Dynamics of growth zone patterning in the milkweed bug <i>Oncopeltus fasciatus</i>

Auman, Tzach; Vreede, Barbara; Weiss, Aryeh; Hester, Susan D.; Williams, Terri A.; Nagy, Lisa M.; Chipman, Ariel D.

doi:10.1242/dev.142091

Cited by 29 publications

(56 citation statements)

References 65 publications

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“…We have previously documented the changes in size of the growth zone throughout the segmentation process (7). Here we expand on these results by documenting the expression levels of two genes holding central positions in the segmentation cascade, relative to the dynamic growth zone ( Fig.…”

Section: Changes In the Growth Zonementioning

confidence: 72%

“…The expression pattern of eve (7,14) includes a domain of solid expression in the posterior growth zone, and a striped expression domain in the anterior growth zone ( Fig. 1A-A').…”

Section: Even-skipped (Eve)mentioning

confidence: 99%

“…Interestingly, h, which is a pair-rule gene in Drosophila and in Tribolium (22), is expressed segmentally late in the cascade, anterior to the expression of wg and inv, although it has an earlier non-segmental mesodermal expression. The point of activation of inv was previously defined as the border between the growth zone and the segmented germband (7). Genes that are expressed in stripes at this border (the segment polarity genes and the secondary pair-rule genes) remain active throughout the germband stage and maintain their striped expression in each segment as the segments continue to mature.…”

Section: The Segmentation "Cascade" Of Oncopeltusmentioning

confidence: 99%

“…Posterior segments are patterned sequentially from a growth zone. Our previous work on the Oncopeltus growth zone (7) showed that it is divided into two functional domains: a posterior growth zone with high levels of cell proliferation and stable gene expression patterns, and an anterior growth zone with dynamic gene expression patterns and a reduced level of cell proliferation. Comparing this organization to that found in other arthropods, we suggested that it is a general feature of sequentially segmenting arthropods.…”

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confidence: 99%

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Growth zone segmentation in the milkweed bug Oncopeltus fasciatus sheds light on the evolution of insect segmentation

Auman

Chipman

2018

Preprint

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One of the best studied developmental processes is the Drosophila segmentation cascade.However, this cascade is generally considered to be highly derived and unusual. We present a detailed analysis of the sequential segmentation cascade of the milkweed bug Oncopletus fasciatus, as a comparison to Drosophila, with the aim of reconstructing the evolution of insect segmentation. We analyzed the expression of 12 genes, representing different phases during segmentation. We reconstruct the spatio-temporal relationships among these genes And their roles and position in the cascade. We conclude that sequential segmentation in the Oncopeltus germband includes three phases: Primary pair-rule genes generate segmental gene expression in the anterior growth zone, followed by secondary pair-rule genes, expressed in the transition between the growth zone and the segmented germband. Segment polarity genes are expressed in the segmented germband. This process generates a single-segment periodicity, and does not have a double-segment pattern at any stage.Introduction:

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Section: Changes In the Growth Zonementioning

confidence: 72%

“…The expression pattern of eve (7,14) includes a domain of solid expression in the posterior growth zone, and a striped expression domain in the anterior growth zone ( Fig. 1A-A').…”

Section: Even-skipped (Eve)mentioning

confidence: 99%

Section: The Segmentation "Cascade" Of Oncopeltusmentioning

confidence: 99%

mentioning

confidence: 99%

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Growth zone segmentation in the milkweed bug Oncopeltus fasciatus sheds light on the evolution of insect segmentation

Auman

Chipman

2018

Preprint

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“…Since we did not perform EdU incorporation studies at the stage that they analyzed (late elongation; stage A9) [22], it is not possible to correlate their findings with our results (early- and mid-elongation). In addition, sequential segmentation starts later in Oncopeltus (from the first abdominal segment) than in Tribolium (from the mandibular segment) [24, 33], making it even more difficult to compare stages between both insects.…”

Section: Resultsmentioning

confidence: 99%

Contribution of cell proliferation to axial elongation in the red flour beetle Tribolium castaneum

et al. 2017

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Most arthropods generate their posterior bodies by adding segments periodically, as the embryo grows, from a posteriorly located region called the segment addition zone. This mode of segmentation is shared with vertebrates and relies on oscillatory mechanisms, where the temporal periodicity of a clock is translated into repetitive spatial patterns. This ordered anterior-to-posterior pattern is achieved at the same time as the tissue elongates, opening the question of the functional coordination between the mechanisms of segmental patterning and posterior growth. The study of these processes in different arthropods has played an important role in unravelling some of the molecular mechanisms of segment formation. However, the behavior of cells during elongation and how cellular processes affect this segmental patterning has been poorly studied. Cell proliferation together with cell rearrangements are presumed to be the major forces driving axis elongation in the red flour beetle Tribolium castaneum. However, there still no strong evidence about the role and distribution of cell proliferation within the embryo. In this study, we propose to address these questions by using whole embryo cultures and pharmacological manipulation. We show that considerable cell proliferation occurs during germband elongation, measured by incorporation of the nucleoside analog of thymidine 5-Ethynyl-2’-deoxyuridine, EdU. Moreover, proliferating cells appeared to be spread along the elongating embryo with a posterior bias at early segmentation. In addition, when we blocked cell division, treated germbands were always shorter than controls and in some cases not able to fully elongate, even when control embryos already started to retract and leg buds are evident. Finally, we found that the absence of cell proliferation has no apparent effect on segmental patterning, as evidenced by Tc-engrailed (Tc-en) gene expression.

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Embryonic expression of priapulid Wnt genes

et al. 2019

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Posterior elongation of the developing embryo is a common feature of animal development. One group of genes that is involved in posterior elongation is represented by the Wnt genes, secreted glycoprotein ligands that signal to specific receptors on neighbouring cells and thereby establish cell-to-cell communication. In segmented animals such as annelids and arthropods, Wnt signalling is also likely involved in segment border formation and regionalisation of the segments. Priapulids represent unsegmented worms that are distantly related to arthropods. Despite their interesting phylogenetic position and their importance for the understanding of ecdysozoan evolution, priapulids still represent a highly underinvestigated group of animals. Here, we study the embryonic expression patterns of the complete sets of Wnt genes in the priapulids Priapulus caudatus and Halicryptus spinulosus . We find that both priapulids possess a complete set of 12 Wnt genes. At least in Priapulus , most of these genes are expressed in and around the posterior-located blastopore and thus likely play a role in posterior elongation. Together with previous work on the expression of other genetic factors such as caudal and even-skipped , this suggests that posterior elongation in priapulids is under control of the same (or very similar) conserved gene regulatory network as in arthropods. Electronic supplementary material The online version of this article (10.1007/s00427-019-00636-6) contains supplementary material, which is available to authorized users.

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Dynamics of growth zone patterning in the milkweed bug Oncopeltus fasciatus

Cited by 29 publications

References 65 publications

Growth zone segmentation in the milkweed bug Oncopeltus fasciatus sheds light on the evolution of insect segmentation

Growth zone segmentation in the milkweed bug Oncopeltus fasciatus sheds light on the evolution of insect segmentation

Contribution of cell proliferation to axial elongation in the red flour beetle Tribolium castaneum

Embryonic expression of priapulid Wnt genes

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