Developmental Biology: Key Terms and Glossary

Floral organs are combinations of transcription-factor classes: A with E for sepals, A, B, and E for petals, B, C, and E for stamens, C with E for carpels, and C, D, and E for ovules inside the carpel. E is required in every whorl, ovules are not a fifth surface whorl, and A is a less tidy molecular class than B or C.

Exocytosis of the sperm acrosome on meeting the right egg coat, which exposes the binding and penetrating machinery used to cross that coat.

The apical ectodermal ridge, a distal ectodermal rim whose FGFs keep the limb mesenchyme proliferating. It maintains outgrowth and does not assign a separate identity to shoulder, forearm, and hand.

Extraembryonic tissue that moves to the future anterior side of the mammalian epiblast and secretes antagonists so Nodal, and therefore the primitive streak, is confined posteriorly.

Differentiation according to a cytoplasmic determinant the cell already contains, which still occurs when neighbours are removed.

The anterior homeodomain protein translated from maternal *bicoid* mRNA in the *Drosophila* syncytium, activating anterior gap genes and blocking translation of *caudal* where its concentration is high.

The sea-urchin sperm protein, displayed after the acrosome reaction, that binds the egg vitelline envelope in a species-specific way.

The proliferative mound that forms under the wound epidermis of a regenerating salamander limb. Its cells are lineage-restricted progenitors, not a return to the pluripotent state of the inner cell mass.

The mammalian embryonic stage in which trophoblast encloses a blastocoel and an inner cell mass, so extraembryonic and embryonic lineages are already distinct.

A hollow ball or sheet of cells whose cavity is the blastocoel, before the extraembryonic split that makes a mammal a blastocyst rather than a simple blastula.

The cytoplasmic IκB-like protein that holds Dorsal out of nuclei until ventral Toll signalling marks it for destruction.

The change mammalian sperm must undergo in the female tract before they can complete the acrosome reaction and fertilise.

Protein made from ubiquitous maternal mRNA only where Bicoid is low, so it accumulates as a posterior gradient.

Enclosure of the syncytial nuclei by membranes at cycle 14, after which the fly can no longer use freely mixing transcription factors as morphogens.

An organiser-secreted antagonist that binds BMPs and thereby protects dorsal mesoderm and neural ectoderm from ventral and epidermal fates.

The peptide from *CLAVATA3*, released by shoot apical stem cells, that represses *WUSCHEL* through CLAVATA receptors and so stops the stem-cell pool from expanding without limit.

The somitogenesis model in which a Notch oscillator ticks in tissue that has just left a posterior FGF and Wnt gradient, cutting one somite per cycle.

Recruitment of an existing toolkit gene to a new place by a new regulatory link, without requiring the two structures to be one organ inherited unchanged.

Correspondence between the order of Hox genes on the chromosome and the order of their expression along the axis, with 3′ genes acting more anteriorly.

A gap in iris, retina, or optic nerve left when the ventral choroid fissure of the optic cup fails to close.

Restriction of developmental path, labile when a tissue is only specified and stable when it is determined.

E-cadherin-dependent flattening of mammalian blastomeres, around the eight-cell stage, that begins the distinction between inner cells and trophoblast.

The temporary ability to answer a signal, set by receptors, transduction, and chromatin, and lost as the tissue ages even if the signal is unchanged.

A fate decided by interactions with neighbours, so that an isolated early blastomere need not produce only the fragment it would have made in place.

Narrowing and lengthening of a tissue by mediolateral cell intercalation, which elongates the frog axis under non-canonical Wnt.

Permanent block to polyspermy in which cortical granules release their contents, altering the egg coat and, in mammals, the egg membrane.

The microtubule-dependent shift of the egg cortex after sperm entry that carries dorsal determinants to the future dorsal side and allows a Nieuwkoop centre to form.

The activity that holds the ovulated egg in metaphase II until the calcium rise at fertilisation lifts the arrest and meiosis can finish.

The *Drosophila* BMP, encoded by *dpp* and expressed where nuclear Dorsal is absent, that specifies dorsal ectoderm.

A shared developmental circuit beneath structures that are not necessarily the same organ, as when *Distal-less* marks many kinds of distal outgrowth.

The account that competent ectoderm becomes neural when BMP signalling is low, not when every signal is missing. FGF helps to bring BMP signalling down and is part of reaching that state.

The dorsal, still epithelial part of the somite, maintained by Wnt, which produces skeletal muscle and the dermis of the back.

Commitment stable enough that a graft into a new embryonic site still follows the original fate.

The prolonged stop of the mammalian oocyte in diplotene of prophase I, from before birth until ovulation.

Overt structural and functional specialisation of a cell, which carries out a gene-expression choice and is not the same step as committing to that fate.

The regeneration rule that a blastema replaces only structures distal to the cut, so a wrist-level blastema makes a hand and not a shoulder.

An NF-κB-family protein present throughout the syncytial embryo that enters nuclei only on the ventral side, where high levels specify mesoderm. The gene is named for the dorsalised loss-of-function phenotype, which is the opposite of where the active protein works.

Spreading of the animal cap over the surface of the frog gastrula by division and intercalation.

Regeneration that depends on a local bud of proliferation, as in the salamander limb, rather than mainly on repatterning tissue already present.

A single median domain of the anterior neural plate, where Wnt signalling is low enough for forebrain, which midline Sonic hedgehog then splits into two optic primordia.

The brief membrane depolarisation, used by sea urchins and frogs but not by mammals, that stops extra sperm fusing until the cortical reaction makes a lasting block.

A record of what each region becomes if development is left undisturbed, which does not test whether that future is already fixed.

The receptor tyrosine kinase for fibroblast growth factor, read in this course mainly through the Ras–MAPK cascade.

The mammalian wound response that lays down a collagen scar and so fails to rebuild a patterned limb in the way a salamander blastema does.

A tetramer of MADS-box proteins, always including an E-class partner, that binds paired DNA sites and specifies one floral organ type.

An organiser antagonist that binds activin tightly and also BMPs, adding to the anti-BMP activity that permits dorsal fates.

Wolpert's picture of one morphogen source whose high, middle, and low concentrations are read as three different instructions.

The seven-pass receptor for Wnt, which with LRP5/6 inhibits the destruction complex and lets β-catenin reach the nucleus.

A zygotic gene expressed in a broad domain that reads the maternal gradients, so that losing it deletes a contiguous block of segments.

The mesenchymal signal, glial-cell-line-derived neurotrophic factor, that attracts and helps to multiply vagal neural crest as it colonises the gut.

The rule that differentiated cells of one individual still hold the same genes, so cell identity is a regulatory state rather than loss of DNA. Real exceptions, such as lymphocyte receptor rearrangement and enucleation of mammalian red cells, are not how a muscle or a neuron is made.

Localised egg cytoplasm that assigns a nucleus entering it to the primordial germ cells, as in *Drosophila* and *Xenopus*.

The transcription-factor family at the end of Hedgehog signalling, activating targets where the ligand is high and, chiefly as Gli3, repressing them where it is absent.

A BMP antagonist induced next to the Sonic hedgehog source so the apical ridge stays active, and whose persistence between digits is why a webbed foot does not separate.

Increase in size by cell proliferation, cell enlargement, or deposition of matrix. Cleavage is not growth, because it only partitions the egg's existing volume.

The organiser at the anterior end of the avian primitive streak, which lays down notochord as it regresses and can induce a second axis if grafted.

An evolutionary change in the timing or rate of a developmental event, as when the axolotl reaches sexual maturity without finishing metamorphosis.

An evolutionary change in the amount of a signal, of the sort that links finch beak depth and width to how much BMP4 the beak primordium expresses. That dose is a real contribution, not a complete explanation of every beak.

An evolutionary change in where a developmental event occurs, as when a familiar wing-margin cassette is redeployed to make a butterfly eyespot.

A change in the kind of molecule rather than only in where it is expressed, illustrated by the insect Ultrabithorax protein gaining repression of *Distal-less*.

Absence of enteric neurons from a distal stretch of bowel because vagal neural crest stopped short, so that segment cannot produce coordinated peristalsis.

Cleavage that divides the entire egg, which is possible when yolk is scarce or only moderately concentrated at the vegetal pole.

A homeodomain selector that gives an existing segment or region its identity, in chromosomal order, without changing how many segments form.

The gap protein set in an anterior gradient because Bicoid turns on zygotic *hunchback* and Nanos stops translation of the maternal message in the posterior.

The uppermost cell of the suspensor, which is recruited into the *Arabidopsis* embryo as the founder of the quiescent centre and the columella.

An interaction in which the signal chooses the fate, rather than merely allowing a fate the tissue has already selected.

BMP-driven death of the mesenchyme between specified digit rays, which frees the digits unless an antagonist such as Gremlin is left in place.

A hydra stem cell, distinct from the epithelial stem cells, that produces neurons, nematocytes, secretory cells, and gametes.

The rolling of marginal-zone cells over the blastopore lip and along the roof of the blastocoel during frog gastrulation.

The sperm-surface protein that must pair with Juno on the egg if the two plasma membranes are to fuse.

The egg-surface partner of Izumo1, which is shed after fertilisation and thereby removes a fusion ligand from the membrane.

Contact-dependent signalling in which the ligand is tethered in the sending membrane, the arrangement used by Notch.

A Notch interaction in which a cell slightly ahead forces its neighbours to abandon the same fate, spacing structures such as bristles without a long-range gradient.

A Nodal antagonist that travels further than Nodal, limiting how far the left-sided domain spreads and, at the midline, blocking a cross to the right.

The transcription factor encoded by *Lmx1b*, induced by Wnt7a in dorsal limb mesenchyme and required for dorsal structures such as nails.

The DNA-binding family to which most floral organ-identity proteins belong. APETALA2, an A-class protein, is the exception and is not a MADS-box factor.

Messenger RNA loaded into the egg, often at a particular pole, so the embryo can be patterned before it transcribes its own genome.

A gene transcribed in the mother during oogenesis, so that the embryo's phenotype follows the mother's genotype rather than alleles the embryo itself carries.

A plant stem-cell population, at the shoot and root tips and in lateral sites, that keeps adding organs after embryogenesis.

Cleavage that fails to cut through dense yolk, either as a disc on top of the yolk or, in insects, as nuclei dividing in a shared cytoplasm.

The transcription factor from *Mesp2* whose stripe, stabilised by one tick of the segmentation clock in competent presomitic mesoderm, initiates a somite boundary.

In *Xenopus*, the lengthening of the cell cycle, the onset of substantial zygotic transcription, and the start of motility after about twelve rapid cleavages. The embryo times the change by the ratio of nuclei to cytoplasm, and mammals activate the zygotic genome much earlier.

A cis-regulatory element that drives only part of a gene's pattern, such as one stripe of *even-skipped*, so that changing it need not alter the protein or the other stripes.

Regeneration that mainly reassigns fates in tissue already present, as in hydra, with less reliance on a local mound of new proliferation.

A signal released from a local source that specifies more than one fate by its concentration, with at least two of those responses direct rather than a relay through a second signal.

Shaping of tissues and organs by organised cell behaviour, as distinct from the patterning that decides which cells should move, fold, or die.

A historical description of embryos whose isolated early blastomeres make only their normal part. It is an experimental emphasis, not a proof that later induction is absent.

A basic helix-loop-helix protein that can start skeletal myogenesis in competent non-muscle cells. In the embryo it shares specification with *Myf5*, and neither it nor the rest of the family specifies cardiac or smooth muscle.

The myogenic regulator required for skeletal myoblasts to carry out differentiation, rather than for the initial decision to become a myoblast.

The posterior protein that, with Pumilio, blocks translation of maternal *hunchback*, which is required both for the abdomen and for the pole cells.

A proliferative cell of the planarian parenchyma. Some clonogenic neoblasts can rebuild an animal, but many are already lineage-biased, and muscle, not the neoblast, stores the positional code.

Border cells between neural plate and epidermis that leave by an epithelial-to-mesenchymal transition and form ganglia, melanocytes, and much of the facial skeleton, remaining ectoderm rather than mesoderm.

The neuroepithelium formed by folding the neural plate, or caudally by cavitation of a solid cord, which becomes the central nervous system and the retinal neuroepithelium.

An opening that remains while the neural tube closes from several starting points. The anterior and posterior neuropores close last, and failure there leaves the brain or the spinal cord open.

The Notch intracellular domain freed by γ-secretase, which enters the nucleus, binds CSL, and turns on targets such as the Hes genes.

The local cells, matrix, and signals that keep a stem cell from differentiating until one of its daughters leaves.

Dorsal vegetal cells in which maternal VegT overlaps stabilised β-catenin. They induce the organiser in the marginal zone above them and do not themselves become that organiser.

Leftward movement of fluid across the mouse node, driven by posteriorly tilted motile cilia, which frees Nodal signalling on the left first. Immotile cilia randomise laterality rather than imposing a mirror-image programme, and the chick reaches the same left-sided readout by a different upstream route.

A TGF-β-family inducer from vegetal cells, such as the *Xenopus* Xnrs, that specifies mesoderm, with the higher dorsal level specifying organiser mesoderm.

A secreted organiser protein that binds BMPs and, with chordin and follistatin, allows neural ectoderm and dorsal mesoderm where the antagonists prevail.

The double-layered structure formed when the optic vesicle folds, with neural retina on the inner layer and pigment epithelium on the outer.

The dorsal lip of the amphibian blastopore, shown by the Spemann–Mangold graft to induce host tissue into a coherent second axis rather than merely differentiating on its own.

Retention of juvenile features in a sexually mature descendant, as in the axolotl, which keeps larval gills because metamorphosis is not run on the ancestral schedule.

A gene expressed in seven stripes under the control of gap proteins, whose loss removes about every other segment.

Signalling by a secreted molecule to nearby cells. A morphogen is paracrine even when matrix or cell projections help it travel.

The repeating unit drawn by segment-polarity genes, offset from the visible segment so that it joins the posterior part of one segment to the anterior part of the next.

The multi-pass receptor that binds Hedgehog and, in the absence of ligand, keeps Smoothened from activating Gli.

The paired-box gene *Pax6*, required for the eye in both *Drosophila* and the mouse, and able to start an ectopic eye only in tissue that is still competent to run the retinal network.

A signal that allows a programme the tissue has already specified to continue, such as survival or outgrowth, without choosing among alternative fates.

A polar auxin-efflux carrier. Its placement orients the seedling axis and spaces new primordia; perception of auxin is left to plant physiology.

The transcription factor from *Pitx2* that remains on the left after Nodal and Lefty have faded, and that heart looping, lung lobation, and gut rotation read. It is not *Pitx1*, which is used in the pelvis.

An ectodermal thickening lateral to the neural crest, neither crest nor neural tube, from which structures such as the lens and the otic vesicle arise.

The phospholipase C delivered by the mammalian sperm, which generates IP3 and the repeated calcium rises needed to activate the egg.

The use of one gene in many times and places, which makes a change in the protein costly because every context is affected.

Auxin-induced transcription factors, products of the *PLETHORA* genes, graded from high at the root tip, where they maintain stem cells, to low levels that permit differentiation.

Able to produce all three germ layers of the body, as the inner cell mass can, but not the trophoblast.

The range of differentiated types a cell can still generate, from the totipotent zygote down to a stem cell that makes only one type.

The posterior midline structure of the chick or mouse epiblast through which cells ingress to form definitive endoderm and mesoderm.

A specified cell that divides a limited number of times while an organ is built, without the lasting self-renewal that defines a stem cell.

The 1973 proposal that proximal–distal limb identity equals time spent proliferating under the apical ridge. Fate maps later showed those levels are already separated in the early bud, and that removing the ridge loses distal tissue which had been specified and then could not be maintained.

A haploid gamete nucleus inside the fertilised egg. In mammals the two pronuclei replicate while still separate and first share a spindle at mitosis, rather than fusing into one interphase nucleus.

The small group of slowly dividing cells in the root tip whose contact keeps the surrounding initials from differentiating.

Holoblastic cleavage in which planes alternate at right angles to the animal–vegetal axis and the blastomeres remain in columns.

A historical description of embryos that can replace a missing part and still make a whole, smaller body. Localised determinants can still be present.

The receptor tyrosine kinase encoded by *RET* on enteric neural-crest cells, which reads GDNF with GFRα1 as a co-receptor.

The outer wall of the optic cup, marked by Mitf, which forms opposite the neural retina and is kept distinct from it by mutual antagonism.

Mammalian cleavage in which the first division is meridional and the second is meridional in one blastomere and equatorial in the other.

The transcription factor from *SCARECROW* that, together with SHORTROOT held in the nucleus, specifies endodermis and the division that separates it from cortex.

The ventral somite compartment, specified by Sonic hedgehog from the notochord and floor plate, which builds vertebrae and ribs.

A gene expressed in a stripe in every parasegment after cellularisation, locking anterior–posterior polarity inside each segment by short-range secreted signals.

A chain in which one tissue induces the next. The optic vesicle is required for the lens, but it is not the first instructor: head ectoderm already carries a lens-forming bias.

The *Drosophila* chordin homologue, encoded by *sog* and made in lateral ectoderm, which antagonises Decapentaplegic and protects the neuroectoderm.

A transcription factor from *SHORTROOT*, transcribed in the stele, whose protein moves outward one cell layer and, with SCARECROW, specifies endodermis.

The transcription factor phosphorylated by TGF-β-family receptors. The BMP branch uses Smad1, Smad5, or Smad8, and the Nodal branch uses Smad2 or Smad3, each with Smad4.

The transducer that becomes active once Hedgehog has bound Patched, allowing Gli to switch from repressor towards activator.

A repressor turned on by high nuclear Dorsal that stops the mesoderm from expressing genes such as *dpp* and *sog*.

The secreted Hedgehog ligand of the zone of polarising activity, and of the midline that splits the eye field. It is a signal read by concentration and by time, not a protocol.

The state in which an explant in neutral culture still follows its fate-map fate, although a new site in an embryo may yet respecify it.

Holoblastic cleavage on oblique planes, typical of molluscs and annelids, usually with autonomous specification of the D lineage and a maternal control of its handedness.

The file of cells produced by the basal daughter of the plant zygote, which anchors the embryo and bears the hypophysis at its embryo-facing end.

The early *Drosophila* stage in which cortical nuclei share one cytoplasm, so maternal protein gradients can pattern many nuclei without crossing membranes.

A concentration at which a morphogen response switches, made sharper by the affinity of enhancers, by repression between neighbouring fates, and by feedback on the ligand.

The receptor activated on the ventral side by cleaved Spätzle, which sends Dorsal into nuclei. Loss of Toll dorsalises the embryo.

The shared set of animal signalling pathways and transcription-factor families. Conservation of those parts is not conservation of a body plan.

A receptor tyrosine kinase activated only at the egg poles, which specifies the unsegmented termini through terminal gap genes rather than through the Bicoid gradient.

A basic helix-loop-helix activator induced by high nuclear Dorsal that drives the ventral mesoderm programme.

The T-box transcription factor encoded by maternal *VegT* mRNA at the vegetal pole, required both to specify endoderm and to produce the signals that induce mesoderm.

The Wnt ligand encoded by *Wnt7a*, secreted by dorsal limb ectoderm, which induces *Lmx1b* in the underlying mesenchyme and also helps to maintain Sonic hedgehog.

The homeobox gene *WOX5* of the root quiescent centre, which keeps columella stem cells dividing. It is a root counterpart of *WUSCHEL* and can largely replace it if the two are swapped.

The homeobox gene *WUSCHEL* of the shoot organising centre, whose product keeps overlying stem cells undifferentiated and which those cells repress by secreting CLAVATA3.

The mammalian cortical-granule response in which cleavage of ZP2 destroys sperm-binding sites and the zona hardens.

The zone of polarising activity, posterior limb mesenchyme whose Sonic hedgehog signal duplicates the digit pattern in mirror image when grafted to the anterior margin.

A transcriptional co-activator that builds up in dorsal nuclei after cortical rotation, and that canonical Wnt signalling stabilises so it can activate targets with TCF. Early dorsal accumulation is not the later gastrula Wnt signal, which posteriorises rather than dorsalises.