser. 24 Dordrecht, Neth.: Springer
    [Google Scholar]
  55. 55.  Delaye L, Valadez-Cano C, Pérez-Zamorano B 2016. How really ancient is Paulinella chromatophora?. PLOS Curr. Tree Life 8:e68a099364bb1a1e129a17b4e06b0c6b
    [Google Scholar]
  56. 56.  Delmont TO, Eren AM, Vineis JH, Post AF 2015. Genome reconstructions indicate the partitioning of ecological functions inside a phytoplankton bloom in the Amundsen Sea, Antarctica. Front. Microbiol. 6:1090
    [Google Scholar]
  57. 57.  Demaegd D, Colinet A-S, Deschamps A, Morsomme P 2014. Molecular evolution of a novel family of putative calcium transporters. PLOS ONE 9:e100851
    [Google Scholar]
  58. 58.  Deng XD, Gu B, Li YJ, Hu XW, Guo JC, Fei XW 2012. The roles of acyl-CoA: diacylglycerol acyltransferase 2 genes in the biosynthesis of triacylglycerols by the green algae Chlamydomonas reinhardtii. Mol. Plant 5:945–47
    [Google Scholar]
  59. 59.  Dent RM, Haglund CM, Chin BL, Kobayashi MC, Niyogi KK 2005. Functional genomics of eukaryotic photosynthesis using insertional mutagenesis of Chlamydomonas reinhardtii. Plant Physiol 137:545–56
    [Google Scholar]
  60. 60.  Dent RM, Sharifi MN, Malnoë A, Haglund C, Calderon RH et al. 2015. Large‐scale insertional mutagenesis of Chlamydomonas supports phylogenomic functional prediction of photosynthetic genes and analysis of classical acetate‐requiring mutants. Plant J 82:337–51
    [Google Scholar]
  61. 61.  DePriest MS, Bhattacharya D, Lopez-Bautista JM 2013. The plastid genome of the red macroalga Grateloupia taiwanensis (Halymeniaceae). PLOS ONE 8:e68246
    [Google Scholar]
  62. 62.  Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ et al. 2006. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. PNAS 103:11647–52
    [Google Scholar]
  63. 63.  Derelle R, López-García P, Timpano H, Moreira D 2016. A phylogenomic framework to study the diversity and evolution of stramenopiles (=heterokonts). Mol. Biol. Evol. 33:2890–98
    [Google Scholar]
  64. 64.  Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik KV et al. 2008. Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol. Biol. Evol. 25:748–61
    [Google Scholar]
  65. 65.  Doebbe A, Rupprecht J, Beckmann J, Mussgnug JH, Hallmann A et al. 2007. Functional integration of the HUP1 hexose symporter gene into the genome of C. reinhardtii: impacts on biological H2 production. J. Biotechnol. 131:27–33
    [Google Scholar]
  66. 66.  Dorrell RG, Gile G, McCallum G, Meheust R, Bapteste EP et al. 2017. Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. eLife 6:e23717
    [Google Scholar]
  67. 67.  Douzery EJP, Snell EA, Bapteste E, Delsuc F, Philippe H 2004. The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils. ? PNAS 101:15386–91
    [Google Scholar]
  68. 68.  Eisen JA 1998. Phylogenomics: improving functional predictions for uncharacterized genes by evolutionary analysis. Genome Res 8:163–67
    [Google Scholar]
  69. 69.  Eisen JA, Kaiser D, Myers RM 1997. Gastrogenomic delights: a movable feast. Nat. Med. 3:1076–78
    [Google Scholar]
  70. 70.  Eisenhut M, Hoecker N, Schmidt SB, Basgaran RM, Flachbart S et al. 2018. The plastid envelope CHLOROPLAST MANGANESE TRANSPORTER1 is essential for manganese homeostasis in Arabidopsis. Mol. Plant 11:955–69
    [Google Scholar]
  71. 71.  Eitzinger N, Wagner V, Weisheit W, Geimer S, Boness D et al. 2015. Proteomic analysis of a fraction with intact eyespots of Chlamydomonas reinhardtii and assignment of protein methylation. Front. Plant Sci. 6:1085
    [Google Scholar]
  72. 72.  Ekman D, Björklund ÅK, Frey-Skött J, Elofsson A 2005. Multi-domain proteins in the three kingdoms of life: orphan domains and other unassigned regions. J. Mol. Biol. 348:231–43
    [Google Scholar]
  73. 73.  Eme L, Sharpe SC, Brown MW, Roger AJ 2014. On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. Cold Spring Harb. Perspect. Biol. 6:a016139
    [Google Scholar]
  74. 74.  Erdner DL, Price NM, Doucette GJ, Peleato ML, Anderson DM 1999. Characterization of ferredoxin and flavodoxin as markers of iron limitation in marine phytoplankton. Mar. Ecol. Prog. Ser. 184:43–53
    [Google Scholar]
  75. 75.  Ewe D, Tachibana M, Kikutani S, Gruber A, Río Bártulos C et al. 2018. The intracellular distribution of inorganic carbon fixing enzymes does not support the presence of a C4 pathway in the diatom Phaeodactylum tricornutum. Photosynth. Res. 137:263–80
    [Google Scholar]
  76. 76.  Facchinelli F, Colleoni C, Ball SG, Weber APM 2013. Chlamydia, cyanobiont, or host: Who was on top in the ménage à trois. ? Trends Plant Sci 18:673–79
    [Google Scholar]
  77. 77.  Fan JH, Ning K, Zeng XW, Luo YC, Wang DM et al. 2015. Genomic foundation of starch-to-lipid switch in oleaginous Chlorella spp. Plant Physiol 169:2444–61
    [Google Scholar]
  78. 78.  Featherston J, Arakaki Y, Hanschen ER, Ferris PJ, Michod RE et al. 2017. The 4-celled Tetrabaena socialis nuclear genome reveals the essential components for genetic control of cell number at the origin of multicellularity in the volvocine lineage. Mol. Biol. Evol. 35:855–70
    [Google Scholar]
  79. 79.  Feiz L, Williams-Carrier R, Belcher S, Montano M, Barkan A, Stern DB 2014. A protein with an inactive pterin-4a-carbinolamine dehydratase domain is required for Rubisco biogenesis in plants. Plant J 80:862–69
    [Google Scholar]
  80. 80.  Ficko-Blean E, Hervé C, Michel G 2015. Sweet and sour sugars from the sea: the biosynthesis and remodeling of sulfated cell wall polysaccharides from marine macroalgae. Perspect. Phycol. 2:51–64
    [Google Scholar]
  81. 81.  Field CB, Behrenfeld MJ, Randerson JT, Falkowski P 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–40
    [Google Scholar]
  82. 82.  Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J et al. 2015. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–85
    [Google Scholar]
  83. 83.  Fischer K, Weber APM, Kunz H-H 2016. The transporters of plastids—new insights into an old field. Chloroplasts: Current Research and Future Trends H Kirchhoff 209–40 Norfolk, UK: Caister Academic
    [Google Scholar]
  84. 84.  Foflonker F, Price DC, Qiu H, Palenik B, Wang S, Bhattacharya D 2015. Genome of the halotolerant green alga Picochlorum sp. reveals strategies for thriving under fluctuating environmental conditions. Environ. Microbiol. 17:412–26
    [Google Scholar]
  85. 85.  Fu G, Nagasato C, Oka S, Cock JM, Motomura T 2014. Proteomics analysis of heterogeneous flagella in brown algae (stramenopiles). Protist 165:662–75
    [Google Scholar]
  86. 86.  Gabaldón T, Koonin EV 2013. Functional and evolutionary implications of gene orthology. Nat. Rev. Genet. 14:360–66
    [Google Scholar]
  87. 87.  Gagat P, Bodył A, Mackiewicz P, Stiller JW 2014. Tertiary plastid endosymbioses in dinoflagellates. Endosymbiosis W Löffelhardt 233–90 Vienna: Springer
    [Google Scholar]
  88. 88.  Gandini C, Schmidt SB, Husted S, Schneider A, Leister D 2017. The transporter SynPAM71 is located in the plasma membrane and thylakoids, and mediates manganese tolerance in Synechocystis PCC 6803. New Phytol 215:256–68
    [Google Scholar]
  89. 89.  Gao C, Wang Y, Shen Y, Yan D, He X et al. 2014. Oil accumulation mechanisms of the oleaginous microalga Chlorella protothecoides revealed through its genome, transcriptomes, and proteomes. BMC Genom 15:582
    [Google Scholar]
  90. 90.  Gee CW, Niyogi KK 2017. The carbonic anhydrase CAH1 is an essential component of the carbon-concentrating mechanism in Nannochloropsis oceanica. PNAS 114:4537–42
    [Google Scholar]
  91. 91.  Gerlt JA, Bouvier JT, Davidson DB, Imker HJ, Sadkhin B et al. 2015. Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): a web tool for generating protein sequence similarity networks. Biochim. Biophys. Acta Proteins Proteom. 1854:1019–37
    [Google Scholar]
  92. 92.  Gibson TM, Shih PM, Cumming VM, Fischer WW, Crockford PW et al. 2017. Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis. Geology 46:135–38
    [Google Scholar]
  93. 93.  Gimmler H, Weis U 1992. Dunaliella acidophila—life at pH 1.0. Dunaliella: Physiology, Biochemistry, and Biotechnology M Avron, A Ben-Amotz 99–133 Boca Raton, FL: CRC
    [Google Scholar]
  94. 94.  Gobler CJ, Berry DL, Dyhrman ST, Wilhelm SW, Salamov A et al. 2011. Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. PNAS 108:4352–57
    [Google Scholar]
  95. 95.  Gong YM, Guo XJ, Wan X, Liang Z, Jiang M 2011. Characterization of a novel thioesterase (PtTE) from Phaeodactylum tricornutum. J. Basic Microbiol 51:666–72
    [Google Scholar]
  96. 96.  Gonzalez-Esquer CR, Twary SN, Hovde BT, Starkenburg SR 2018. Nuclear, chloroplast, and mitochondrial genome sequences of the prospective microalgal biofuel strain Picochlorum soloecismus. Genome Announc 6:e01498–17
    [Google Scholar]
  97. 97.  Gould SB, Waller RF, McFadden GI 2008. Plastid evolution. Annu. Rev. Plant Biol. 59:491–517
    [Google Scholar]
  98. 98.  Hanikenne M, Baurain D 2013. Origin and evolution of metal P-type ATPases in Plantae (Archaeplastida). Front. Plant Sci. 4:544
    [Google Scholar]
  99. 99.  Hanschen ER, Marriage TN, Ferris PJ, Hamaji T, Toyoda A et al. 2016. The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity. Nat. Commun. 7:11370
    [Google Scholar]
  100. 100.  Hansen BO, Vaid N, Musialak-Lange M, Janowski M, Mutwil M 2014. Elucidating gene function and function evolution through comparison of co-expression networks of plants. Front. Plant Sci. 5:394
    [Google Scholar]
  101. 101.  Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–33
    [Google Scholar]
  102. 102.  Hedges SB, Blair JE, Venturi ML, Shoe JL 2004. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol. Biol. 4:2
    [Google Scholar]
  103. 103.  Helliwell KE, Wheeler GL, Leptos KC, Goldstein RE, Smith AG 2011. Insights into the evolution of vitamin B12 auxotrophy from sequenced algal genomes. Mol. Biol. Evol. 28:2921–33
    [Google Scholar]
  104. 104.  Herron MD, Hackett JD, Aylward FO, Michod RE 2009. Triassic origin and early radiation of multicellular volvocine algae. PNAS 106:3254–58
    [Google Scholar]
  105. 105.  Hippmann AA, Schuback N, Moon K-M, McCrow JP, Allen AE et al. 2017. Contrasting effects of copper limitation on the photosynthetic apparatus in two strains of the open ocean diatom Thalassiosira oceanica. PLOS ONE 12:e0181753
    [Google Scholar]
  106. 106.  Hirooka S, Hirose Y, Kanesaki Y, Higuchi S, Fujiwara T et al. 2017. Acidophilic green algal genome provides insights into adaptation to an acidic environment. PNAS 114:E8304–13
    [Google Scholar]
  107. 107.  Hoham RW, Ling H 2000. Snow algae: the effects of chemical and physical factors on their life cycles and populations. Journey to Diverse Microbial Worlds: Adaptation to Exotic Environments J Seckbach 131–45 Dordrecht, Neth.: Springer
    [Google Scholar]
  108. 108.  Hopkins JF, Spencer DF, Laboissiere S, Neilson JAD, Eveleigh RJM et al. 2012. Proteomics reveals plastid- and periplastid-targeted proteins in the chlorarachniophyte alga Bigelowiella natans. Genome Biol. Evol. 4:1391–406
    [Google Scholar]
  109. 109.  Hopkinson BM, Dupont CL, Allen AE, Morel FMM 2011. Efficiency of the CO2-concentrating mechanism of diatoms. PNAS 108:3830–37
    [Google Scholar]
  110. 110.  Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N et al. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5:3978
    [Google Scholar]
  111. 111.  Hovde BT, Deodato CR, Hunsperger HM, Ryken SA, Yost W et al. 2015. Genome sequence and transcriptome analyses of Chrysochromulina tobin: metabolic tools for enhanced algal fitness in the prominent order Prymnesiales (Haptophyceae). PLOS Genet 11:e1005469
    [Google Scholar]
  112. 112.  Howe CJ, Schlarb-Ridley BG, Wastl J, Purton S, Bendall DS 2006. The novel cytochrome c6 of chloroplasts: a case of evolutionary bricolage. ? J. Exp. Bot. 57:13–22
    [Google Scholar]
  113. 113.  Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ et al. 2017. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol. Biol. Evol. 34:2115–22
    [Google Scholar]
  114. 114.  Ishida K, Green BR 2002. 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. PNAS 99:9294–99
    [Google Scholar]
  115. 115.  Jackson C, Knoll AH, Chan CX, Verbruggen H 2018. Plastid phylogenomics with broad taxon sampling further elucidates the distinct evolutionary origins and timing of secondary green plastids. Sci. Rep. 8:1523
    [Google Scholar]
  116. 116.  Johnson MD 2011. The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynth. Res. 107:117–32
    [Google Scholar]
  117. 117.  Johnston AM 1991. The acquisition of inorganic carbon by marine macroalgae. Can. J. Bot. 69:1123–32
    [Google Scholar]
  118. 118.  Kang MK, Nielsen J 2017. Biobased production of alkanes and alkenes through metabolic engineering of microorganisms. J. Ind. Microbiol. Biotechnol. 44:613–22
    [Google Scholar]
  119. 119.  Karakashian SJ 1963. Growth of Paramecium bursaria as influenced by the presence of algal symbionts. Physiol. Zool. 36:52–68
    [Google Scholar]
  120. 120.  Karkar S, Facchinelli F, Price DC, Weber APM, Bhattacharya D 2015. Metabolic connectivity as a driver of host and endosymbiont integration. PNAS 112:10208–15
    [Google Scholar]
  121. 121.  Karpowicz SJ, Prochnik SE, Grossman AR, Merchant SS 2011. The GreenCut2 resource, a phylogenomically derived inventory of proteins specific to the plant lineage. J. Biol. Chem. 286:21427–39
    [Google Scholar]
  122. 122.  Keeling PJ 2013. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu. Rev. Plant. Biol. 64:583–607
    [Google Scholar]
  123. 123.  Krabberød AK, Orr RJS, Bråte J, Kristensen T, Bjørklund KR, Shalchian-Tabrizi K 2017. Single cell transcriptomics, mega-phylogeny, and the genetic basis of morphological innovations in Rhizaria. Mol. Biol. Evol. 34:1557–73
    [Google Scholar]
  124. 124.  Kropat J, Gallaher SD, Urzica EI, Nakamoto SS, Strenkert D et al. 2015. Copper economy in Chlamydomonas: prioritized allocation and reallocation of copper to respiration versus photosynthesis. PNAS 112:2644–51
    [Google Scholar]
  125. 125.  Ku C, Nelson-Sathi S, Roettger M, Sousa FL, Lockhart PJ et al. 2015. Endosymbiotic origin and differential loss of eukaryotic genes. Nature 524:427–32
    [Google Scholar]
  126. 126.  Kyrpides NC, Ouzounis CA 1999. Whole-genome sequence annotation: ‘Going wrong with confidence.’. Mol. Microbiol. 32:886–87
    [Google Scholar]
  127. 127.  Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM et al. 2004. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117:541–52
    [Google Scholar]
  128. 128.  Lin S, Cheng S, Song B, Zhong X, Lin X et al. 2015. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350:691–94
    [Google Scholar]
  129. 129.  Lojek LJ, Farrand AJ, Wisecaver JH, Blaby-Haas CE, Michel BW et al. 2017. Chlamydomonas reinhardtii LFO1 is an IsdG family heme oxygenase. mSphere 2:e00176–17
    [Google Scholar]
  130. 130.  Lommer M, Specht M, Roy AS, Kraemer L, Andreson R et al. 2012. Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol 13:R66
    [Google Scholar]
  131. 131.  Ma YH, Wang X, Niu YF, Yang ZK, Zhang MH et al. 2014. Antisense knockdown of pyruvate dehydrogenase kinase promotes the neutral lipid accumulation in the diatom Phaeodactylum tricornutum. Microb. Cell Fact. 13:100
    [Google Scholar]
  132. 132.  Marcotte EM, Pellegrini M, Ng HL, Rice DW, Yeates TO, Eisenberg D 1999. Detecting protein function and protein-protein interactions from genome sequences. Science 285:751–53
    [Google Scholar]
  133. 133.  Martin W, Rujan T, Richly E, Hansen A, Cornelsen S et al. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. PNAS 99:12246–51
    [Google Scholar]
  134. 134.  Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M et al. 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–57
    [Google Scholar]
  135. 135.  Méheust R, Bhattacharya D, Pathmanathan JS, McInerney JO, Lopez P, Bapteste E 2018. Formation of chimeric genes with essential functions at the origin of eukaryotes. BMC Biol 16:30
    [Google Scholar]
  136. 136.  Méheust R, Zelzion E, Bhattacharya D, Lopez P, Bapteste E 2016. Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis. PNAS 113:3579–84
    [Google Scholar]
  137. 137.  Meinesz A 1999. Killer Algae transl. D Simberloff Chicago: Univ. Chicago Press
  138. 138.  Merchant SS, Bogorad L 1986. Regulation by copper of the expression of plastocyanin and cytochrome c552 in Chlamydomonas reinhardi. Mol. Cell. Biol. 6:462–69
    [Google Scholar]
  139. 139.  Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–50
    [Google Scholar]
  140. 140.  Mock T, Otillar RP, Strauss J, McMullan M, Paajanen P et al. 2017. Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature 541:536–40
    [Google Scholar]
  141. 141.  Moore CE, Archibald JM 2009. Nucleomorph genomes. Annu. Rev. Genet. 43:251–64
    [Google Scholar]
  142. 142.  Moreau H, Verhelst B, Couloux A, Derelle E, Rombauts S et al. 2012. Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage. Genome Biol 13:R74
    [Google Scholar]
  143. 143.  Morgan RM, Ivanov AG, Priscu JC, Maxwell DP, Huner NPA 1998. Structure and composition of the photochemical apparatus of the Antarctic green alga, Chlamydomonas subcaudata. Photosynth Res. 56:303–14
    [Google Scholar]
  144. 144.  Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P et al. 2018. The timescale of early land plant evolution. PNAS 115:E2274–83
    [Google Scholar]
  145. 145.  Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D 2009. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724–26
    [Google Scholar]
  146. 146.  Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M et al. 2013. The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLOS ONE 8:e57122
    [Google Scholar]
  147. 147.  Naponelli V, Noiriel A, Ziemak MJ, Beverley SM, Lye LF et al. 2008. Phylogenomic and functional analysis of pterin-4a-carbinolamine dehydratase family (COG2154) proteins in plants and microorganisms. Plant Physiol 146:1515–27
    [Google Scholar]
  148. 148.  Nelson DR, Khraiwesh B, Fu W, Alseekh S, Jaiswal A et al. 2017. The genome and phenome of the green alga Chloroidium sp. UTEX 3007 reveal adaptive traits for desert acclimatization. eLife 6:e25783
    [Google Scholar]
  149. 149.  Nguyen HM, Baudet M, Cuiné S, Adriano JM, Barthe D et al. 2011. Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics 11:4266–73
    [Google Scholar]
  150. 150.  Nishitsuji K, Arimoto A, Iwai K, Sudo Y, Hisata K et al. 2016. A draft genome of the brown alga, Cladosiphon okamuranus, S-strain: a platform for future studies of ‘mozuku’ biology. DNA Res 23:561–70
    [Google Scholar]
  151. 151.  Niu YF, Zhang MH, Li DW, Yang WD, Liu JS et al. 2013. Improvement of neutral lipid and polyunsaturated fatty acid biosynthesis by overexpressing a type 2 diacylglycerol acyltransferase in marine diatom Phaeodactylum tricornutum. Mar. Drugs 11:4558–69
    [Google Scholar]
  152. 152.  North WJ 1971. Growth of individual fronds. The Biology of Giant Kelp Beds (Macrocystis) in California WJ North 123–68 Beihefte zur Nova Hedwigia, Heft 32 Lehre, Ger.: J. Cramer
    [Google Scholar]
  153. 153.  Nowack ECM, Melkonian M, Glöckner G 2008. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr. Biol. 18:410–18
    [Google Scholar]
  154. 154.  Nowack ECM, Weber APM 2018. Genomics-informed insights into endosymbiotic organelle evolution in photosynthetic eukaryotes. Annu. Rev. Plant. Biol. 69:51–84
    [Google Scholar]
  155. 155.  Nozaki H, Takano H, Misumi O, Terasawa K, Matsuzaki M et al. 2007. A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5:28
    [Google Scholar]
  156. 156.  Osterman A, Overbeek R 2003. Missing genes in metabolic pathways: a comparative genomics approach. Curr. Opin. Chem. Biol. 7:238–51
    [Google Scholar]
  157. 157.  Palenik B, Grimwood J, Aerts A, Rouzé P, Salamov A et al. 2007. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. PNAS 104:7705–10
    [Google Scholar]
  158. 158.  Parfrey LW, Lahr DJ, Knoll AH, Katz LA 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. PNAS 108:13624–29
    [Google Scholar]
  159. 159.  Parra G, Bradnam K, Korf I 2007. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061–67
    [Google Scholar]
  160. 160.  Pazour GJ, Agrin N, Leszyk J, Witman GB 2005. Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170:103–13
    [Google Scholar]
  161. 161.  Peers G, Price NM 2006. Copper-containing plastocyanin used for electron transport by an oceanic diatom. Nature 441:341–44
    [Google Scholar]
  162. 162.  Pellegrini M, Marcotte E, Thompson M, Eisenberg D, Yeates T 1999. Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. PNAS 96:4285–88
    [Google Scholar]
  163. 163.  Perry JJP, Shin DS, Getzoff ED, Tainer JA 2010. The structural biochemistry of the superoxide dismutases. Biochim. Biophys. ActaProteins Proteom. 1804:245–62
    [Google Scholar]
  164. 164.  Pocock T, Lachance MA, Pröschold T, Priscu JC, Kim SS, Huner N 2004. Identification of a psychrophilic green alga from Lake Bonney Antarctica: Chlamydomonas raudensis Ettl. (UWO 241) Chlorophyceae. J. Phycol. 40:1138–48
    [Google Scholar]
  165. 165.  Polle JEW, Barry K, Cushman J, Schmutz J, Tran D et al. 2017. Draft nuclear genome sequence of the halophilic and beta-carotene-accumulating green alga Dunaliella salina strain CCAP19/18. Genome Announc 5:e01105–17
    [Google Scholar]
  166. 166.  Pombert J-F, Blouin NA, Lane C, Boucias D, Keeling PJ 2014. A lack of parasitic reduction in the obligate parasitic green alga Helicosporidium. PLOS Genet 10:e1004355
    [Google Scholar]
  167. 167.  Poptsova MS, Gogarten JP 2010. Using comparative genome analysis to identify problems in annotated microbial genomes. Microbiology 156:1909–17
    [Google Scholar]
  168. 168.  Price DC, Chan CX, Yoon HS, Yang EC, Qiu H et al. 2012. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335:843–47
    [Google Scholar]
  169. 169.  Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM et al. 2010. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329:223–26
    [Google Scholar]
  170. 170.  Pruitt KD, Tatusova T, Maglott DR 2005. NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33:D501–4
    [Google Scholar]
  171. 171.  Qiu H, Price DC, Weber APM, Facchinelli F, Yoon HS, Bhattacharya D 2013. Assessing the bacterial contribution to the plastid proteome. Trends Plant Sci 18:680–87
    [Google Scholar]
  172. 172.  Qiu H, Price DC, Weber APM, Reeb V, Yang EC et al. 2013. Adaptation through horizontal gene transfer in the cryptoendolithic red alga Galdieria phlegrea. Curr. Biol. 23:R865–66
    [Google Scholar]
  173. 173.  Qiu H, Yoon HS, Bhattacharya D 2016. Red algal phylogenomics provides a robust framework for inferring evolution of key metabolic pathways. PLOS Curr. Tree Life 8:7b037376e6d84a1be34af756a4d90846
    [Google Scholar]
  174. 174.  Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE et al. 2012. Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat. Commun. 3:686
    [Google Scholar]
  175. 175.  Raimunda D, González-Guerrero M, Leeber BW, Argüello JM 2011. The transport mechanism of bacterial Cu+-ATPases: distinct efflux rates adapted to different function. Biometals 24:467–75
    [Google Scholar]
  176. 176.  Rastogi A, Maheswari U, Dorrell RG, Vieira FRJ, Maumus F 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
    [Google Scholar]
  177. 177.  Raven JA, Cockell CS, De La Rocha CL 2008. The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos. Trans. R. Soc. B 363:2641–50
    [Google Scholar]
  178. 178.  Raven JA, Giordano M 2017. Acquisition and metabolism of carbon in the Ochrophyta other than diatoms. Philos. Trans. R. Soc. B 372:20160400
    [Google Scholar]
  179. 179.  Raven JA, Giordano M, Beardall J, Maberly SC 2012. Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Philos. Trans. R. Soc. B 367:493–507
    [Google Scholar]
  180. 180.  Raymond JA, Kim HJ 2012. Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLOS ONE 7:e35968
    [Google Scholar]
  181. 181.  Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC et al. 2013. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–13
    [Google Scholar]
  182. 182. Ref. Genome Group Gene Ontol. Consort. 2009. The Gene Ontology's Reference Genome Project: a unified framework for functional annotation across species. PLOS Comput. Biol. 5:e1000431
    [Google Scholar]
  183. 183.  Reinfelder JR, Kraepiel AM, Morel FM 2000. Unicellular C4 photosynthesis in a marine diatom. Nature 407:996–99
    [Google Scholar]
  184. 184.  Reiskind JB, Bowes G 1991. The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. PNAS 88:2883–87
    [Google Scholar]
  185. 185.  Reyes-Prieto A, Weber APM, Bhattacharya D 2007. The origin and establishment of the plastid in algae and plants. Annu. Rev. Genet. 41:147–68
    [Google Scholar]
  186. 186.  Rhoads A, Au KF 2015. PacBio sequencing and its applications. Genom. Proteom. Bioinform. 13:278–89
    [Google Scholar]
  187. 187.  Roth MS, Cokus SJ, Gallaher SD, Walter A, Lopez D et al. 2017. Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production. PNAS 114:E4296–305
    [Google Scholar]
  188. 188.  Ruprecht C, Vaid N, Proost S, Persson S, Mutwil M 2017. Beyond genomics: studying evolution with gene coexpression networks. Trends Plant Sci 22:298–307
    [Google Scholar]
  189. 189.  Sánchez-Baracaldo P, Raven JA, Pisani D, Knoll AH 2017. Early photosynthetic eukaryotes inhabited low-salinity habitats. PNAS 114:E7737–45
    [Google Scholar]
  190. 190.  Schirmer A, Rude MA, Li X, Popova E, del Cardayre SB 2010. Microbial biosynthesis of alkanes. Science 329:559–62
    [Google Scholar]
  191. 191.  Schneider A, Steinberger I, Herdean A, Gandini C, Eisenhut M et al. 2016. The evolutionarily conserved protein PHOTOSYNTHESIS AFFECTED MUTANT71 is required for efficient manganese uptake at the thylakoid membrane in Arabidopsis. Plant Cell 28:892–910
    [Google Scholar]
  192. 192.  Schnoes AM, Brown SD, Dodevski I, Babbitt PC 2009. Annotation error in public databases: misannotation of molecular function in enzyme superfamilies. PLOS Comput. Biol. 5:e1000605
    [Google Scholar]
  193. 193.  Schönknecht G, Chen W-H, Ternes CM, Barbier GG, Shrestha RP et al. 2013. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–10
    [Google Scholar]
  194. 194.  Schönknecht G, Weber APM, Lercher MJ 2014. Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. BioEssays 36:9–20
    [Google Scholar]
  195. 195.  Sevcikova T, Horak A, Klimes V, Zbrankova V, Demir-Hilton E et al. 2015. Updating algal evolutionary relationships through plastid genome sequencing: Did alveolate plastids emerge through endosymbiosis of an ochrophyte. ? Sci. Rep. 5:10134
    [Google Scholar]
  196. 196.  Sevim V, Bashir A, Chin CS, Miga KH 2016. Alpha-CENTAURI: assessing novel centromeric repeat sequence variation with long read sequencing. Bioinformatics 32:1921–24
    [Google Scholar]
  197. 197.  Shen C, Dupont CL, Hopkinson BM 2017. The diversity of CO2-concentrating mechanisms in marine diatoms as inferred from their genetic content. J. Exp. Bot. 68:3937–48
    [Google Scholar]
  198. 198.  Shikanai T, Müller-Moulé P, Munekage Y, Niyogi KK, Pilon M 2003. PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15:1333–46
    [Google Scholar]
  199. 199.  Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S et al. 2013. Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr. Biol. 23:1399–408
    [Google Scholar]
  200. 200.  Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–12
    [Google Scholar]
  201. 201.  Sonnhammer ELL, Gabaldón T, Sousa da Silva AW, Martin M, Robinson-Rechavi M et al. 2014. Big data and other challenges in the quest for orthologs. Bioinformatics 30:2993–98
    [Google Scholar]
  202. 202.  Sorigué D, Légeret B, Cuiné S, Blangy S, Moulin S et al. 2017. An algal photoenzyme converts fatty acids to hydrocarbons. Science 357:903–7
    [Google Scholar]
  203. 203.  Sorigué D, Légeret B, Cuiné S, Morales P, Mirabella B et al. 2016. Microalgae synthesize hydrocarbons from long-chain fatty acids via a light-dependent pathway. Plant Physiol 171:2393–405
    [Google Scholar]
  204. 204.  Soupene E, Inwood W, Kustu S 2004. Lack of the Rhesus protein Rh1 impairs growth of the green alga Chlamydomonas reinhardtii at high CO2. PNAS 101:7787–92
    [Google Scholar]
  205. 205.  Soupene E, King N, Feild E, Liu P, Niyogi KK et al. 2002. Rhesus expression in a green alga is regulated by CO2. PNAS 99:7769–73
    [Google Scholar]
  206. 206.  Steffensen DA 1976. Morphological variation of Ulva in the Avon‐Heathcote Estuary, Christchurch. N. Z. J. Mar. Freshw. Res. 10:329–41
    [Google Scholar]
  207. 207.  Stiller JW, Schreiber J, Yue J, Guo H, Ding Q, Huang J 2014. The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat. Commun. 5:5764
    [Google Scholar]
  208. 208.  Sultemeyer D, Rinast KA 1996. The CO2 permeability of the plasma membrane of Chlamydomonas reinhardtii: Mass-spectrometric 18O-exchange measurements from 13C18O2 in suspensions of carbonic anhydrase-loaded plasma-membrane vesicles. Planta 200:358–68
    [Google Scholar]
  209. 209.  Suzuki S, Yamaguchi H, Nakajima N, Kawachi M 2018. Raphidocelis subcapitata (=Pseudokirchneriella subcapitata) provides an insight into genome evolution and environmental adaptations in the Sphaeropleales. Sci. Rep. 8:8058
    [Google Scholar]
  210. 210.  Tanaka T, Maeda Y, Veluchamy A, Tanaka M, Abida H et al. 2015. Oil accumulation by the oleaginous diatom Fistulifera solaris as revealed by the genome and transcriptome. Plant Cell 27:162–76
    [Google Scholar]
  211. 211.  Tartar A, Boucias DG, Becnel JJ, Adams BJ 2003. Comparison of plastid 16S rRNA (rrn16) genes from Helicosporidium spp.: evidence supporting the reclassification of Helicosporidia as green algae (Chlorophyta). Int. J. Syst. Evol. Microbiol. 53:1719–23
    [Google Scholar]
  212. 212.  Terashima M, Specht M, Naumann B, Hippler M 2010. Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol. Cell Proteom. 9:1514–32
    [Google Scholar]
  213. 213.  Thomas DN, Dieckmann GS 2002. Antarctic sea ice—a habitat for extremophiles. Science 295:641–44
    [Google Scholar]
  214. 214.  Tian W, Skolnick J 2003. How well is enzyme function conserved as a function of pairwise sequence identity. ? J. Mol. Biol. 333:863–82
    [Google Scholar]
  215. 215.  Tottey S, Rich PR, Rondet SA, Robinson NJ 2001. Two Menkes-type ATPases supply copper for photosynthesis in Synechocystis PCC 6803. J. Biol. Chem. 276:19999–20004
    [Google Scholar]
  216. 216.  Traller JC, Cokus SJ, Lopez DA, Gaidarenko O, Smith SR et al. 2016. Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype. Biotechnol. Biofuels 9:258
    [Google Scholar]
  217. 217.  Treangen TJ, Salzberg SL 2011. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat. Rev. Genet. 13:36–46
    [Google Scholar]
  218. 218.  Trentacoste EM, Shrestha RP, Smith SR, Gle C, Hartmann AC et al. 2013. Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth. PNAS 110:19748–53
    [Google Scholar]
  219. 219.  Treves H, Raanan H, Finkel OM, Berkowicz SM, Keren N et al. 2013. A newly isolated Chlorella sp. from desert sand crusts exhibits a unique resistance to excess light intensity. FEMS Microbiol. Ecol. 86:373–80
    [Google Scholar]
  220. 220.  Tu CK, Acevedo-Duncan M, Wynns GC, Silverman DN 1986. Oyxgen-18 exchange as a measure of accessibility of CO2 and HCO3 to carbonic anhydrase in Chlorella vulgaris (UTEX 263). Plant Physiol 80:997–1001
    [Google Scholar]
  221. 221.  Tulin F, Cross FR 2014. A microbial avenue to cell cycle control in the plant superkingdom. Plant Cell 26:4019–38
    [Google Scholar]
  222. 222.  Tyra HM, Linka M, Weber APM, Bhattacharya D 2007. Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol 8:R212
    [Google Scholar]
  223. 223. UniProt Consort. 2015. UniProt: a hub for protein information. Nucleic Acids Res 43:D204–12
    [Google Scholar]
  224. 224.  Vadeboncoeur Y, Power ME 2017. Attached algae: the cryptic base of inverted trophic pyramids in freshwaters. Annu. Rev. Ecol. Evol. Syst. 48:255–79
    [Google Scholar]
  225. 225.  van Baren MJ, Bachy C, Reistetter EN, Purvine SO, Grimwood J et al. 2016. Evidence-based green algal genomics reveals marine diversity and ancestral characteristics of land plants. BMC Genom 17:267
    [Google Scholar]
  226. 226.  Vieler A, Wu G, Tsai CH, Bullard B, Cornish AJ et al. 2012. Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLOS Genet 8:e1003064
    [Google Scholar]
  227. 227.  Wang Q, Sun H, Huang J 2017. Re-analyses of “algal” genes suggest a complex evolutionary history of oomycetes. Front. Plant Sci. 8:1540
    [Google Scholar]
  228. 228.  Ward BA, Follows MJ 2016. Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. PNAS 113:2958–63
    [Google Scholar]
  229. 229.  Waterhouse RM, Seppey M, Simão FA, Manni M, Ioannidis P et al. 2017. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol. Biol. Evol. 35:543–48
    [Google Scholar]
  230. 230.  Wheatley NM, Sundberg CD, Gidaniyan SD, Cascio D, Yeates TO 2014. Structure and identification of a pterin dehydratase-like protein as a ribulose-bisphosphate carboxylase/oxygenase (RuBisCO) assembly factor in the α-carboxysome. J. Biol. Chem. 289:7973–81
    [Google Scholar]
  231. 231.  Wheeler G, Ishikawa T, Pornsaksit V, Smirnoff N 2015. Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes. eLife 4:e06369
    [Google Scholar]
  232. 232.  Whitney LP, Lins JJ, Hughes MP, Wells ML, Chappell PD, Jenkins BD 2011. Characterization of putative iron responsive genes as species-specific indicators of iron stress in Thalassiosiroid diatoms. Front. Microbiol. 2:234
    [Google Scholar]
  233. 233.  Wierzchos J, DiRuggiero J, Vítek P, Artieda O, Souza-Egipsy V et al. 2015. Adaptation strategies of endolithic chlorophototrophs to survive the hyperarid and extreme solar radiation environment of the Atacama Desert. Front. Microbiol. 6:934
    [Google Scholar]
  234. 234.  Winck FV, Riaño‐Pachón DM, Sommer F, Rupprecht J, Mueller‐Roeber B 2012. The nuclear proteome of the green alga Chlamydomonas reinhardtii. Proteomics 12:95–100
    [Google Scholar]
  235. 235.  Woo YH, Ansari H, Otto TD, Klinger CM, Kolisko M et al. 2015. Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. eLife 4:e06974
    [Google Scholar]
  236. 236.  Worden AZ, Lee JH, Mock T, Rouzé P, Simmons MP et al. 2009. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–72
    [Google Scholar]
  237. 237.  Xue J, Niu YF, Huang T, Yang WD, Liu JS, Li HY 2015. Genetic improvement of the microalga Phaeodactylum tricornutum for boosting neutral lipid accumulation. Metab. Eng. 27:1–9
    [Google Scholar]
  238. 238.  Ye N, Zhang X, Miao M, Fan X, Zheng Y et al. 2015. Saccharina genomes provide novel insight into kelp biology. Nat. Commun. 6:6986
    [Google Scholar]
  239. 239.  Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D 2004. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21:809–18
    [Google Scholar]
  240. 240.  Zaslavskaia LA, Lippmeier JC, Shih C, Ehrhardt D, Grossman AR, Apt KE 2001. Trophic conversion of an obligate photoautotrophic organism through metabolic engineering. Science 292:2073–75
    [Google Scholar]
  241. 241.  Zhan Y, Marchand CH, Maes A, Mauries A, Sun Y et al. 2018. Pyrenoid functions revealed by proteomics in Chlamydomonas reinhardtii. PLOS ONE 13:e0185039
    [Google Scholar]
  242. 242.  Zhang B, Zhang C, Liu C, Jing Y, Wang Y et al. 2018. Inner envelope CHLOROPLAST MANGANESE TRANSPORTER 1 supports manganese homeostasis and phototrophic growth in Arabidopsis. Mol. Plant 11:943–54
    [Google Scholar]
  243. 243.  Zimmer A, Lang D, Richardt S, Frank W, Reski R, Rensing SA 2007. Dating the early evolution of plants: detection and molecular clock analyses of orthologs. Mol. Genet. Genom. 278:393–402
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-050718-095841
Loading
/content/journals/10.1146/annurev-arplant-050718-095841
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error