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Scaling of internal organs during Drosophila embryonic development

Many species show a diverse range of sizes; for example, domestic dogs have large variation in body mass. Yet, the internal structure of the organism remains similar, i.e., the system scales to organism size. Drosophila melanogaster has been a powerful model system for exploring scaling mechanisms....

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Autores principales: Tiwari, Prabhat, Rengarajan, Hamsawardhini, Saunders, Timothy E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Biophysical Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8516638/
https://www.ncbi.nlm.nih.gov/pubmed/34087212
http://dx.doi.org/10.1016/j.bpj.2021.05.023
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author Tiwari, Prabhat
Rengarajan, Hamsawardhini
Saunders, Timothy E.
author_facet Tiwari, Prabhat
Rengarajan, Hamsawardhini
Saunders, Timothy E.
author_sort Tiwari, Prabhat
collection PubMed
description Many species show a diverse range of sizes; for example, domestic dogs have large variation in body mass. Yet, the internal structure of the organism remains similar, i.e., the system scales to organism size. Drosophila melanogaster has been a powerful model system for exploring scaling mechanisms. In the early embryo, gene expression boundaries scale very precisely to embryo length. Later in development, the adult wings grow with remarkable symmetry and scale well with animal size. Yet, our knowledge of whether internal organs initially scale to embryo size remains largely unknown. Here, we utilize artificially small Drosophila embryos to explore how three critical internal organs—the heart, hindgut, and ventral nerve cord (VNC)—adapt to changes in embryo morphology. We find that the heart scales precisely with embryo length. Intriguingly, reduction in cardiac cell length, rather than number, appears to be important in controlling heart length. The hindgut, which is the first chiral organ to form, displays scaling with embryo size under large-scale changes in the artificially smaller embryos but shows few hallmarks of scaling within wild-type size variation. Finally, the VNC only displays weak scaling behavior; even large changes in embryo geometry result in only small shifts in VNC length. This suggests that the VNC may have an intrinsic minimal length that is largely independent of embryo length. Overall, our work shows that internal organs can adapt to embryo size changes in Drosophila, but the extent to which they scale varies significantly between organs.
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spelling pubmed-85166382022-10-05 Scaling of internal organs during Drosophila embryonic development Tiwari, Prabhat Rengarajan, Hamsawardhini Saunders, Timothy E. Biophys J Articles Many species show a diverse range of sizes; for example, domestic dogs have large variation in body mass. Yet, the internal structure of the organism remains similar, i.e., the system scales to organism size. Drosophila melanogaster has been a powerful model system for exploring scaling mechanisms. In the early embryo, gene expression boundaries scale very precisely to embryo length. Later in development, the adult wings grow with remarkable symmetry and scale well with animal size. Yet, our knowledge of whether internal organs initially scale to embryo size remains largely unknown. Here, we utilize artificially small Drosophila embryos to explore how three critical internal organs—the heart, hindgut, and ventral nerve cord (VNC)—adapt to changes in embryo morphology. We find that the heart scales precisely with embryo length. Intriguingly, reduction in cardiac cell length, rather than number, appears to be important in controlling heart length. The hindgut, which is the first chiral organ to form, displays scaling with embryo size under large-scale changes in the artificially smaller embryos but shows few hallmarks of scaling within wild-type size variation. Finally, the VNC only displays weak scaling behavior; even large changes in embryo geometry result in only small shifts in VNC length. This suggests that the VNC may have an intrinsic minimal length that is largely independent of embryo length. Overall, our work shows that internal organs can adapt to embryo size changes in Drosophila, but the extent to which they scale varies significantly between organs. The Biophysical Society 2021-10-05 2021-06-02 /pmc/articles/PMC8516638/ /pubmed/34087212 http://dx.doi.org/10.1016/j.bpj.2021.05.023 Text en © 2021 Biophysical Society. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Articles
Tiwari, Prabhat
Rengarajan, Hamsawardhini
Saunders, Timothy E.
Scaling of internal organs during Drosophila embryonic development
title Scaling of internal organs during Drosophila embryonic development
title_full Scaling of internal organs during Drosophila embryonic development
title_fullStr Scaling of internal organs during Drosophila embryonic development
title_full_unstemmed Scaling of internal organs during Drosophila embryonic development
title_short Scaling of internal organs during Drosophila embryonic development
title_sort scaling of internal organs during drosophila embryonic development
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8516638/
https://www.ncbi.nlm.nih.gov/pubmed/34087212
http://dx.doi.org/10.1016/j.bpj.2021.05.023
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