A caudal mRNA gradient controls posterior development in the wasp Nasonia.
One of the earliest steps of embryonic development is the establishment of polarity along the anteroposterior axis. Extensive studies of Drosophila embryonic development have elucidated mechanisms for establishing polarity, while studies with other model systems have found that many of these molecular components are conserved through evolution. One exception is Bicoid, the master organizer of anterior development in Drosophila and higher dipterans, which is not conserved. Thus, the study of anteroposterior patterning in insects that lack Bicoid can provide insight into the evolution of the diversity of body plan patterning networks. To this end, we have established the long germ parasitic wasp Nasonia vitripennis as a model for comparative studies with Drosophila. Here we report that, in Nasonia, a gradient of localized caudal mRNA directs posterior patterning, whereas, in Drosophila, the gradient of maternal Caudal protein is established through translational repression by Bicoid of homogeneous caudal mRNA. Loss of caudal function in Nasonia results in severe segmentation defects. We show that Nasonia caudal is an activator of gap gene expression that acts far towards the anterior of the embryo, placing it atop a cascade of early patterning. By contrast, activation of gap genes in flies relies on redundant functions of Bicoid and Caudal, leading to a lack of dramatic action on gap gene expression: caudal instead plays a limited role as an activator of pair-rule gene expression. These studies, together with studies in short germ insects, suggest that caudal is an ancestral master organizer of patterning, and that its role has been reduced in higher dipterans such as Drosophila.
Olesnicky
Eugenia C
EC
New York University, Department of Biology, New York, NY 10003, USA.
Brent
Ava E
AE
Tonnes
Lori
L
Walker
Megan
M
Pultz
Mary Anne
MA
Leaf
David
D
Desplan
Claude
C
D000818:Animals; D019521:Body Patterning / Q000235:genetics*; D004330:Drosophila / Q000254:growth & development; D029721:Drosophila Proteins / Q000235:genetics / Q000502:physiology; D004625:Embryo, Nonmammalian / Q000737:chemistry / Q000378:metabolism; D005260:Female; D018507:Gene Expression Regulation, Developmental; D018398:Homeodomain Proteins / Q000235:genetics / Q000502:physiology; D019476:Insect Proteins / Q000037:antagonists & inhibitors / Q000235:genetics / Q000502:physiology*; D009154:Mutation; D010053:Ovary / Q000737:chemistry / Q000196:embryology; D034622:RNA Interference; D012333:RNA, Messenger / Q000032:analysis / Q000378:metabolism*; D014157:Transcription Factors / Q000235:genetics / Q000502:physiology; D014863:Wasps / Q000737:chemistry / Q000196:embryology* / Q000235:genetics; D015053:Zygote
D029721:Drosophila Proteins; D018398:Homeodomain Proteins; D019476:Insect Proteins; D012333:RNA, Messenger; D014157:Transcription Factors; C084564:cad protein, Drosophila