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Epithelial cell-turnover ensures robust coordination of tissue growth in Drosophila ribosomal protein mutants.

ABSTRACT: Highly reproducible tissue development is achieved by robust, time-dependent coordination of cell proliferation and cell death. To study the mechanisms underlying robust tissue growth, we analyzed the developmental process of wing imaginal discs in Drosophila Minute mutants, a series of heterozygous mutants for a ribosomal protein gene. Minute animals show significant developmental delay during the larval period but develop into essentially normal flies, suggesting there exists a mechanism ensuring robust tissue growth during abnormally prolonged developmental time. Surprisingly, we found that both cell death and compensatory cell proliferation were dramatically increased in developing wing pouches of Minute animals. Blocking the cell-turnover by inhibiting cell death resulted in morphological defects, indicating the essential role of cell-turnover in Minute wing morphogenesis. Our analyses showed that Minute wing discs elevate Wg expression and JNK-mediated Dilp8 expression that causes developmental delay, both of which are necessary for the induction of cell-turnover. Furthermore, forced increase in Wg expression together with developmental delay caused by ecdysone depletion induced cell-turnover in the wing pouches of non-Minute animals. Our findings suggest a novel paradigm for robust coordination of tissue growth by cell-turnover, which is induced when developmental time axis is distorted.

SUBMITTER: Akai N

PROVIDER: S-EPMC7842893 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Epithelial cell-turnover ensures robust coordination of tissue growth in Drosophila ribosomal protein mutants.

Akai Nanami N Ohsawa Shizue S Sando Yukari Y Igaki Tatsushi T

PLoS genetics 20210128 1

Highly reproducible tissue development is achieved by robust, time-dependent coordination of cell proliferation and cell death. To study the mechanisms underlying robust tissue growth, we analyzed the developmental process of wing imaginal discs in Drosophila Minute mutants, a series of heterozygous mutants for a ribosomal protein gene. Minute animals show significant developmental delay during the larval period but develop into essentially normal flies, suggesting there exists a mechanism ensur ...[more]

PMID: 33507966

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Project description:BACKGROUND:Organisms, tissues and cells are genetically programmed to grow to a specific largely pre-set size and shape within the appropriate developmental timing. In the event of mutation, cell death, or tissue damage, the remaining cells may increase their rate of growth to compensate and generate an intact, potentially smaller, tissue or organism in order to achieve the desired size. A delay in the developmental timing could aid in this process. The insulin receptor signalling pathway with its central component, the Akt1 kinase, and endpoint regulator, the transcription factor foxo, plays a significant role in the control of growth. Drosophila melanogaster is an excellent model organism with a well-studied life cycle and a consistently developing compound eye that can undergo analysis to compare changes in the properties of adult ommatidia as an indicator of growth. FINDINGS:Imprecise excision of a PZ P-element inserted in the upstream region of Akt1 generated several novel hypomorphic alleles with internally deleted regions of the Pelement. These mutations lead to small, viable Drosophila that present with delays in development. Suppression of this phenotype by the directed expression of Akt1 (+) indicates that the phenotypes observed are Akt1 dependent. Somatic clones of the eyes, consisting of homozygous tissue in otherwise heterozygous organisms that develop within a standard timeframe, signify that more severe phenotypes are masked by an extension in the time of development of homozygous mutants. Generation of Drosophila having the hypomorphic Akt1 alleles and a null allele of the downstream target foxo result in a phenotype very similar to that of the foxo mutant and do not resemble the Akt1 mutants. CONCLUSION:The developmental delay of these novel Akt1 hypomorphs results in a latent phenotype uncovered by generation of somatic clones. The compensatory growth occurring during the extended time of development appears to be implemented through alteration of foxo activity. Production of clones is an effective and informative way to observe the effects of mutations that result in small, viable, developmentally delayed flies.

Dataset Information

Epithelial cell-turnover ensures robust coordination of tissue growth in Drosophila ribosomal protein mutants.

Publications

Epithelial cell-turnover ensures robust coordination of tissue growth in Drosophila ribosomal protein mutants.

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