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Selective mirror-image reversal of ciliary patterns inTetrahymena thermophila homozygous for ajanus mutation

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Summary

The development of the oral apparatus (OA) and of neighboring ciliary structures ofTetrahymena thermophila was analyzed in cells homozygous for ajanus (jan A) mutation plus a recessiveenhancer of janA (eja). Such cells frequently possess two OAs located on opposite sides of the cell, a primary (1°) OA previously reported to be normal, and a secondary (2°) OA previously reported to express a mirror-reversal of right-left asymmetry. This study confirms the reality of a reversal in the gross orientation of membranelles in most developing 2° OAs. It also shows that there is a reversal of asymmetry in the pattern of resorption of basal bodies of ciliary rows adjacent to the 2° OA, and in the arrangement of basal-body couplets making up the portion of the apical “crown” of the cell situated close to the 2° OA. However, the locations at which membranelles of the 2° OA become modified during late phases of oral development remain normal, so that membranelles of 2° OAs are superimposable on those of 1° OAs. In addition, the membranelles of 2° OAs frequently undergo a rotation during the final phases of oral development, so that even their spatial orientation becomes normal. This mixture of reversed and normal features can be accounted for by postulating a superimposition of a reversed largescale asymmetry on a normal local asymmetry of ciliary units. This postulate predicts that no single mutation can bring about a complete mirror-image reversal of ciliary patterns.

1° OAs appear normal by light microscopy. However, detailed analysis of SEM, preparations of isolated 1° OAs indicate subtle abnormalities of basal body arrangement in some of these OAs.

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References

  • Allen SL (1967) Genomic exclusion: A rapid means for inducing homozygous diploid lines inTetrahymena pyriformis. Syngen 1 Science 155:575–577

    Google Scholar 

  • Allen SL, Gibson I (1973) In: Elliot AM (ed) The biology ofTetrahymena. Dowden, Hutchinson and Ross, Stroudsburg Pennsylvania, pp 307–373

    Google Scholar 

  • Aufderheide K (1980) Mitochondrial associations with specific microtubular components of the cortex ofTetrahymena thermophila. II Response of mitochondrial pattern to changes in the microtubule pattern. J Cell Sci 42:247–260

    Google Scholar 

  • Aufderheide K (1982) An improvement of the protargol technique of Ng and Nelsen. Trans Am Micros Soc 101:100–104

    Google Scholar 

  • Bakowska J, Frankel J, Nelsen EM (1982a) Regulation of the pattern of basal bodies within the oral apparatus ofTetrahymena thermophila. J Embryol Exp Morphol 69:83–105

    Google Scholar 

  • Bakowska J, Nelsen EM, Frankel J (1982b) Development of the ciliary pattern of the oral apparatus ofTetrahymena thermophila. J Protozool 29:366–382

    Google Scholar 

  • Beisson J, Sonneborn TM (1965) Cytoplasmic inheritance of the organization of the cell cortex ofParamecium. Proc Natl Acad Sci USA 53:275–282

    Google Scholar 

  • Bernard F, Bohatier J (1981) Ultrastructure et mise en place des organelles buccaux au cours de la régénération orale chez Stentor coeruleus (Cilié Hétérotriche). Can J Zool 59:2306–2318

    Google Scholar 

  • Bohatier J (1979) Morphogenèse de régénération chez le ciliéCondylostoma magnum (Spiegel): etude ultrastructurale. J Protozool 26:404–415

    Google Scholar 

  • Bruns PJ, Sanford YM (1978) Mass isolation and fertility testing of temperature sensitive mutants inTetrahymena. Proc Natl Acad Sci USA 75:3355–3358

    Google Scholar 

  • Frankel J (1979) An analysis of cell-surface patterning inTetrahymena In: Subtelny, S, Konigsberg, IR (eds) Determinants of spatial organization. Academic Press, New York, pp 215–246

    Google Scholar 

  • Frankel J (1984) Pattern formation in ciliated protozoa. In: Malacinski GM (ed) Primers in developmental biology, vol I, Pattern formation. MacMillan, New York, 163–196

    Google Scholar 

  • Frankel J, Heckmann K (1968) A simplified Chatton-Lwoff silver impregnation procedure for use in experimental studies with ciliates. Trans Am Micros Soc 87:317–321

    Google Scholar 

  • Frankel J, Jenkins LM (1979) A mutant ofTetrahymena thermophila with a partial mirror-image duplication of cell surface pattern. II Nature of genic control. J Embryol Exp Morphol 49:203–227

    Google Scholar 

  • Frankel J, Nelsen, EM (1981) Discontinuities and overlaps in patterning within single cells. Phil Trans R Soc B 295:525–538

    Google Scholar 

  • Frankel J, Jenkins LM, Bakowska J, Nelsen EM (1984a) Mutational analysis of the patterning of oral structures inTetrahymena I Effects of increased size on organization. J Embryol Exp Morphol 82:41–66

    Google Scholar 

  • Frankel J, Nelsen EM, Bakowska J, Jenkins LM (1984b) Mutational analysis of patterning of oral structures inTetrahymena. II A graded basis for the individuality of intracellular structural arrays. J Embryol Exp Morphol 82:67–95

    Google Scholar 

  • Frankel J, Nelsen EM, Martel E (1981) Development of the ciliature ofTetrahymena thermophila. II Spatial subdivision prior to cytokinesis. Dev Biol 88:39–54

    Google Scholar 

  • Garcia-Bellido A, Santamaria P (1972) Developmental analysis of the wing disc in the mutantengrailed ofDrosophila melanogaster. Genetics 72:87–104

    Google Scholar 

  • Grimes G (1972) Cortical structure in nondividing and cortical morphogenesis in dividingOxytricha fallax. J Protozool 19:428–445

    Google Scholar 

  • Grimes GW (1982) Pattern determination in hypotrich ciliates. Am Zool 22:35–46

    Google Scholar 

  • Grimes GW, L'Hernault S (1979) Cytogeometrical determination of ciliary pattern formation in the hypotrich ciliateStylonychia mytilus. Dev Biol 70:372–395

    Google Scholar 

  • Grimes GW, McKenna ME, Goldsmith-Spoegler CM, Knaupp EA (1980) Patterning and assembly of ciliature are independent processes in hypotrich ciliates. Science 209:281–283

    Google Scholar 

  • Jaeckel-Williams R (1978) Nuclear division with reduced numbers of microtubules inTetrahymena. J Cell Sci 34:303–319

    Google Scholar 

  • James AA, Bryant PJ (1981) Mutations causing pattern deficiencies and duplications in the imaginal wing disc. Dev Biol 85:39–54

    Google Scholar 

  • Jerka-Dziadosz M (1981a) Ultrastructural study on development of the hypotrich ciliateParaurostyla weissei. II Formation of the adoral zone of membranelles and its bearing on problems of ciliate morphogenesis. Protistologica 17:67–81

    Google Scholar 

  • Jerka-Dziadosz M (1981b) Patterning of ciliary structures injanus mutant ofTetrahymena with mirror-image cortical duplications. An ultrastructural study. Acta Protozool 20:337–356

    Google Scholar 

  • Jerka-Dziadosz M (1983) The origin of mirror-symmetry doublet cells in the hypotrichParaurostyla weissei. Wilhelm Roux's Arch 192:179–188

    Google Scholar 

  • Jerka-Dziadosz M, Frankel J (1979) A mutant ofTetrahymena thermophila with a partial mirror image duplication of cell surface pattern. I Analysis of the phenotype. J Embryol Exp Morphol 49:167–202

    Google Scholar 

  • Lansing TJ, Frankel J, Jenkins LM (1985) Oral ultrastructure and oral development of the misaligned undulating membrane mutant ofTetrahymena thermophila. J Protozool [in press]

  • Lynn D (1981) The organization and evolution of microtubular organelles in ciliated protozoa. Biol Rev 56:243–292

    Google Scholar 

  • McCoy JW (1974) New features of the tetrahyminid cortex revealed by protargol staining. Acta Protozool 8:155–159

    Google Scholar 

  • Morata G, Lawrence PA (1977) The development of wingless, a homoeotic mutant ofDrosophila. Dev Biol 56:227–240

    Google Scholar 

  • Nelsen EM (1981) The undulating membrane ofTetrahymena formation and reconstruction. Trans Am Microsc Soc 100:285–295

    Google Scholar 

  • Nelsen EM, DeBault LE (1978) Transformation inTetrahymena pyriformis-description of an inducible phenotype. J Protozool 25:113–119

    Google Scholar 

  • Nelsen EM, Frankel J, Martel E (1981) Development of the ciliature ofTetrahymena thermophila. I Temporal coordination with oral development. Dey Biol 88:27–38

    Google Scholar 

  • Ng SF, Frankel J (1977) 180°-rotation of ciliary rows and its morphogenetic implications inTetrahymena pyriformis. Proc Natl Acad Sci USA 74:1115–1119

    Google Scholar 

  • Ng SF, Nelsen EM (1977) The protargol staining technique: an improved version forTetrahymena pyriformis. Trans Am Micros Soc 96:369–376

    Google Scholar 

  • Ng SF, Williams RJ (1977) An ultrastructural investigation of 180°-rotated ciliary meridians inTetrahymena pyriformis. J Protozool 24:257–263

    Google Scholar 

  • Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity inDrosophila. Nature 287:795–801

    Google Scholar 

  • Tokunaga C (1961) The differentiation of the secondary sexcomb under the influences of the geneengrailed inDrosophila melanogaster. Genetics 46:157–176

    Google Scholar 

  • Williams NE, Bakowska J (1982) Scanning electron microscopy of the cytoskeletal elements in the oral apparatus ofTetrahymena. J Protozool 29:382–389

    Google Scholar 

  • Williams NE, Frankel J (1973) Regulation of microtubules inTetrahymena. I Electron microscopy of oral replacement. J Cell Biol 56:441–457

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of Iowa, 52242, Iowa City, Iowa, USA

    Joseph Frankel, Leslie Meek Jenkins & Julita Bakowska

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  1. Joseph Frankel
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  2. Leslie Meek Jenkins
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  3. Julita Bakowska
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Frankel, J., Jenkins, L.M. & Bakowska, J. Selective mirror-image reversal of ciliary patterns inTetrahymena thermophila homozygous for ajanus mutation. Wilhelm Roux' Archiv 194, 107–120 (1984). https://doi.org/10.1007/BF00848350

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  • DOI: https://doi.org/10.1007/BF00848350

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