The expression pattern of the genes engrailed, pax6, otd and six3 with special respect to head and eye development in Euperipatoides kanangrensis Reid 1996 (Onychophora: Peripatopsidae)

Abstract

The genes otd/otx, six3, pax6 and engrailed are involved in eye patterning in many animals. Here we describe the expression pattern of the homologs to otd/otx, six3, pax6 and engrailed in the developing Euperipatoides kanangrensis embryos. Special reference is given to the expression in the protocerebral/ocular region. E.kanangrensis otd is expressed in the posterior part of the protocerebral/ocular segment before, during, and after eye invagination. E.kanangrensis otd is also expressed segmentally in the developing ventral nerve cord. The E.kanangrensis six3 is located at the extreme anterior part of the protocerebral/ocular segment and not at the location of the developing eyes. Pax6 is expressed in a broad zone at the posterior part of the protocerebral/ocular segment but only week expression can be seen at early onset of eye invagination. In late stages of development, the expression in the eye is upregulated. Pax6 is also expressed in the invaginating hypocerebral organs, thus supporting earlier suggestions that the hypocerebral organs in onychophorans are glands. Pax6 transcripts are also present in the developing ventral nerve cord. The segment polarity gene engrailed is expressed at the dorsal side of the developing eye including only a subset of the cells of the invaginating eye vesicle. We show that engrailed is not expressed in the neuroectoderm of the protocerebral/ocular segment as in the other segments. In addition, we discuss other aspect of otd, six3 and pax6 expression that are relevant to our understanding of evolutionary changes in morphology and function in arthropods.

Onychophora

“…In embryos of Euperipatoides kanangrensis , six3 is expressed in the anterior-most region of the antennal segment, whereas otd / otx is expressed in the posterior region. Furthermore, otd / otx is also expressed in the neuroectoderm and eye anlagen of the antennal segment as well as in the anterior part of the stomodeum, which lies between the antennal and jaw segments (note that optix in Steinmetz et al 2010 corresponds to otd / otx in Eriksson et al 2013 ). In addition to otd / otx , the onychophoran eye anlage expresses a pax6 homolog, which is considered to be a master control gene for eye development in various bilaterians (Gehring and Ikeo 1999 ;Kozmik 2008 ;Eriksson et al 2013 ).…”

“…Furthermore, otd / otx is also expressed in the neuroectoderm and eye anlagen of the antennal segment as well as in the anterior part of the stomodeum, which lies between the antennal and jaw segments (note that optix in Steinmetz et al 2010 corresponds to otd / otx in Eriksson et al 2013 ). In addition to otd / otx , the onychophoran eye anlage expresses a pax6 homolog, which is considered to be a master control gene for eye development in various bilaterians (Gehring and Ikeo 1999 ;Kozmik 2008 ;Eriksson et al 2013 ). Moreover, pax6 expression is present in the invaginating anlagen of the hypocerebral organs in onychophorans, thus supporting the hypothesis of a neurosecretory/glandular function of these structures (Eriksson et al 2005(Eriksson et al , 2013.…”

“…4.20E-H ;Kennel 1888 ;Sedgwick 1888a ;Walker and Tait 2004 ;Mayer 2006b ;Eriksson et al 2013 ). Each eye vesicle buds off from the ectoderm and its proximal cells develop into the retina, which contains the photoreceptors and shading pigment granules, whereas the distal cells give rise to the sub-cornea (Mayer 2006b ).…”

“…As in many other bilaterians, the anterior-most body region of the onychophoran embryo is patterned by typical anterior/head patterning genes, including six3 , orthodenticle ( otd / otx ), pax6 , and collier ( col ) (Steinmetz et al 2010 ;Janssen et al 2011 ;Eriksson et al 2013 ). In embryos of Euperipatoides kanangrensis , six3 is expressed in the anterior-most region of the antennal segment, whereas otd / otx is expressed in the posterior region.…”

The metameric pattern of Hypsibius dujardini(Eutardigrada) and its relationship to that of other panarthropods

“…Thus, although the panarthropod common ancestor is characterized as being homonomously segmented [19,22,23,32,[47][48][49][50], these comparative data suggest that segmental diversity may have evolved prior to the divergence of the three panarthropod lineages. The developmental mechanism responsible for differentiating anterior segments in Onychophora and Arthropoda is conserved [51,52]. The discovery of segmental diversity in tardigrades raises the question of whether this mechanism is even evolutionarily more ancient.…”