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

2018 ◽  
Author(s):  
Tzach Auman ◽  
Ariel D. Chipman

AbstractOne 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.

Development ◽  
1987 ◽  
Vol 101 (1) ◽  
pp. 1-22 ◽  
Author(s):  
M. Akam

The metameric organization of the Drosophila embryo is generated in the first 5 h after fertilization. An initially rather simple pattern provides the foundation for subsequent development and diversification of the segmented part of the body. Many of the genes that control the formation of this pattern have been identified and at least twenty have been cloned. By combining the techniques of genetics, molecular biology and experimental embryology, it is becoming possible to unravel the role played by each of these genes. The repeating segment pattern is defined by the persistent expression of engrailed and of other genes of the ‘segment polarity’ class. The establishment of this pattern is directed by a transient molecular prepattern that is generated in the blastoderm by the activity of the ‘pair-rule’ genes. Maternal determinants at the poles of the egg coordinate this prepattern and define the anteroposterior sequence of pattern elements. The primary effect of these determinants is not known, but genes required for their production have been identified and the product of one of these, bicoid is known to be localized at the anterior of the egg. One early consequence of their activity is to define domains along the A-P axis within which a series of ‘cardinal’ genes are transcribed. The activity of the cardinal genes is required both to coordinate the process of segmentation and to define the early domains of homeotic gene expression. Further interactions between the homeotic genes and other classes of segmentation genes refine the initial establishment of segment identities.


Development ◽  
2019 ◽  
Vol 146 (17) ◽  
pp. dev181453 ◽  
Author(s):  
Katie Reding ◽  
Mengyao Chen ◽  
Yong Lu ◽  
Alys M. Cheatle Jarvela ◽  
Leslie Pick

2009 ◽  
Vol 334 (1) ◽  
pp. 300-310 ◽  
Author(s):  
Deniz F. Erezyilmaz ◽  
Hans C. Kelstrup ◽  
Lynn M. Riddiford

PLoS ONE ◽  
2014 ◽  
Vol 9 (11) ◽  
pp. e112909 ◽  
Author(s):  
Cornelia M. Hooper ◽  
Susan M. Hawes ◽  
Ursula R. Kees ◽  
Nicholas G. Gottardo ◽  
Peter B. Dallas

Gigabyte ◽  
2021 ◽  
Vol 2021 ◽  
pp. 1-13
Author(s):  
Sherry Miller ◽  
Teresa D. Shippy ◽  
Prashant S. Hosmani ◽  
Mirella Flores-Gonzalez ◽  
Lukas A. Mueller ◽  
...  

Insects have a segmented body plan that is established during embryogenesis when the anterior–posterior (A–P) axis is divided into repeated units by a cascade of gene expression. The cascade is initiated by protein gradients created by translation of maternally provided mRNAs, localized at the anterior and posterior poles of the embryo. Combinations of these proteins activate specific gap genes to divide the embryo into distinct regions along the anterior–posterior axis. Gap genes then activate pair-rule genes, which are usually expressed in parts of every other segment. The pair-rule genes, in turn, activate expression of segment polarity genes in a portion of each segment. The segmentation genes are generally conserved among insects, although there is considerable variation in how they are deployed. We annotated 25 segmentation gene homologs in the Asian citrus psyllid, Diaphorina citri. Most of the genes expected to be present in D. citri based on their phylogenetic distribution in other insects were identified and annotated. Two exceptions were eagle and invected, which are present in at least some hemipterans, but were not found in D. citri. Many of the segmentation pathway genes are likely to be essential for D. citri development, and thus they may be useful targets for gene-based pest control methods.


Development ◽  
1988 ◽  
Vol 104 (Supplement) ◽  
pp. 35-50 ◽  
Author(s):  
Ken Howard

The first indication of the formation of segment primordia in Drosophila is expression of the segment-polarity genes in particular parts of each primordium. These patterns are controlled by another class of genes, the pair-rule genes, which show characteristic two-segment periodic expression. Each pair-rule gene has a unique domain of activity and in one view different combinations of pair-rule gene products directly control the expression of the segment-polarity genes. There is a hierarchy within the pair-rule class revealed by pair-rule gene interactions. It is unlikely that these interactions generate the periodicity de novo. Instead, pair-rule genes respond to positional information generated by a system involving zygotic gap and maternal coordinate genes. In this paper, I will concentrate on the problem of the mechanism that generates these pair-rule patterns, the first periodic ones seen during segmentation. I will review and discuss some of the relevant literature, illustrating certain points with data from my recent work.


Development ◽  
1991 ◽  
Vol 113 (2) ◽  
pp. 419-430 ◽  
Author(s):  
R. Sommer ◽  
D. Tautz

Drosophila and Musca both belong to the group of higher dipteran flies and show morphologically a very similar early development. However, these two species are evolutionary separated by at least 100 million years. This presents the opportunity for a comparative analysis of segmentation gene expression across a large evolutionary distance in a very similar embryonic background. We have analysed in detail the early expression of the maternal gene bicoid, the gap genes hunchback, Kruppel, knirps and tailless, the pair-rule gene hairy, the segment-polarity gene engrailed and the homoeotic gene Ultrabithorax. We show that the primary expression domains of these genes are conserved, while some secondary expression aspects have diverged. Most notable is the finding of hunchback expression in 11–13 stripes shortly before gastrulation, as well as a delayed expression of terminal domains of various genes. We conclude that the early developmental gene hierarchy, as it has been defined in Drosophila, is evolutionary conserved in Musca domestica.


2019 ◽  
Author(s):  
Katie Reding ◽  
Mengyao Chen ◽  
Yong Lu ◽  
Alys M. Cheatle Jarvela ◽  
Leslie Pick

AbstractThe discovery of pair-rule genes (PRGs) in Drosophila revealed the existence of an underlying two-segment-wide prepattern directing embryogenesis. The milkweed bug Oncopeltus, a hemimetabolous insect, is a more representative arthropod: most of its segments form sequentially after gastrulation. Here we report the expression and function of orthologs of the complete set of nine Drosophila PRGs in Oncopeltus. Seven Of-PRG-orthologs are expressed in stripes in the primordia of every segment, rather than every-other segment, Of-runt is PR-like, and several are also expressed in the segment addition zone. RNAi-mediated knockdown of Of-odd-skipped, paired and sloppy-paired impacted all segments, with no indication of PR-like register. We confirm that Of-E75A is expressed in PR-like stripes, although it is not PR in Drosophila, demonstrating the existence of an underlying PR-like prepattern in Oncopeltus. These findings reveal that a switch occurred in regulatory circuits leading to segment formation: while several holometabolous insects are “Drosophila-like,” utilizing PRG-orthologs for PR-patterning, most Of-PRGs are expressed segmentally in Oncopeltus, a more basally-branching insect. Thus, an evolutionarily stable phenotype – segment formation – is directed by alternate regulatory pathways in diverse species.Summary StatementDespite the broad of conservation of segmentation in insects, the regulatory genes underlying this process in Drosophila have different roles in the hemipteran, Oncopeltus fasciatus.


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