1932

Abstract

While sex is an ancient and highly conserved eukaryotic invention, self-incompatibility systems such as mating types or sexes appear to be derived limitations that show considerable evolutionary plasticity. Within a single class of ciliates, and species have long been known to present a wide variety of mating type numbers and modes of inheritance, but only recently have the genes involved been identified. Although similar transmembrane proteins mediate self/nonself recognition in both ciliates, the mechanisms of mating type determination differ widely, ranging from Mendelian systems to developmental nuclear differentiation, either stochastic or maternally inherited. The non-Mendelian systems rely on programmed editing of the germline genome that occurs during differentiation of the somatic nucleus, and they have co-opted different DNA recombination mechanisms—some previously unknown. Here we review the recent molecular advances and some remaining unsolved questions and discuss the possible implications of these diverse mechanisms for inbreeding/outbreeding balance regulation.

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2017-09-08
2024-11-08
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Literature Cited

  1. Arnaiz O, Mathy N, Baudry C, Malinsky S, Aury JM. 1.  et al. 2012. The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences. PLOS Genet 8:e1002984 [Google Scholar]
  2. Arslanyolu M, Doerder FP. 2.  2000. Genetic and environmental factors affecting mating type frequency in natural isolates of Tetrahymena thermophila. J. Eukaryot. Microbiol. 47:412–18 [Google Scholar]
  3. Aury JM, Jaillon O, Duret L, Noel B, Jubin C. 3.  et al. 2006. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171–78 [Google Scholar]
  4. Betermier M, Duharcourt S. 4.  2014. Programmed rearrangement in ciliates: Paramecium. Microbiol. Spectr. 2:MDNA3–0035-2014 [Google Scholar]
  5. Betermier M, Duharcourt S, Seitz H, Meyer E. 5.  2000. Timing of developmentally programmed excision and circularization of Paramecium internal eliminated sequences. Mol. Cell Biol. 20:1553–61 [Google Scholar]
  6. Bleyman LK, Simon EM. 6.  1968. Clonal analysis of nuclear differentiation in Tetrahymena. Dev. Biol. 18:217–31 [Google Scholar]
  7. Booth L, Wolfe B, Doerder FP. 7.  2015. Molecular polymorphism in the MTA and MTB mating type genes of Tetrahymena thermophila and related asexual species. J. Eukaryot. Microbiol. 62:750–61 [Google Scholar]
  8. Bruns PJ, Palestine RF. 8.  1975. Costimulation in Tetrahymena pyriformis: a developmental interaction between specially prepared cells. Dev. Biol. 42:75–83 [Google Scholar]
  9. Brygoo Y. 9.  1977. Genetic analysis of mating-type differentiation in Paramecium tetraurelia. Genetics 87:633–1286 [Google Scholar]
  10. Brygoo Y, Keller AM. 10.  1981. A mutation with pleiotropic effects on macronuclearly differentiated functions in Paramecium tetraurelia. Dev. Genet. 2:23–34 [Google Scholar]
  11. Brygoo Y, Keller AM. 11.  1981. Genetic analysis of mating type differentiation in Paramecium tetraurelia: III. A mutation restricted to mating type E and affecting the determination of mating type. Dev. Genet. 2:13–22 [Google Scholar]
  12. Brygoo Y, Sonneborn TM, Keller AM, Dippell RV, Schneller MV. 12.  1980. Genetic analysis of mating type differentiation in Paramecium tetraurelia: II. Role of the micronuclei in mating-type determination. Genetics 94:951–59 [Google Scholar]
  13. Butzel HM Jr.. 13.  1955. Mating type mutations in variety 1 of Paramecium aurelia, and their bearing upon the problem of mating type determination. Genetics 40:321 [Google Scholar]
  14. Byrne BC. 14.  1973. Mutational analysis of mating type inheritance in syngen 4 of Paramecium aurelia. Genetics 74:63–80 [Google Scholar]
  15. Cervantes MD, Hamilton EP, Xiong J, Lawson MJ, Yuan D. 15.  et al. 2013. Selecting one of several mating types through gene segment joining and deletion in Tetrahymena thermophila. PLOS Biol 11:e1001518 Correction 2015. PLOS Biol 13:e1002284 [Google Scholar]
  16. Chalker DL, Meyer E, Mochizuki K. 16.  2013. Epigenetics of ciliates. Cold Spring Harb. Perspect. Biol. 5:a017764 [Google Scholar]
  17. Doerder FP. 17.  2014. Abandoning sex: multiple origins of asexuality in the ciliate Tetrahymena. BMC Evol. Biol. 14:112 [Google Scholar]
  18. Doerder FP, Arslanyolu M, Saad Y. 18.  1996. Ecological genetics of Tetrahymena thermophila: mating types, i‐antigens, multiple alleles and epistasis. J. Euk. Microbiol. 43:95–100 [Google Scholar]
  19. Doerder FP, Gates MA, Eberhardt FP, Arslanyolu M. 19.  1995. High frequency of sex and equal frequencies of mating types in natural populations of the ciliate Tetrahymena thermophila. PNAS 92:8715–18 [Google Scholar]
  20. Feng XL SQ, Cao TG, Li LY, Chen YZ. 20.  1988. The S1 strain of Tetrahymena from Shanghai—Tetrahymena shanghaiensis sp. nov. Acta Zool. Sin 34:42–52 [Google Scholar]
  21. Finley MJ, Bruns PJ. 21.  1980. Costimulation in Tetrahymena: II. A nonspecific response to heterotypic cell–cell interactions. Dev. Biol. 79:81–94 [Google Scholar]
  22. Goodenough U, Heitman J. 22.  2014. Origins of eukaryotic sexual reproduction. Cold Spring Harb. Perspect. Biol. 6:a016154 [Google Scholar]
  23. Haggard BW. 23.  1974. Interspecies crosses in Paramecium aurelia (syngen 4 by syngen 8). J. Protozool. 21:152–59 [Google Scholar]
  24. Hiwatashi K. 24.  1968. Determination and inheritance of mating types in Paramecium caudatum. Genetics 58:373–86 [Google Scholar]
  25. Iwano M, Takayama S. 25.  2012. Self/non-self discrimination in angiosperm self-incompatibility. Curr. Opin. Plant Biol. 15:78–83 [Google Scholar]
  26. Lhuillier-Akakpo M, Frapporti A, Denby Wilkes C, Matelot M, Vervoort M. 26.  et al. 2014. Local effect of enhancer of zeste-like reveals cooperation of epigenetic and cis-acting determinants for zygotic genome rearrangements. PLOS Genet 10:e1004665 [Google Scholar]
  27. McGrath CL, Gout JF, Doak TG, Yanagi A, Lynch M. 27.  2014. Insights into three whole-genome duplications gleaned from the Paramecium caudatum genome sequence. Genetics 197:1417–28 [Google Scholar]
  28. Meyer E, Keller AM. 28.  1996. A Mendelian mutation affecting mating-type determination also affects developmental genomic rearrangements in Paramecium tetraurelia. Genetics 143:191–202 [Google Scholar]
  29. Nanney DL. 29.  1957. Mating type inheritance at conjugation in variety 4 of Paramecium aurelia. J. Protozool. 4:89–95 [Google Scholar]
  30. Nanney DL. 30.  1958. Epigenetic factors affecting mating type expression in certain ciliates. Cold Spring Harb. Symp. Quant. Biol. 23:327–35 [Google Scholar]
  31. Nanney DL. 31.  1960. Temperature effects on nuclear differentiation in variety 1 of Tetrahymena pyriformis. Physiol. Zool. 33:146–51 [Google Scholar]
  32. Nanney DL, Allen SL. 32.  1959. Intranuclear co-ordination in Tetrahymena. Physiol. Zool. 32:221–29 [Google Scholar]
  33. Nanney DL, Caughey PA. 33.  1953. Mating type determination of Tetrahymena pyriformis. PNAS 39:1057–63 [Google Scholar]
  34. Orias E. 34.  1963. Mating type determination in variety 8, Tetrahymena pyriformis. Genetics 48:1509–18 [Google Scholar]
  35. Orias E. 35.  1981. Probable somatic DNA rearrangements in mating type determination in Tetrahymena thermophila: a review and a model. Dev. Genet. 2:185–202 [Google Scholar]
  36. Orias E, Baum MP. 36.  1985. Mating type differentiation in Tetrahymena thermophila: characterization of the delayed refeeding effect and its implications concerning intranuclear coordination. Devel. Genet. 5:141–56 [Google Scholar]
  37. Phadke SS, Zufall RA. 37.  2009. Rapid diversification of mating systems in ciliates. Biol. J. Linn. Soc. 98:187–97 [Google Scholar]
  38. Preparata RM, Nanney DL, Simon EM. 38.  1983. The inheritance of acid phosphatase and NADP-malate dehydrogenase isozymes in Tetrahymena pigmentosa. J. Hered. 74:251–59 [Google Scholar]
  39. Ruehle MD, Orias E, Pearson CG. 39.  2016. Tetrahymena as a unicellular model eukaryote: genetic and genomic tools. Genetics 203:649–65 [Google Scholar]
  40. Sandoval PY, Swart EC, Arambasic M, Nowacki M. 40.  2014. Functional diversification of Dicer-like proteins and small RNAs required for genome sculpting. Dev. Cell 28:174–88 [Google Scholar]
  41. Simon EM. 41.  1980. Mating-type inheritance and maturity times in crosses between subspecies of Tetrahymena pigmentosa. Genetics 94:93–113 [Google Scholar]
  42. Simon EM, Orias E. 42.  1987. Genetic instability in the mating type system of Tetrahymena pigmentosa. Genetics 117:437–49 [Google Scholar]
  43. Singh DP, Saudemont B, Guglielmi G, Arnaiz O, Gout JF. 43.  et al. 2014. Genome-defence small RNAs exapted for epigenetic mating-type inheritance. Nature 509:447–52 [Google Scholar]
  44. Sonneborn TM. 44.  1937. Sex, sex inheritance and sex determination in Paramecium aurelia. PNAS 23:378–85 [Google Scholar]
  45. Sonneborn TM. 45.  1954. Patterns of nucleo-cytoplasmic integration in Paramecium. Caryologia 6:Suppl.307–25 [Google Scholar]
  46. Sonneborn TM. 46.  1974. Paramecium aurelia. Handbook of Genetics RC King 469–594 New York: Plenum [Google Scholar]
  47. Sonneborn TM. 47.  1975. The Paramecium aurelia complex of fourteen sibling species. Trans. Am. Microsc. Soc. 94:155–78 [Google Scholar]
  48. Sonneborn TM. 48.  1977. Genetics of cellular differentiation: stable nuclear differentiation in eucaryotic unicells. Annu. Rev. Genet. 11:349–67 [Google Scholar]
  49. Suganuma Y, Shimode C, Yamamoto H. 49.  1984. Conjugation in Tetrahymena: formation of a special junction area for conjugation during the co-stimulation period. J. Electron. Microsc. 33:10–18 [Google Scholar]
  50. Taub SR. 50.  1963. The genetic control of mating type differentiation in Paramecium. Genetics 48:815–34 [Google Scholar]
  51. Tsukii Y, Hiwatashi K. 51.  1983. Genes controlling mating-type specificity in Paramecium caudatum: three loci revealed by intersyngenic crosses. Genetics 104:41–62 [Google Scholar]
  52. Wong L, Klionsky L, Wickert S, Merriam V, Orias E, Hamilton EP. 52.  2000. Autonomously replicating macronuclear DNA pieces are the physical basis of genetic coassortment groups in Tetrahymena thermophila. Genetics 155:1119–25 [Google Scholar]
  53. Xu X, Kumakura M, Kaku E, Takahashi M. 53.  2001. Odd mating-type substances may work as precursor molecules of even mating-type substances in Paramecium caudatum. J. Eukaryot. Microbiol. 48:683–89 [Google Scholar]
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