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Mitotic Domains Partition Fly Embryos, Reflecting Early Cell
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AMER. ZOOL., 29:617-652 (1989)
Mitoti
cDomain
sPartitio
n Fly Embryos,Reflectin
g Earl y Cel lBiologica
lConsequence
s o fDeterminatio
n in Progress 1VICTORI
A E. FOE
Friday Harbor Laboratories, University of Washington,Friday Harbor, Washington 98250
AN DGARRET
T M. ODELL
Department of Zoology, University of Washington,
Seattle, Washington 98195
SYNOPSIS
. We link classical observational developmental biology with modern techniquesand concepts o f cell biology, focusing on early development in the fruit fly, Drosophilamelanogaster. In contrast to the first thirteen synchronous nuclear division cycles followingfertilization
o f the egg, cell division in the fourteenth cycle partitions the embryo intomitotic domains. These are bilaterally symmetric clusters of cells, spatially and temporallypatterned, invariantly, embryo-to-embryo. Cells
i n a given mitotic domain share the samemitotic schedule, different from that in neighboring domains. In addition, cells in at leastsome mitotic domains share distinct attributes such
as special cell morphologies, spindleorientations, morphogenetic movement behaviors, and eventual differentiated tissue fates.We argue that
a mitotic domain differentiates its control of the fundamental cell cycleprocess a s a consequence of its having embarked on a developmental pathway differentfrom that of neighboring domains. In embryos of flies with certain mutations at early-acting genetic loci, perturbations
o f the normal pattern of mitotic domains forecast the final mutan t phenotypeMitoti
c domain s are visible by non-invasive light microscopicobservation o f live developing embryos, or by staining fixed embryos with fluorescentlylabeled antibodies t o microtubules - methods that will likely work well on embryos of phylogeneticall y divers e type . We document the methodological and phylogenetic gen- eralit y o f mitoti c domain s wit h micrograph s of Calliphora (blow-fly) embryos; the homologytoDrosophila is obvious. We present a theoretical framework for thinking about the processof embryonic cell determination
a s a gradual dynamical process and argue that, to learnmost about determination, w e should correlate the earliest perturbations we can inflictwith the earliest phenotypic consequences we can assess: perturbations of the mitoticdomain pattern serve this purpose perfectly.
INTRODUCTIO
N these groups of cells "mitotic domains"
I n thi s pape r w e tr y t o link classical because cells in a given group share the observationa l developmenta l biolog y wit h sam e mitoti c schedule differen t fro m tha tmodern techniques an d concepts of cell i n neighborin g groups Th e cell s in at least biology Afte r a general introduction, we som e mitoti c domain s shar e mor e tha n a wil l focu s almos t entirel y on the cell biol- common cell cycle length. They shareogy o f early development, including gas- attributes such as special cell morpholo- trulation i n Drosophila. We will concen- g ies > spindle orientations, morphogenetic trat e o n a recently discovered phenomenon movement behaviors, and eventual tissue tha t begin s jus t afte r th e mid-blastula tran- fates. sition i n which some mechanism finely Control of the cell cycle, and of mitosis,partitions th e blastula/gastrula into sepa- ar e amon g the most fundamental of cellrate groups o f embryonic cells. We call biological processes in all cells (see A. Mur-ray's [1989] essay i n this volume). We arguethat a mitotic domain differentiates its con-. trol o f this fundamental process as a con-' 1 Fro m the Symposium on Science as a Way of Know- c • i i_ i J J i ing-Cell and Molecular Biology presented at the Annual sequence of its having embarked on a devel-Meetin
g of the American Society of Zoologists, 27- opmental pathway different from that of 3 0Decembe
r 1988, at San Francisco, California. neighboring domains. That is, we believe, 61
7Downloaded from https://academic.oup.com/icb/article/29/2/617/117863 by guest on 20 October 2023
618V. E. FOE AND G. M. ODELL
differen t mitoti c domain s compris e cel lgroups on their way toward determinationas the primordia of different larval struc- tures , and the distinct characteristics sharedby cells in a mitotic domain reflect this. Th e fruit s o f geneti c mutan t screens,carried out by Niisslein-Volhard, Wie-schaus, Jiirgens, and their co-workers,seeking early-acting genes in
Drosophila, arenow available as an extensive menagerie ofmutant flies whose embryos exhibit devel-opmental defects, as assessed by examiningthe cuticle
2 secrete d b y larva e (Tearl e andNiisslein-Volhard, 1987). We include in thispaper preliminary evidence that, in at leastsome of these mutants, very early pertur-bations of the normal pattern of mitoticdomains forecast the perturbations of
cuti cl e patter n tha t th e larv a produce s mucquotesdbs_dbs44.pdfusesText_44