Transcriptome analyses in eukaryotes, including mice and humans, have identified polyA-containing transcripts that lack long open reading frames (ORFs; >100 amino acids)1,2. These transcripts are believed most likely to function as non-coding RNAs, but their translational capacities and biological activities have not been characterized in detail. Here, we report that polished rice (pri), which was previously identified as a gene for a non-coding RNA in Drosophila3,4, is in fact transcribed into a polycistronic mRNA that contains evolutionarily conserved short ORFs that encode 11 or 32 amino acid-long peptides. pri was expressed in all epithelial tissues during embryogenesis. The loss of pri function completely eliminated apical cuticular structures, including the epidermal denticles and tracheal taenidia, and also caused defective tracheal-tube expansion. We found that pri is essential for the formation of specific F-actin bundles that prefigures the formation of the denticles and taenidium. We provide evidences that pri acts non-cell autonomously and that four of the conserved pri ORFs are functionally redundant. These results demonstrate that pri has essential roles in epithelial morphogenesis by regulating F-actin organization.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
BMC Genomics Open Access 30 November 2022
Mammalian Genome Open Access 31 January 2022
Molecular Cancer Open Access 04 February 2020
Subscribe to Journal
Get full journal access for 1 year
only $8.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Ota, T. et al. Complete sequencing and characterization of 21,243 full-length human cDNAs. Nature Genet. 36, 40–45 (2004).
Carninci, P. et al. The transcriptional landscape of the mammalian genome. Science 309, 1559–1563 (2005).
Tupy, J. L. et al. Identification of putative noncoding polyadenylated transcripts in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 102, 5495–5500 (2005).
Inagaki, S. et al. Identification and expression analysis of putative mRNA-like non-coding RNA in Drosophila. Genes Cells 10, 1163–1173 (2005).
Delon, I., Chanut-Delalande, H. & Payre, F. The Ovo/Shavenbaby transcription factor specifies actin remodelling during epidermal differentiation in Drosophila. Mech. Dev. 120, 747–758 (2003).
Price, M. H., Roberts, D. M., McCartney, B. M., Jezuit, E. & Peifer, M. Cytoskeletal dynamics and cell signaling during planar polarity establishment in the Drosophila embryonic denticle. J. Cell Sci. 119, 403–415 (2006).
Walters, J. W., Dilks, S. A. & Dinardo, S. Planar polarization of the denticle field in the Drosophila embryo: roles for myosin II (zipper) and fringe. Dev. Biol. 297, 323–339 (2006).
Kiehart, D. P., Galbraith, C. G., Edwards, K. A., Rickoll, W. L. & Montague, R. A. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149, 471–490 (2000).
Payre, F., Vincent, A. & Carreno, S. ovo/svb integrates Wingless and DER pathways to control epidermis differentiation. Nature 400, 271–275 (1999).
Shiga, Y., Tanaka-Matakatsu, M. & Hayashi, S. A nuclear GFP β-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Differ. 38, 99–106 (1996).
Matusek, T. et al. The Drosophila formin DAAM regulates the tracheal cuticle pattern through organizing the actin cytoskeleton. Development 133, 957–966 (2006).
Chihara, T., Kato, K., Taniguchi, M., Ng, J. & Hayashi, S. Rac promotes epithelial cell rearrangement during tracheal tubulogenesis in Drosophila. Development 130, 1419–1428 (2003).
Beitel, G. J. & Krasnow, M. A. Genetic control of epithelial tube size in the Drosophila tracheal system. Development 127, 3271–3282 (2000).
Moussian, B., Soding, J., Schwarz, H. & Nusslein-Volhard, C. Retroactive, a membrane-anchored extracellular protein related to vertebrate snake neurotoxin-like proteins, is required for cuticle organization in the larva of Drosophila melanogaster. Dev. Dyn. 233, 1056–1063 (2005).
Moussian, B. et al. Drosophila Knickkopf and Retroactive are needed for epithelial tube growth and cuticle differentiation through their specific requirement for chitin filament organization. Development 133, 163–171 (2006).
Luschnig, S., Batz, T., Armbruster, K. & Krasnow, M. A. serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr. Biol. 16, 186–194 (2006).
Savard, J., Marques-Souza, H., Aranda, M. & Tautz, D. A segmentation gene in tribolium produces a polycistronic mRNA that codes for multiple conserved peptides. Cell 126, 559–569 (2006).
Chanut-Delalande, H., Fernandes, I., Roch, F., Payre, F. & Plaza, S. Shavenbaby couples patterning to epidermal cell shape control. PLoS Biol. 4, e290 (2006).
Parks, A. L. et al. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nature Genet. 36, 288–292 (2004).
Spradling, A. C. & Rubin, G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341–347 (1982).
Bartoszewski, S. & Gibson, J. B. Injecting un-dechrionated eggs of Drosophila melanogaster under ethanol Drosophila Information Newsletter 14 (1994).
Stern, D. L. & Sucena, E. in Drosophila Protocols (eds Sullivan, W., Ashburner, M. & Hawley, R. S.) 601–615 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 2000).
Nagaso, H., Murata, T., Day, N. & Yokoyama, K. K. Simultaneous detection of RNA and protein by in situ hybridization and immunological staining. J. Histochem. Cytochem. 49, 1177–1182 (2001).
Patel, N. in Drosophila melanogaster: Practical Uses in Cell and Molecular Biology (ed. Lawrence S. B. Goldstein, E. A. F.) 445–488 (Academic Press, San Diego, 1995).
Brook, W. J. & Cohen, S. M. Antagonistic interactions between wingless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila Leg. Science 273, 1373–1377 (1996).
Tonning, A. et al. A transient luminal chitinous matrix is required to model epithelial tube diameter in the Drosophila trachea. Dev. Cell 9, 423–430 (2005).
Kondo, T., Inagaki, S., Yasuda, K. & Kageyama, Y. Rapid construction of Drosophila RNAi transgenes using pRISE, a P-element-mediated transformation vector exploiting an in vitro recombination system. Genes Genet. Syst. 81, 129–134 (2006).
We thank Y. Hiromi, A. Nakamura and K. Yasuda for critical comments and discussion. We also thank Bloomington and Kyoto Drosophila Stock Center, as well as National Institute of Genetics (Mishima, Japan) and Harvard Medical School, for kind supply of Drosophila strains. This work was supported by Grant-in-Aid for Scientific Research on Priority Areas from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) to S.H. and Y.K.
The authors declare no competing financial interests.
Supplementary figures S1, S2, S3, S4 and Supplementary methods (PDF 1730 kb)
Supplementary Movie 1 (MOV 4450 kb)
Supplementary Movie 2 (MOV 4050 kb)
Supplementary Movie 3 (MOV 2604 kb)
Supplementary Movie 4 (MOV 3634 kb)
About this article
Cite this article
Kondo, T., Hashimoto, Y., Kato, K. et al. Small peptide regulators of actin-based cell morphogenesis encoded by a polycistronic mRNA. Nat Cell Biol 9, 660–665 (2007). https://doi.org/10.1038/ncb1595
This article is cited by
BMC Genomics (2022)
Mammalian Genome (2022)
Genome Instability & Disease (2021)
Molecular Cancer (2020)
Nature Chemical Biology (2020)