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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Main Authors: Savvas J. Constantinou, Nicole Duan, Lisa M. Nagy, Ariel D. Chipman, Terri A. Williams
Format: Article
Language:English
Published: BMC 2020-01-01
Series:EvoDevo
Subjects:
Wnt
EdU
Online Access:https://doi.org/10.1186/s13227-020-0147-0
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spelling 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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