We explored how the number of structures is determined in an intracellular organelle series. In Tetrahymena, the oral apparatus contains three diagonal ciliary rows: M1, M2, and M3. During development, the M rows emerge by sequential segmentation of a group of basal bodies, starting with the longest and most anterior M1 and ending with the shortest and most posterior M3. The mpD-1 and mpH-1 alleles increase and decrease the number of M rows, respectively. We identify MpH as a TPR protein and MpD as an importin-9. Both proteins localize to the M rows and form concentration gradients. MpH is a row elongation factor whose loss shortens all M rows and often prevents the formation of M3. MpD limits row initiation after the emergence of M2. MpD could be a part of a negative feedback loop that limits row initiation when M1 assembly is properly advanced. We conclude that the forming oral apparatus has properties of a semi-autonomous intracellular developmental field.
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March 28 2025
Importin-9 and a TPR domain protein MpH drive periodic patterning of ciliary arrays in Tetrahymena
Anushi Suwaneththiya Deraniyagala
,
Anushi Suwaneththiya Deraniyagala
*
(Conceptualization, Investigation, Validation, Visualization, Writing - review & editing)
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
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Wolfgang Maier
,
Wolfgang Maier
*
(Data curation, Formal analysis, Writing - review & editing)
2
Bioinformatics, University of Freiburg
, Freiburg, Germany
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Mireya Parra
,
Mireya Parra
(Investigation, Validation, Visualization)
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
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Elise Nanista
,
Elise Nanista
(Investigation, Writing - review & editing)
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
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Deborah Oluwabukola Sowunmi
,
Deborah Oluwabukola Sowunmi
(Investigation, Visualization)
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
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Michael Hassan
,
Michael Hassan
(Investigation)
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
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Nathan Chasen
,
Nathan Chasen
(Formal analysis, Visualization, Writing - review & editing)
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
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Sunita Sharma
,
Sunita Sharma
(Investigation)
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
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Karl F. Lechtreck
,
Karl F. Lechtreck
(Funding acquisition, Investigation, Supervision)
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
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Eric S. Cole
,
Eric S. Cole
(Investigation, Visualization, Writing - review & editing)
3Biology Department,
St. Olaf College
, Northfield, MN, USA
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Natalia Bernardes
,
Natalia Bernardes
(Formal analysis, Visualization)
4Departments of Pharmacology and Biophysics,
University of Texas Southwestern Medical Center
, Dallas, TX, USA
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Yuh Min Chook
,
Yuh Min Chook
(Formal analysis, Supervision, Visualization, Writing - review & editing)
4Departments of Pharmacology and Biophysics,
University of Texas Southwestern Medical Center
, Dallas, TX, USA
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Jacek Gaertig
(Conceptualization, Funding acquisition, Investigation, Project administration, Supervision, Writing - original draft, Writing - review & editing)
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
Correspondence to Jacek Gaertig: [email protected]
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Anushi Suwaneththiya Deraniyagala
Conceptualization, Investigation, Validation, Visualization, Writing - review & editing
*
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
Wolfgang Maier
Data curation, Formal analysis, Writing - review & editing
*
2
Bioinformatics, University of Freiburg
, Freiburg, Germany
Mireya Parra
Investigation, Validation, Visualization
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
Elise Nanista
Investigation, Writing - review & editing
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
Deborah Oluwabukola Sowunmi
Investigation, Visualization
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
Michael Hassan
Investigation
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
Nathan Chasen
Formal analysis, Visualization, Writing - review & editing
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
Sunita Sharma
Investigation
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
Karl F. Lechtreck
Funding acquisition, Investigation, Supervision
1Department of Cellular Biology,
University of Georgia
, Athens, GA, USA
Eric S. Cole
Investigation, Visualization, Writing - review & editing
3Biology Department,
St. Olaf College
, Northfield, MN, USA
Natalia Bernardes
Formal analysis, Visualization
4Departments of Pharmacology and Biophysics,
University of Texas Southwestern Medical Center
, Dallas, TX, USA
Yuh Min Chook
Formal analysis, Supervision, Visualization, Writing - review & editing
4Departments of Pharmacology and Biophysics,
University of Texas Southwestern Medical Center
, Dallas, TX, USA
Correspondence to Jacek Gaertig: [email protected]
*
A.S. Deraniyagala and W. Maier contributed equally to this paper.
Disclosures: The authors declare no competing interests exist.
1
“Left and right” are based on the cell’s perspective.
Received:
September 09 2024
Revision Received:
January 11 2025
Accepted:
February 27 2025
Online ISSN: 1540-8140
Print ISSN: 0021-9525
Funding
Funder(s):
National Institutes of Health
- Award Id(s): R01GM135444,R35GM152057,R35GM144137
Funder(s):
Welch Foundation
- Award Id(s): I-1532
Funder(s):
National Science Foundation
- Award Id(s): 1947608
Funder(s):
German Federal Ministry of Education and Research
- Award Id(s): 031L0101C
© 2025 Deraniyagala et al.
2025
Deraniyagala et al.
This article is distributed under the terms as described at https://rupress.org/pages/terms102024/.
J Cell Biol (2025) 224 (6): e202409057.
Article history
Received:
September 09 2024
Revision Received:
January 11 2025
Accepted:
February 27 2025
Citation
Anushi Suwaneththiya Deraniyagala, Wolfgang Maier, Mireya Parra, Elise Nanista, Deborah Oluwabukola Sowunmi, Michael Hassan, Nathan Chasen, Sunita Sharma, Karl F. Lechtreck, Eric S. Cole, Natalia Bernardes, Yuh Min Chook, Jacek Gaertig; Importin-9 and a TPR domain protein MpH drive periodic patterning of ciliary arrays in Tetrahymena. J Cell Biol 2 June 2025; 224 (6): e202409057. doi: https://doi.org/10.1083/jcb.202409057
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