Genes controlling pattern formation in Drosophila embryogenesis

Maternal Anteroposterior Axis

Gene	Expression Pattern	Mutant Phenotype	Molecular Nature	Developmental Function
dicephalic (dic)	Maternal	Abnormal position of nurse cells relative to oocyte		Contributes to anteroposterior polarity of nurse cell oocyte complex
gurken (grk)	Oocyte	Eggs ventralized with dorsal appendages reduced or missing	Similar to vertebrate transforming growth factor alpha (TGF-α), ligand for torpedo	Establishes first posterior and then dorsal identity of ovarian follicle cells
spindle (spn) (several loci)	Maternal germ line	Disturbed anteroposterior polarity of oocyte		Determination of prospective oocyte among cystocytes
torpedo (trp)	Ovarian follicle cells	Similar to grk	Receptor tyrosine kinase, receptor for grk	Same as grk

Maternal Anterior Class

Gene	Expression Pattern	Mutant Phenotype	Molecular Nature	Developmental Function
bicoid (bcd)	mRNA transcribed in nurse cells and transported to anterior of oocyte. Translated during cleavage. Protein forms anteroposterior gradient.	Head and thorax replaced with mirror image of telson	Transcriptional regulator (homeodomain and paired repeat)	Activates hb transcription; acts as a morphogen on embryonic genes; expressed anteriorly
exuperantia (exu)	Testis and ovary	Reducion of head; defective gastrulation	RNA-binding protein	Needed to transport bcd mRNA from nurse cells to oocyte
hunchback (hb)	See Zygotic anteroposterior gap class
staufen (stau)	Maternal germ line, emryonic central nervous system	Most abdominal segments missing, no pole cells, also head defects	Double-stranded RNA-binding protein	Required for bicoid mRNA localization and polar granule assembly
swallow (swa)	Maternal germ line	Reduction of head; cellularization defects	Rna-binding protein	Required for localization of bcd mRNA

Maternal Posterior Class

Gene	Expression Pattern	Mutant Phenotype	Molecular Nature	Developmental Function
cappuccino (capu)	Maternal	Abdominal segments A2-A7 missing; no pole cells	Putative transmembrane receptor	Required for polar granule assembly
nanos	Transcription in oocyte and nurse cells. Partial localization to polar granules. Only this localized mRNA is translated.	Absence of abdomen; pole cells normal	RNA-binding protein, translational repressor	Inhibits translation of maternal hb mRNA and hastens its destruction, hence allows activation of kni in posterior.
oskar (osk)	Maternal germ line	Similar to capu		Required for polar granule assembly, localizes nos mRNA
pumilio (pum)	Transcription maternal. Protein probably localized to posterior	Most of abdomen missing; pole cells normal	RNA-binding protein	Recruits nos protein to hb mRNA
spire (spir)	Maternal	Similar to capu	Actin-binding protein	Required for polar granule assembly
staufen (stau)	See maternal anterior system
tudor (tud)	Male and female germ line	Similar to capu		Required for pole cell formation
vasa (vas)	Transcription in nurse cells and oocyte; mRNA uniform in early embryo. Protein localized in posterior of oocyte, egg, and in pole cells.	Similar to capu	RNA helicase	Required for pole cell formation

Maternal Terminal Class

Gene	Expression Pattern	Mutant Phenotype	Molecular Nature	Developmental Function
NTF-1			Transcriptional inhibitor	Inhibits transcription of hkb and tll
torso (tor)	Transcription in nurse cells. Transport to oocyte, where protein distributed uniformly in plasma membrane.	Absence of labrum, reduction of head skeleton, absence of A8 and telson; gain of function; suppression of segmentation in thorax and abdomen	Tyrosine kinase receptor, likely receptor for active trunk protein	Activates tll hkb by inhibiting NTF-1
torsolike (tsl)	Protein secreted by anterior and posterior ovarian follicle cells probably associates with vitelline envelope near egg poles	Similar to tolr (loss of function only)	Modifying protein	Generates active form of trunk near egg poles
Trunk (trk)	Maternal mRNA translated in early embryo, protein released into preivitelline space	Similar to tor	Secreted protein	Probably ligand of tor, after processing by tsl

Zygotic Anteroposterior Gap Class

Gene	Expression Pattern	Mutant Phenotype	Molecular Nature	Developmental Function
empty spiracles	Transcription during blastoderm 78-67% EL; later, in cells forming tracheal pits and spiracles	Defects in antennal segment, tracheal system	Transcriptional regulator (homeodomain)	Specifies procephalic segments
giant (gt)	Initial transcription at preblastoderm stage 82-60% and 33-0% EL; changes later	Defects in or absence of labrum, labium, and abdominal segments	Transcriptional regulator (Leucine zipper)	Activates Scr; represses Kr
huckebein (hkb)	Anterior and posterior ends of blastoderm	Defects in terminal body structures and gut	Transcriptional regulator (zinc finger domain)	Specifies terminal structures in concert with tll
hunchback (hb)	Maternal mRNA initially uniform; protein forms anteroposterior gradient. Embryonic transcription 100-50% EL and 20-10% EL. Posterior domain long-lasting.	Embryonic: deletion of labium, thorax, aA7/pA8 (PS 13). No pure maternal effect, but if mother and sperm are hb-, then deletion of all mouthparts and thoracic segments and A1-A3, with mirror duplication of abdomen.	Transcriptional regulator (zinc finger domain)	Represses kni; represses Kr at high level and activates at low level; regulates eve; regulates h, run, ftz; activates Antp (with ftz); represses Ubx
knirps (kni)	Transcription starts at preblastoderm stage forming zone 45-30% EL. Ventral patch and narrow ring form in atnerior by cellular blastoderm stage.	Replacement of A1-A7 by single A-type segment	Transcriptional regulator (zinc finguer)	Represses Kr; regulates h, run, eve, ftz; represses Abd-B and Antp
Krüppel (Kr)	Transcription starts at preblastoderm stage in central zone, eventually expanding to 60-30% EL. Later also posterior patch and patch in head.	Purely embryonic. Head normal, deletion of thorax and A1-A5. Duplicated inverted A6.	Trancriptional regulator (zinc finguer)	Activates kni; represses gt; regulates eve; regulates h, run, ftz; represses Scr; activates Antp; represses Abd-B
orthodenticle (otd)	Narrow band (75-92% EL) in anterior blastoderm	Defects in eyes and anterior head parts	Transcriptional regulator (homeodomain, paired domain)	Activated by bcd and tor, otd - along with ems - specifies procephalic segments
tailless (tll)	Transcription in termini of preblastoderm embryo	Head skeleton reduced but labrum present. Hindgut, Malpighian tubules absent.	Transcriptional regulator (steroid receptor family)	Activates hb; represses Kr; represses kni; activates h

Zygotic Pair-Rule Class

Gene	Expression Pattern	Mutant Phenotype	Molecular Nature	Developmental Function
even-skipped (eve)	Transcription starts at preblastoderm stage; 7 stripes corresponding to parasegments 1, 3, 5, etc., by cellularization stage. Fades during gastrulation.	Abolishes segmentation, giving lawn of denticles. Weak alleles delete odd parasegments.	Transcriptional regulator (homeodomain)	Represses ftz, odd, run; activates itself; activates en; represses wg; activates Dfd
fushi tarazu (ftz)	Transcription starts at preblastoderm stage; 7 stripes corresponding to parasegments 2, 4, 6, etc., by cellularization. Fades during germ band extension.	Deletes even parasegments	Transcriptional regulator (homeodomain)	Activates itself; activates en; activates Antp; activates Ubx; represses wg
hairy (h)	Transcription starts at preblastoderm stage; 7 stripes + dorsal head patch by time of cellularization. Fades during gastrulation.	Range from deletion of odd parasegments to formation of lawn of denticles. Also loss of labral tooth. Other alleles give extra hairs in adult.	Transcriptional regulator (helix-loop-helix domain)	Represses run, ftz; activates eve
paired (prd)	Transcription starts at preblastoderm stage; 8 stripes with dorsal head patch by cellularization. During germ band extension stripes 2-7 split and then fade.	Deletions about 1 segment wide starting in middle of denticle band affecting mainly odd abdominal segments	Transcriptional regulator (homeodomain)	Activates wg, en
runt (run)	Transcription starts at preblastoderm stage; 7 stripes. After cellularization, patter becomes single-segment stripes, which persist through germ band extension.	Deletions more than 1 segment wide centered on T2, A1, A3, A5, A7, with mirror duplication of what is left	Transcriptional regulator (novel)	Represses h, eve; activates ftz

Zygotic Segment Polarity Class

Gene	Expression Pattern	Mutant Phenotype	Molecular Nature	Developmental Function
engrailed (en)	Transcription starts at blastoderm stage and produces 14 narrow stripes by extended germ band stage, marking the anterior of each parasegment. Expression in posterior compartments of larval imaginal discs	Ventral cuticle a continuous lawn of denticles. Less severe alleles delete even-numbered parasegments	Transcriptional regulator (homeodomain)	Maintains hh and indirectly wg activity; selector gene defining posterior compartment
frizzled (fz)	Various imaginal discs	Variable orientation of wing hairs, irregular ommatidia in eye	Seven-pass transmembrane receptor	Receptor for wg
frizzled-2 (fz-2)	Apparently redundant with fz
hedgehog (hh)	Posterior compartments of larval segments and imaginal discs	Posterior compartment replaced with mirror image of anterior compartment