Gene expression suggests double-segmental and single-segmental patterning mechanisms during posterior segment addition in the beetle Tribolium castaneum

Abstract

In the model arthropod Drosophila, all segments are patterned simultaneously in the blastoderm. In most other arthropods, however, posterior segments are added sequentially from a posterior segment addition zone. Posterior addition of single segments likely represents the ancestral mode of arthropod segmentation, although in Drosophila, segments are patterned in pairs by the pair-rule genes. It has been shown that in the new model insect, the beetle Tribolium, a segmentation clock operates that apparently patterns all segments in pairs as well. Here, I report on the expression of the segment polarity gene H15/midline in Tribolium. In the anterior embryo, segmental stripes of H15 appear in pairs, but in the posterior of the embryo stripes appear in a single-segmental periodicity. This implies that either two completely different segmentationmechanisms may act in the germ band of Tribolium, that the segmentation clock changes its periodicity during development, or that the speed in which posterior segments are patterned changes. In any case, the data suggest the presence of another (or modified), yet undiscovered, mechanism of posterior segment addition in one of the best-understood arthropod models. The finding of a hitherto unrecognized segmentation mechanism in Tribolium may have major implications for the understanding of the origin of segmentation mechanisms, including the origin of pair rule patterning. It also calls for (re)-investigation of posterior segment addition in Tribolium and other previously studied arthropod models. KEY WORDS: segmentation, arthropod development, arthropod evolution, segment polarityOur understanding of arthropod segmentation comes primarily from studies on the model organism Drosophila melanogaster. Here, a hierarchic segmentation gene cascade operates to subdivide, in a stepwise fashion, a syncytial blastoderm that later develops without posterior segment addition into the complete adult body. Notably, one step of this segmentation mechanism comprises the temporal establishment of double-segmental units, as shown by the function (and expression) of the pair-rule genes. In most other arthropods, only anterior segments are formed from the blastoderm, and posterior segments are added from a posterior segment addition zone (Davis and Patel 2002). Posterior segment addition with a single-segmental periodicity likely represents the ancestral mechanism, as suggested by morphological observations and gene expression analysis Damen 2005, Janssen 2011). Evidence for double-segmental patterning mechanisms in the blastoderm, superficially comparable to Drosophila pair-rule patterning, has, however, been found in distantly related arthropods (Dearden et al., 2002, Janssen et al., 2012 Double-segmental patterning has also been found in tissue that is generated from the posterior segment addition zone in the beetle Tribolium castaneum (Choe et al., 2006) in addition to other insects (Davis et al., 2001, Mito et al., 2007, Erezyilmaz et al., 2009) and a distantly related arthropod, ...

A timer gene network is spatially regulated by the terminal system in theDrosophilaembryo

“…Intriguingly, a remarkably similar switch from double-segment to single-segment periodicity occurs towards the end of segmentation in the centipede Strigamia maritima , where stable, resolved eve stripes start appearing de novo in the anterior segmentation zone instead of emerging from posterior oscillatory expression (Brena and Akam, 2013). A possible switch from double-segmental to single-segmental patterning has also been reported for terminal segments in the beetle Tribolium (Janssen, 2014). These observations hint that terminal and trunk segments may be homonomous at the level of segment-polarity gene expression but derived from distinct ontogenetic programs.…”

Changing cell behaviours during beetle embryogenesis correlates with slowing of segmentation

“…Recently published work 51 suggests the terminal Tribolium segments may also switch from a pair-rule patterning mechanism to an unknown mechanism that generated single segments. Similarly, in a detailed analysis of axial variability in vertebrate segmentation, the transition between a constant rate of addition to a gradually slowing rate occurs at approximately the trunk/tail boundary 6 .…”

Gene expression analysis reveals that Delta/Notch signalling is not involved in onychophoran segmentation

“…Liu and Kaufman 2005 ; Kimelman and Martin 2012 ). The great majority of arthropods, including most other insects, add segments one by one or in pairs from a posterior segmentation zone (Chipman et al 2004 ; Schoppmeier and Damen 2005a ; Janssen 2011 , 2014 )—so-called short-germ mode development. Most of the segmentation genes that act during Drosophila segmentation also play a conserved or similar role in the segmentation process in short-germ arthropods (e.g.…”