Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 29, 2015, Pages 8827-8834

  Speijer, Dave ^a   Lukeš, Julius ^b,c   Eliáš, Marek ^d  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

^d UNIVERSITY OF OSTRAVA   (Czech Republic)

Author keywords

Eukaryotes; Evolution; Protists; Reactive oxygen species; Sex

Indexed keywords

REACTIVE OXYGEN METABOLITE;

CELL FUSION; CLONAL SPECIES; CLONAL VARIATION; EUKARYOTE; EXTANT SPECIES; MICROBIAL GENOME; MITOCHONDRION; NONHUMAN; NUCLEAR ENERGY; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTIST; REPRODUCTION; REVIEW; SEQUENCE HOMOLOGY; SEXUAL DEVELOPMENT; SPECIES DIVERSITY; DNA SEQUENCE; EUKARYOTIC CELL; GENOME; MEIOSIS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY;

EUKARYOTA; METAZOA; PROKARYOTA; PROTISTA;

CELL FUSION; EUKARYOTIC CELLS; GENOME; MEIOSIS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; REACTIVE OXYGEN SPECIES; REPRODUCTION; SEQUENCE ANALYSIS, DNA;

EID: 84937468655     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501725112     Document Type: Review

References (140)

1. Lynch M (2010) Evolution of the mutation rate. Trends Genet 26(8):345-352.
2. Adl SM, et al. (2012) The revised classification of eukaryotes. JEukaryotMicrobiol59(5):429-493.
3. Chepurnov VA, Mann DG, Sabbe K, Vyverman W (2004) Experimental studies on sexual reproduction in diatoms. Int Rev Cytol 237:91-154.
4. Umen JG (2011) Evolution of sex and mating loci: An expanded view from Volvocine algae. Curr Opin Microbiol 14(6):634-641.
5. Cole E, Sugai T (2012) Developmental progression of Tetrahymena through the cell cycle and conjugation. Methods Cell Biol 109:177-236.
6. Dunthorn M, Katz LA (2010) Secretive ciliates and putative asexuality in microbial eukaryotes. Trends Microbiol 18(5):183-188.
7. Lahr DJ, Parfrey LW, Mitchell EA, Katz LA, Lara E (2011) The chastity of amoebae: Reevaluating evidence for sex in amoeboid organisms. Proc Biol Sci 278(1715):2081-2090.
8. del Campo J, et al. (2014) The others: Our biased perspective of eukaryotic genomes. Trends Ecol Evol 29(5):252-259.
9. Schurko AM, Logsdon JM, Jr (2008) Using a meiosis detection toolkit to investigate ancient asexual "scandals" and the evolution of sex. BioEssays 30(6):579-589.
10. Peacock L, et al. (2011) Identification of the meiotic life cycle stage of Trypanosoma brucei in the tsetse fly. Proc Natl Acad Sci USA 108(9):3671-3676.
11. Peacock L, Bailey M, Carrington M, Gibson W (2014) Meiosis and haploid gametes in the pathogen Trypanosoma brucei. Curr Biol 24(2):181-186.
12. O'Gorman CM, Fuller H, Dyer PS (2009) Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457(7228):471-474.
13. Brakhage AA, Langfelder K (2002) Menacing mold: The molecular biology of Aspergillus fumigatus. Annu Rev Microbiol 56:433-455.
14. Shenoy BD, Jeewon R, Hyde KD (2007) Impact of DNA sequence-data on the taxonomy of anamorphic fungi. Fungal Divers 26(1):1-54.
15. Houdan A, et al. (2004) Holococcolithophore-heterococcolithophore (Haptophyta) life cycles: Flow cytometric analysis of relative ploidy levels. Syst Biodivers 1(4):453-465.
16. Frada M, et al. (2009) First observations of heterococcolithophore-holococcolithophore life cycle combinations in the family Pontosphaeraceae (Calcihaptophycideae, Haptophyta). Mar Micropaleontol 71(1-2):20-27.
17. Evans NM, Holder MT, Barbeitos MS, Okamura B, Cartwright P (2010) The phylogenetic position of Myxozoa: Exploring conflicting signals in phylogenomic and ribosomal data sets. Mol Biol Evol 27(12):2733-2746.
18. Ringuette MJ, Koehler A, Desser SS (2011) Shared antigenicity between the polar filaments of myxosporeans and other Cnidaria. J Parasitol 97(1):163-166.
19. Wolf K, Markiw ME (1984) Biology contravenes taxonomy in the myxozoa: New discoveries show alternation of invertebrate and vertebrate hosts. Science 225(4669):1449-1452.
20. Morris DJ (2012) A new model for myxosporean (Myxozoa) development explains the endogenous budding phenomenon, the nature of cell within cell life stages and evolution of parasitism from a cnidarian ancestor. Int J Parasitol 42(9):829-840.
21. Kim E, Archibald JM (2009) Diversity and evolution of plastids and their genomes. The Chloroplast - Interactions with the Environment, eds Aronsson H, Sandelius AS (Springer, Berlin), pp 1-39.
22. Kugrens P, Lee RE (1988) Ultrastructure of fertilization in a cryptomonad. J Phycol 24(3):385-393.
23. Hill DRA, Wetherbee R (1986) Proteomonas sulcata gen. et sp. nov. (Cryptophyceae), a cryptomonad with two morphologically distinct and alternating forms. Phycologia 25(4):521-543.
24. Hoef-Emden K, Marin B, Melkonian M (2002) Nuclear and nucleomorph SSU rDNA phylogeny in the Cryptophyta and the evolution of cryptophyte diversity. J Mol Evol 55(2):161-179.
25. Hoef-Emden K, Melkonian M (2003) Revision of the genus Cryptomonas (Cryptophyceae): A combination of molecular phylogeny and morphology provides insights into a long-hidden dimorphism. Protist 154(3-4):371-409.
26. Guillou L (2011) Characterization of the Parmales: Much more than the resolution of a taxonomic enigma. J Phycol 47(1):2-4.
27. Guillou L, et al. (1999) Bolidomonas: A new genus with two species belonging to a new algal class, the Bolidophyceae (Heterokonta). J Phycol 35(2):368-381.
28. Ichinomiya M, et al. (2011) Isolation and characterization of Parmales (Heterokonta/ Heterokontophyta/Stramenopiles) from the Oyashio region, Western North Pacific. J Phycol 47(1):144-151.
29. Kessenich CR, Ruck EC, Schurko AM, Wickett NJ, Alverson AJ (2014) Transcriptomic insights into the life history of Bolidophytes, the sister lineage to diatoms. J Phycol 50(6):977-983.
30. Schurko AM, Neiman M, Logsdon JM, Jr (2009) Signs of sex: What we know and how we know it. Trends Ecol Evol 24(4):208-217.
31. Carr M, Leadbeater BS, Hassan R, Nelson M, Baldauf SL (2008) Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proc Natl Acad Sci USA 105(43):16641-16646.
32. King N, et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451(7180):783-788.
33. Carr M, Nelson M, Leadbeater BS, Baldauf SL (2008) Three families of LTR retrotransposons are present in the genome of the choanoflagellate Monosiga brevicollis. Protist 159(4):579-590.
34. Arkhipova I, Meselson M (2005) Deleterious transposable elements and the extinction of asexuals. BioEssays 27(1):76-85.
35. Carr M, Leadbeater BS, Baldauf SL (2010) Conserved meiotic genes point to sex in the choanoflagellates. J Eukaryot Microbiol 57(1):56-62.
36. Levin TC, King N (2013) Evidence for sex and recombination in the choanoflagellate Salpingoeca rosetta. Curr Biol 23(21):2176-2180.
37. Derelle E, et al. (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103(31):11647-11652.
38. Grimsley N, Péquin B, Bachy C, Moreau H, Piganeau G (2010) Cryptic sex in the smallest eukaryotic marine green alga. Mol Biol Evol 27(1):47-54.
39. Blanc-Mathieu R, Sanchez-Ferandin S, Eyre-Walker A, Piganeau G (2013) Organellar inheritance in the green lineage: Insights from Ostreococcus tauri. Genome Biol Evol 5(8):1503-1511.
40. Andersson JO (2012) Double peaks reveal rare diplomonad sex. Trends Parasitol 28(2):46-52.
41. Cooper MA, Adam RD, Worobey M, Sterling CR (2007) Population genetics provides evidence for recombination in Giardia. Curr Biol 17(22):1984-1988.
42. Ramesh MA, Malik SB, Logsdon JM, Jr (2005) A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol 15(2):185-191.
43. Malik SB, Pightling AW, Stefaniak LM, Schurko AM, Logsdon JM, Jr (2008) An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLoS ONE 3(8):e2879.
44. Fritz-Laylin LK, et al. (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140(5):631-642.
45. Fučíková K, Pažoutová M, Rindi F (2015) Meiotic genes and sexual reproduction in the green algal class Trebouxiophyceae (Chlorophyta). J Phycol, 10.1111/jpy.12293.
46. Cuomo CA, et al. (2012) Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res 22(12):2478-2488.
47. Corradi N, Lildhar L (2012) Meiotic genes in the arbuscular mycorrhizal fungi: What for? Commun Integr Biol 5(2):187-189.
48. Tisserant E, et al. (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci USA 110(50):20117-20122.
49. Glöckner G, et al. (2014) The genome of the foraminiferan Reticulomyxa filosa. Curr Biol 24(1):11-18.
50. Suga H, et al. (2013) The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun 4:2325.
51. Chi J, Parrow MW, Dunthorn M (2014) Cryptic sex in Symbiodinium (Alveolata, Dinoflagellata) is supported by an inventory of meiotic genes. J Eukaryot Microbiol 61(3):322-327.
52. Weedall GD, Hall N (2015) Sexual reproduction and genetic exchange in parasitic protists. Parasitology 142(Suppl 1):S120-S127.
53. Wong JL, Johnson MA (2010) Is HAP2-GCS1 an ancestral gamete fusogen? Trends Cell Biol 20(3):134-141.
54. Liu Y, Pei J, Grishin N, Snell WJ (2015) The cytoplasmic domain of the gamete membrane fusion protein HAP2 targets the protein to the fusion site in Chlamydomonas and regulates the fusion reaction. Development 142(5):962-971.
55. Ning J, et al. (2013) Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates. Genes Dev 27(10):1198-1215.
56. Flot JF, et al. (2013) Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500(7463):453-457.
57. Pan K, et al. (2011) Nuclear monoploidy and asexual propagation of Nannochloropsis oceanica (Eustigmatophyceae) as revealed by its genome sequence. J Phycol 47(6):1425-1432.
58. Radakovits R, et al. (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 3:686.
59. Corteggiani Carpinelli E, et al. (2014) Chromosome scale genome assembly and transcriptome profiling of Nannochloropsis gaditana in nitrogen depletion. Mol Plant 7(2):323-335.
60. Paasche E (2001) A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcificationphotosynthesis interactions. Phycologia 40(6):503-529.
61. Frada M, Probert I, Allen MJ, Wilson WH, de Vargas C (2008) The "Cheshire Cat" escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proc Natl Acad Sci USA 105(41):15944-15949.
62. von Dassow P, et al. (2014) Life-cycle modification in open oceans accounts for genome variability in a cosmopolitan phytoplankton. ISME J.
63. Lai DH, Hashimi H, Lun ZR, Ayala FJ, Lukeš J (2008) Adaptations of Trypanosoma brucei to gradual loss of kinetoplast DNA: Trypanosoma equiperdum and Trypanosoma evansi are petite mutants of T. brucei. Proc Natl Acad Sci USA 105(6):1999-2004.
64. Dean S, Gould MK, Dewar CE, Schnaufer AC (2013) Single point mutations in ATP synthase compensate for mitochondrial genome loss in trypanosomes. Proc Natl Acad Sci USA 110(36):14741-14746.
65. Carnes J, et al. (2015) Genome and phylogenetic analyses of trypanosoma evansi reveal extensive similarity to T. brucei and multiple independent origins for dyskinetoplasty. PLoS Negl Trop Dis 9(1):e3404.
66. Judson OP, Normark BB (1996) Ancient asexual scandals. Trends Ecol Evol 11(2):41-46.
67. Normark BB, Judson OP, Moran NA (2003) Genomic signatures of ancient asexual lineages. Biol J Linn Soc Lond 79(1):69-84.
68. Doerder FP (2014) Abandoning sex: Multiple origins of asexuality in the ciliate Tetrahymena. BMC Evol Biol 14:112.
69. Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 106:2-9.
70. van Valen L (1973) A new evolutionary law. Evol Theory 1(1):1-30.
71. Hörandl E (2009) A combinational theory for maintenance of sex. Heredity (Edinb) 103(6):445-457.
72. Birdsell JA, Wills C (2003) The evolutionary origin and maintenance of sexual recombination: A review of contemporary models. Evolutionary Biology, eds Macintyre RJ, Clegg MT (Springer, New York), Vol 33, pp 27-138.
73. Ben-Ami F, Heller J (2005) Spatial and temporal patterns of parthenogenesis and parasitism in the freshwater snail Melanoides tuberculata. J Evol Biol 18(1):138-146.
74. Campbell N (2006) The advantages of sex. Nat Rev Genet 7(4):240.
75. Jokela J, Lively CM, Dybdahl MF, Fox JA (2003) Genetic variation in sexual and clonal lineages of a freshwater snail. Biol J Linn Soc Lond 79(1):165-181.
76. Hörandl E (2009) Geographical parthenogenesis: Opportunities for asexuality. Lost Sex, eds Schön I, Martens K, Van Dijk P (Springer, Heidelberg, Germany), Vol 58, pp 161-186.
77. Lewis WM, Jr (1987) The cost of sex. The Evolution of Sex and its Consequences, ed Stearns SC (Birkhäuser, Basel), pp 33-57.
78. Egel R, Penny D (2008) On the origin of meiosis in eukaryotic evolution: coevolution of meiosis and mitosis from feeble beginnings. Recombination and Meiosis, Genome Dynamics and Stability, eds Egel R, Lankenau D-H (Springer Berlin), Vol 3, pp 249-288.
79. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6(11):836-846.
80. Sterkers Y, et al. (2012) Novel insights into genome plasticity in Eukaryotes: Mosaic aneuploidy in Leishmania. Mol Microbiol 86(1):15-23.
81. Paris Z, Hashimi H, Lun S, Alfonzo JD, Lukeš J (2011) Futile import of tRNAs and proteins into the mitochondrion of Trypanosoma brucei evansi. Mol Biochem Parasitol 176(2):116-120.
82. Lun ZR, Lai DH, Li FJ, Lukeš J, Ayala FJ (2010) Trypanosoma brucei: Two steps to spread out from Africa. Trends Parasitol 26(9):424-427.
83. Nowacki M, et al. (2008) RNA-mediated epigenetic programming of a genomerearrangement pathway. Nature 451(7175):153-158.
84. Nowacki M, Shetty K, Landweber LF (2011) RNA-Mediated epigenetic programming of genome rearrangements. Annu Rev Genomics Hum Genet 12:367-389.
85. Goodenough U, Heitman J (2014) Origins of eukaryotic sexual reproduction. Cold Spring Harb Perspect Biol 6(3):a016154.
86. Gross J, Bhattacharya D (2010) Uniting sex and eukaryote origins in an emerging oxygenic world. Biol Direct 5:53.
87. Naor A, Gophna U (2013) Cell fusion and hybrids in Archaea: Prospects for genome shuffling and accelerated strain development for biotechnology. Bioengineered 4(3):126-129.
88. Nedelcu AM (2005) Sex as a response to oxidative stress: Stress genes co-opted for sex. Proc Biol Sci 272(1575):1935-1940.
89. Nedelcu AM, Michod RE (2003) Sex as a response to oxidative stress: The effect of antioxidants on sexual induction in a facultatively sexual lineage. Proc Biol Sci 270 (Suppl 2):S136-S139.
90. Hörandl E, Hadacek F (2013) The oxidative damage initiation hypothesis for meiosis. Plant Reprod 26(4):351-367.
91. Pennisi E (2014) Microbiology. Modern symbionts inside cells mimic organelle evolution. Science 346(6209):532-533.
92. Knoll AH, Javaux EJ, Hewitt D, Cohen P (2006) Eukaryotic organisms in Proterozoic oceans. Philos Trans R Soc Lond B Biol Sci 361(1470):1023-1038.
93. Holland HD (2006) The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond B Biol Sci 361(1470):903-915.
94. Dyall SD, Brown MT, Johnson PJ (2004) Ancient invasions: From endosymbionts to organelles. Science 304(5668):253-257.
95. Schopf JW (2006) Fossil evidence of Archaean life. Philos Trans R Soc Lond B Biol Sci 361(1470):869-885.
96. Koonin EV (2010) The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol 11(5):209.
97. Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504(7479):231-236.
98. Gray MW (2014) The pre-endosymbiont hypothesis: A new perspective on the origin and evolution of mitochondria. Cold Spring Harb Perspect Biol 6(3):a016097.
99. Szklarczyk R, Huynen MA (2010) Mosaic origin of the mitochondrial proteome. Proteomics 10(22):4012-4024.
100. Martin W, Koonin EV (2006) Introns and the origin of nucleus-cytosol compartmentalization. Nature 440(7080):41-45.
101. Speijer D (2011) Oxygen radicals shaping evolution: why fatty acid catabolism leads to peroxisomes while neurons do without it: FADH?/NADH flux ratios determining mitochondrial radical formation were crucial for the eukaryotic invention of peroxisomes and catabolic tissue differentiation. BioEssays 33(2):88-94.
102. Speijer D (2014) Reconsidering ideas regarding the evolution of peroxisomes: The case for a mitochondrial connection. Cell Mol Life Sci 71(13):2377-2378.
103. Speijer D (2014) How the mitochondrion was shaped by radical differences in substrates: What carnitine shuttles and uncoupling tell us about mitochondrial evolution in response to ROS. BioEssays 36(7):634-643.
104. Bolte K, Rensing SA, Maier UG (2015) The evolution of eukaryotic cells from the perspective of peroxisomes: Phylogenetic analyses of peroxisomal beta-oxidation enzymes support mitochondria-first models of eukaryotic cell evolution. BioEssays 37(2):195-203.
105. Camões F, et al. (2015) New insights into the peroxisomal protein inventory: Acyl- CoA oxidases and -dehydrogenases are an ancient feature of peroxisomes. Biochim Biophys Acta 1853(1):111-125.
106. Speijer D, Manjeri GR, Szklarczyk R (2014) How to deal with oxygen radicals stemming from mitochondrial fatty acid oxidation. Philos Trans R Soc Lond B Biol Sci 369(1646):20130446.
107. Lane N, Martin W (2010) The energetics of genome complexity. Nature 467(7318):929-934.
108. Hörandl E (2013) Meiosis and the paradox of sex in nature. Meiosis, ed Bernstein C (InTech, Rijeka, Croatia), pp 17-39.
109. Bernstein H, Bernstein C (2013) Evolutionary origin and adaptive function of meiosis. Meiosis, ed Bernstein C (InTech, Rijeka, Croatia), pp 41-75.
110. Lane N (2006) Power, Sex, Suicide. Mitochondria and the Meaning of Life (Oxford Univ Press, Oxford).
111. Chouchani ET, et al. (2014) Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature 515(7527):431-435.
112. Burki F (2014) The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb Perspect Biol 6(5):a016147.
113. Simpson AG, Roger AJ (2004) The real 'kingdoms' of eukaryotes. Curr Biol 14(17):R693-R696.
114. Stechmann A, Cavalier-Smith T (2003) The root of the eukaryote tree pinpointed. Curr Biol 13(17):R665-R666.
115. Richards TA, Cavalier-Smith T (2005) Myosin domain evolution and the primary divergence of eukaryotes. Nature 436(7054):1113-1118.
116. Burki F, et al. (2007) Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE 2(8):e790.
117. Burki F, Okamoto N, Pombert JF, Keeling PJ (2012) The evolutionary history of haptophytes and cryptophytes: Phylogenomic evidence for separate origins. Proc Biol Sci 279(1736):2246-2254.
118. Okamoto N, Chantangsi C, Horák A, Leander BS, Keeling PJ (2009) Molecular phylogeny and description of the novel katablepharid Roombia truncata gen. et sp. nov., and establishment of the Hacrobia taxon nov. PLoS ONE 4(9):e7080.
119. Yabuki A, et al. (2014) Palpitomonas bilix represents a basal cryptist lineage: Insight into the character evolution in Cryptista. Sci Rep 4:4641.
120. Seenivasan R, Sausen N, Medlin LK, Melkonian M (2013) Picomonas judraskeda gen. et sp. nov.: The first identified member of the Picozoa phylum nov., a widespread group of picoeukaryotes, formerly known as 'picobiliphytes'. PLoS ONE 8(3):e59565.
121. Yabuki A, Chao EE, Ishida K, Cavalier-Smith T (2012) Microheliella maris (Microhelida ord. n.), an ultrastructurally highly distinctive new axopodial protist species and genus, and the unity of phylum Heliozoa. Protist 163(3):356-388.
122. Kim E, et al. (2011) Newly identified and diverse plastid-bearing branch on the eukaryotic tree of life. Proc Natl Acad Sci USA 108(4):1496-1500.
123. Mackiewicz P, Gagat P (2014) Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus? Acta Soc Bot Pol 83(4):399-407.
124. Pawlowski J (2013) The new micro-kingdoms of eukaryotes. BMC Biol 11:40.
125. Brown MW, et al. (2013) Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc Biol Sci 280(1769):20131755.
126. Yabuki A, Ishida K, Cavalier-Smith T (2013) Rigifila ramosa n. gen., n. sp., a filose apusozoan with a distinctive pellicle, is related to Micronuclearia. Protist 164(1):75-88.
127. Paps J, Medina-Chacón LA, Marshall W, Suga H, Ruiz-Trillo I (2013) Molecular phylogeny of unikonts: New insights into the position of apusomonads and ancyromonads and the internal relationships of opisthokonts. Protist 164(1):2-12.
128. Zhao S, Shalchian-Tabrizi K, Klaveness D (2013) Sulcozoa revealed as a paraphyletic group in mitochondrial phylogenomics. Mol Phylogenet Evol 69(3):462-468.
129. Cavalier-Smith T, et al. (2014) Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa. Mol Phylogenet Evol 81:71-85.
130. Takishita K, Kakizoe N, Yoshida T, Maruyama T (2010) Molecular evidence that phylogenetically diverged ciliates are active in microbial mats of deep-sea cold-seep sediment. J Eukaryot Microbiol 57(1):76-86.
131. Roger AJ, Simpson AG (2009) Evolution: Revisiting the root of the eukaryote tree. Curr Biol 19(4):R165-R167.
132. Rogozin IB, Basu MK, Csürös M, Koonin EV (2009) Analysis of rare genomic changes does not support the unikont-bikont phylogeny and suggests cyanobacterial symbiosis as the point of primary radiation of eukaryotes. Genome Biol Evol 1:99-113.
133. Cavalier-Smith T (2010) Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol Lett 6(3):342-345.
134. Katz LA, Grant JR, Parfrey LW, Burleigh JG (2012) Turning the crown upside down: Gene tree parsimony roots the eukaryotic tree of life. Syst Biol 61(4):653-660.
135. Wideman JG, Gawryluk RM, Gray MW, Dacks JB (2013) The ancient and widespread nature of the ER-mitochondria encounter structure. Mol Biol Evol 30(9):2044-2049.
136. He D, et al. (2014) An alternative root for the eukaryote tree of life. Curr Biol 24(4):465-470.
137. Derelle R, Lang BF (2012) Rooting the eukaryotic tree with mitochondrial and bacterial proteins. Mol Biol Evol 29(4):1277-1289.
138. Derelle R, et al. (2015) Bacterial proteins pinpoint a single eukaryotic root. Proc Natl Acad Sci USA 112(7):E693-E699.
139. Koumandou VL, et al. (2013) Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit Rev Biochem Mol Biol 48(4):373-396.
140. Yubuki N, Leander BS (2013) Evolution of microtubule organizing centers across the tree of eukaryotes. Plant J 75(2):230-244.