Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia.
The Bicoid (Bcd) gradient in Drosophila has long been a model for the action of a morphogen in establishing embryonic polarity. However, it is now clear that bcd is a unique feature of higher Diptera. An evolutionarily ancient gene, orthodenticle (otd), has a bcd-like role in the beetle Tribolium. Unlike the Bcd gradient, which arises by diffusion of protein from an anteriorly localized messenger RNA, the Tribolium Otd gradient forms by translational repression of otd mRNA by a posteriorly localized factor. These differences in gradient formation are correlated with differences in modes of embryonic patterning. Drosophila uses long germ embryogenesis, where the embryo derives from the entire anterior-posterior axis, and all segments are patterned at the blastoderm stage, before gastrulation. In contrast, Tribolium undergoes short germ embryogenesis: the embryo arises from cells in the posterior of the egg, and only anterior segments are patterned at the blastoderm stage, with the remaining segments arising after gastrulation from a growth zone. Here we describe the role of otd in the long germband embryo of the wasp Nasonia vitripennis. We show that Nasonia otd maternal mRNA is localized at both poles of the embryo, and resulting protein gradients pattern both poles. Thus, localized Nasonia otd has two major roles that allow long germ development. It activates anterior targets at the anterior of the egg in a manner reminiscent of the Bcd gradient, and it is required for pre-gastrulation expression of posterior gap genes.
Lynch
Jeremy A
JA
Center for Developmental Genetics, NYU Biology, 100 Washington Square East New York, New York 10003, USA.
Brent
Ava E
AE
Leaf
David S
DS
Pultz
Mary Anne
MA
Desplan
Claude
C
D000818:Animals; D019521:Body Patterning; D001517:Coleoptera / Q000196:embryology / Q000378:metabolism; D029721:Drosophila Proteins; D004331:Drosophila melanogaster / Q000196:embryology / Q000378:metabolism; D018507:Gene Expression Regulation, Developmental; D017344:Genes, Insect / Q000235:genetics; D018398:Homeodomain Proteins / Q000502:physiology; D019476:Insect Proteins / Q000235:genetics / Q000378:metabolism*; D008954:Models, Biological; D008969:Molecular Sequence Data; D034622:RNA Interference; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015534:Trans-Activators / Q000502:physiology; D014863:Wasps / Q000196:embryology* / Q000235:genetics / Q000378:metabolism*
D029721:Drosophila Proteins; D018398:Homeodomain Proteins; D019476:Insect Proteins; D012333:RNA, Messenger; D015534:Trans-Activators; C056478:bcd protein, Drosophila