Tissue-specific compensatory mechanisms maintain tissue architecture and body size independent of cell size in polyploid zebrafish

Genome duplications and ploidy transitions have occurred in nearly every major taxon of eukaryotes, but they are far more common in plants than in animals. Due to the conservation of the nuclear:cytoplasmic volume ratio increased DNA content results in larger cells. In plants, polyploid organisms ar...

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Veröffentlicht in:Developmental biology 2024-05, Vol.509, p.85-96
Hauptverfasser: Small, C.D., Benfey, T.J., Crawford, B.D.
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Sprache:eng
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Zusammenfassung:Genome duplications and ploidy transitions have occurred in nearly every major taxon of eukaryotes, but they are far more common in plants than in animals. Due to the conservation of the nuclear:cytoplasmic volume ratio increased DNA content results in larger cells. In plants, polyploid organisms are larger than diploids as cell number remains relatively constant. Conversely, vertebrate body size does not correlate with cell size and ploidy as vertebrates compensate for increased cell size to maintain tissue architecture and body size. This has historically been explained by a simple reduction in cell number that matches the increase in cell size maintaining body size as ploidy increases, but here we show that the compensatory mechanisms that maintain body size in triploid zebrafish are tissue-specific: A) erythrocytes respond in the classical pattern with a reduced number of larger erythrocytes in circulation, B) muscle, a tissue comprised of polynucleated muscle fibers, compensates by reducing the number of larger nuclei such that myofiber and myotome size in unaffected by ploidy, and C) vascular tissue compensates by thickening blood vessel walls, possibly at the expense of luminal diameter. Understanding the physiological implications of ploidy on tissue function requires a detailed description of the specific mechanisms of morphological compensation occurring in each tissue to understand how ploidy changes affect development and physiology. [Display omitted] •Tissue-specific mechanisms compensate for changes in cell size.•Blastomere size, cleavage pattern and rate are not affected by ploidy.•Erythrocytes conform to the canonical pattern of ‘fewer but larger cells'.•Multinucleate skeletal muscle cells adjust the number of nuclei to maintain size.•Vasculature is comprised of the same number and pattern of larger endothelial cells.
ISSN:0012-1606
1095-564X
DOI:10.1016/j.ydbio.2024.02.005