Elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, Thamnocephalus platyurus
Abstract Background Segmentation in arthropods typically occurs by sequential addition of segments from a posterior growth zone. However, the amount of tissue required for growth and the cell behaviors producing posterior elongation are sparsely documented. Results Using precisely staged larvae of t...
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doaj-819ed57f33594b04bcb4ffaafcc24b252021-01-17T12:03:11ZengBMCEvoDevo2041-91392020-01-0111111810.1186/s13227-020-0147-0Elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, Thamnocephalus platyurusSavvas J. Constantinou0Nicole Duan1Lisa M. Nagy2Ariel D. Chipman3Terri A. Williams4Biology Department, Trinity CollegeBiology Department, Trinity CollegeDepartment of Molecular and Cellular Biology, University of ArizonaThe Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of JerusalemBiology Department, Trinity CollegeAbstract Background Segmentation in arthropods typically occurs by sequential addition of segments from a posterior growth zone. However, the amount of tissue required for growth and the cell behaviors producing posterior elongation are sparsely documented. Results Using precisely staged larvae of the crustacean, Thamnocephalus platyurus, we systematically examine cell division patterns and morphometric changes associated with posterior elongation during segmentation. We show that cell division occurs during normal elongation but that cells in the growth zone need only divide ~ 1.5 times to meet growth estimates; correspondingly, direct measures of cell division in the growth zone are low. Morphometric measurements of the growth zone and of newly formed segments suggest tagma-specific features of segment generation. Using methods for detecting two different phases in the cell cycle, we show distinct domains of synchronized cells in the posterior trunk. Borders of cell cycle domains correlate with domains of segmental gene expression, suggesting an intimate link between segment generation and cell cycle regulation. Conclusions Emerging measures of cellular dynamics underlying posterior elongation already show a number of intriguing characteristics that may be widespread among sequentially segmenting arthropods and are likely a source of evolutionary variability. These characteristics include: the low rates of posterior mitosis, the apparently tight regulation of cell cycle at the growth zone/new segment border, and a correlation between changes in elongation and tagma boundaries.https://doi.org/10.1186/s13227-020-0147-0ArthropodSegmentationGrowth zoneMitosisWntEdU |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Savvas J. Constantinou Nicole Duan Lisa M. Nagy Ariel D. Chipman Terri A. Williams |
spellingShingle |
Savvas J. Constantinou Nicole Duan Lisa M. Nagy Ariel D. Chipman Terri A. Williams Elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, Thamnocephalus platyurus EvoDevo Arthropod Segmentation Growth zone Mitosis Wnt EdU |
author_facet |
Savvas J. Constantinou Nicole Duan Lisa M. Nagy Ariel D. Chipman Terri A. Williams |
author_sort |
Savvas J. Constantinou |
title |
Elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, Thamnocephalus platyurus |
title_short |
Elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, Thamnocephalus platyurus |
title_full |
Elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, Thamnocephalus platyurus |
title_fullStr |
Elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, Thamnocephalus platyurus |
title_full_unstemmed |
Elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, Thamnocephalus platyurus |
title_sort |
elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, thamnocephalus platyurus |
publisher |
BMC |
series |
EvoDevo |
issn |
2041-9139 |
publishDate |
2020-01-01 |
description |
Abstract Background Segmentation in arthropods typically occurs by sequential addition of segments from a posterior growth zone. However, the amount of tissue required for growth and the cell behaviors producing posterior elongation are sparsely documented. Results Using precisely staged larvae of the crustacean, Thamnocephalus platyurus, we systematically examine cell division patterns and morphometric changes associated with posterior elongation during segmentation. We show that cell division occurs during normal elongation but that cells in the growth zone need only divide ~ 1.5 times to meet growth estimates; correspondingly, direct measures of cell division in the growth zone are low. Morphometric measurements of the growth zone and of newly formed segments suggest tagma-specific features of segment generation. Using methods for detecting two different phases in the cell cycle, we show distinct domains of synchronized cells in the posterior trunk. Borders of cell cycle domains correlate with domains of segmental gene expression, suggesting an intimate link between segment generation and cell cycle regulation. Conclusions Emerging measures of cellular dynamics underlying posterior elongation already show a number of intriguing characteristics that may be widespread among sequentially segmenting arthropods and are likely a source of evolutionary variability. These characteristics include: the low rates of posterior mitosis, the apparently tight regulation of cell cycle at the growth zone/new segment border, and a correlation between changes in elongation and tagma boundaries. |
topic |
Arthropod Segmentation Growth zone Mitosis Wnt EdU |
url |
https://doi.org/10.1186/s13227-020-0147-0 |
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