aristaless1 has a dual role in appendage formation and wing color specification during butterfly development
Abstract Background Highly diverse butterfly wing patterns have emerged as a powerful system for understanding the genetic basis of phenotypic variation. While the genetic basis of this pattern variation is being clarified, the precise developmental pathways linking genotype to phenotype are not wel...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-05-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-023-01601-6 |
| _version_ | 1797831886169440256 |
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| author | Erick X. Bayala Nicholas VanKuren Darli Massardo Marcus R. Kronforst |
| author_facet | Erick X. Bayala Nicholas VanKuren Darli Massardo Marcus R. Kronforst |
| author_sort | Erick X. Bayala |
| collection | DOAJ |
| description | Abstract Background Highly diverse butterfly wing patterns have emerged as a powerful system for understanding the genetic basis of phenotypic variation. While the genetic basis of this pattern variation is being clarified, the precise developmental pathways linking genotype to phenotype are not well understood. The gene aristaless, which plays a role in appendage patterning and extension, has been duplicated in Lepidoptera. One copy, aristaless1, has been shown to control a white/yellow color switch in the butterfly Heliconius cydno, suggesting a novel function associated with color patterning and pigmentation. Here we investigate the developmental basis of al1 in embryos, larvae, and pupae using new antibodies, CRISPR/Cas9, RNAi, qPCR assays of downstream targets, and pharmacological manipulation of an upstream activator. Results We find that Al1 is expressed at the distal tips of developing embryonic appendages consistent with its ancestral role. In developing wings, we observe Al1 accumulation within developing scale cells of white H. cydno during early pupation while yellow scale cells exhibit little Al1 at this time point. Reduced Al1 expression is also associated with yellow scale development in al1 knockouts and knockdowns. We propose that Al1 expression in future white scales might be related to an observed downregulation of the enzyme Cinnabar and other genes that synthesize and transport the yellow pigment, 3–hydroxykynurenine (3-OHK). Finally, we provide evidence that Al1 activation is under the control of Wnt signaling. Conclusions We propose a model in which high levels of Al1 during early pupation, which are mediated by Wnt, are important for melanic pigmentation and specifying white portions of the wing while reduced levels of Al1 during early pupation promote upregulation of proteins needed to move and synthesize 3-OHK, promoting yellow pigmentation. In addition, we discuss how the ancestral role of aristaless in appendage extension may be relevant in understanding the cellular mechanism behind color patterning in the context of the heterochrony hypothesis. |
| first_indexed | 2024-04-09T13:59:59Z |
| format | Article |
| id | doaj.art-685cea320bd84851b15a3c9cc9b9496d |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-09T13:59:59Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-685cea320bd84851b15a3c9cc9b9496d2023-05-07T11:24:15ZengBMCBMC Biology1741-70072023-05-0121111910.1186/s12915-023-01601-6aristaless1 has a dual role in appendage formation and wing color specification during butterfly developmentErick X. Bayala0Nicholas VanKuren1Darli Massardo2Marcus R. Kronforst3Department of Ecology & Evolution, University of ChicagoDepartment of Ecology & Evolution, University of ChicagoDepartment of Ecology & Evolution, University of ChicagoDepartment of Ecology & Evolution, University of ChicagoAbstract Background Highly diverse butterfly wing patterns have emerged as a powerful system for understanding the genetic basis of phenotypic variation. While the genetic basis of this pattern variation is being clarified, the precise developmental pathways linking genotype to phenotype are not well understood. The gene aristaless, which plays a role in appendage patterning and extension, has been duplicated in Lepidoptera. One copy, aristaless1, has been shown to control a white/yellow color switch in the butterfly Heliconius cydno, suggesting a novel function associated with color patterning and pigmentation. Here we investigate the developmental basis of al1 in embryos, larvae, and pupae using new antibodies, CRISPR/Cas9, RNAi, qPCR assays of downstream targets, and pharmacological manipulation of an upstream activator. Results We find that Al1 is expressed at the distal tips of developing embryonic appendages consistent with its ancestral role. In developing wings, we observe Al1 accumulation within developing scale cells of white H. cydno during early pupation while yellow scale cells exhibit little Al1 at this time point. Reduced Al1 expression is also associated with yellow scale development in al1 knockouts and knockdowns. We propose that Al1 expression in future white scales might be related to an observed downregulation of the enzyme Cinnabar and other genes that synthesize and transport the yellow pigment, 3–hydroxykynurenine (3-OHK). Finally, we provide evidence that Al1 activation is under the control of Wnt signaling. Conclusions We propose a model in which high levels of Al1 during early pupation, which are mediated by Wnt, are important for melanic pigmentation and specifying white portions of the wing while reduced levels of Al1 during early pupation promote upregulation of proteins needed to move and synthesize 3-OHK, promoting yellow pigmentation. In addition, we discuss how the ancestral role of aristaless in appendage extension may be relevant in understanding the cellular mechanism behind color patterning in the context of the heterochrony hypothesis.https://doi.org/10.1186/s12915-023-01601-6HeliconiusAristalessAppendage formationButterfly color patterningWing pigmentationHeterochrony |
| spellingShingle | Erick X. Bayala Nicholas VanKuren Darli Massardo Marcus R. Kronforst aristaless1 has a dual role in appendage formation and wing color specification during butterfly development BMC Biology Heliconius Aristaless Appendage formation Butterfly color patterning Wing pigmentation Heterochrony |
| title | aristaless1 has a dual role in appendage formation and wing color specification during butterfly development |
| title_full | aristaless1 has a dual role in appendage formation and wing color specification during butterfly development |
| title_fullStr | aristaless1 has a dual role in appendage formation and wing color specification during butterfly development |
| title_full_unstemmed | aristaless1 has a dual role in appendage formation and wing color specification during butterfly development |
| title_short | aristaless1 has a dual role in appendage formation and wing color specification during butterfly development |
| title_sort | aristaless1 has a dual role in appendage formation and wing color specification during butterfly development |
| topic | Heliconius Aristaless Appendage formation Butterfly color patterning Wing pigmentation Heterochrony |
| url | https://doi.org/10.1186/s12915-023-01601-6 |
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