Cell Lineage and Determination of Cell Fate in Ascidian Embryos

Int..J.De\', BiuJ.33: 197-111(19S9) 197 Review Cell lineage and determination of cell fate in ascidian embryos JUDITH M. VENUTI and WilLIAM R. JEFFERY' Center for Developmental Biology, Department of Zoology, University of Texas, U.S.A. CONTENTS Introd ucti on 198 Cell Lineage 198 Early cell lineage studies 198 Refining the classic cell lineage 201 Revising the classic cell lineage 202 Muscle cell lineage 202 Endodermal cell lineage 203 Notochord cell lineage 203 Neural cell lineage 204 Epidermal cell lineage 204 Restriction of cell fate during embryogenesis 205 Determination of Cell Fate 205 Mosaic development 205 Auto nom 0 us deve I0 pme nt 206 Cyto pIas m ic dete rm inants 206 Inductive cell interactions 209 Brai n sensory cells 209 Muscle cells 209 Summary and Key Words 210 References 210 <-Address for reprints: Center for Developmental Biology, Department of Zoology, University of Texas, Austin, Texas 78712 U.S.A @ UBC Press. Leioa. Spain In .I.M. Vel/wi and \YR. Jeffay Introduction After a day or less of development, the larva hatches and begins locomotion. Depending on the species, the dura- The comparative development of different taxa and the tion of larval life varies from minutes to several days. When origin of the primary germ layers were major problems in the larva has dispersed and a suitable attachment site is embryology at the turn of the century. The principal tech- selected, it attaches to a substratum and undergoes meta- nique used to address these problems was direct observa- morphosis. During metamorphosis, the tail is retracted tion of developing embryos. Painstakingly, the early em- into the head, the differentiated tail muscle and notochord bryologists followed the history of embryonic cells, from cells are resorbed, and the larval anlagen differentiate into the uncleaved egg through the daughter cells of each clea- the tissues and organs of the sessile adult. Our knowledge vage, and sometimes as far as the rudiments of larval of ascidian cell lineage extends only to the larval stage; no tissues and organs. These observations led them to recog- cell lineage determinations have been attempted through nize that in some embryos particular cell types arose from metamorphosis. specific regions of the egg. These results were often ex- pressed as a fate map with the future tissues superimpo- Cell lineage sed on the surface of the egg or early embryo. The clonal origin and fate of each embryonic cell can also be expres- Early eel/lineage studies sed as a cell lineage. The term "cell lineage" was first used by Wilson (18921, who observed that the mesodermal Although Kowalevsky (1866; 18711 was the first to pro- derivatives of Nereis embryos could be traced back to a vide a detailed description of ascidian development, he single blastomere, the mesoblast. The observations of made no attempt to follow the fates ofthe embryon ic cells. Conklin (1905al on the pigmented eggs of Stye/a partita Shortly thereafter, however, van Beneden and Julin (1885; provided the first definitive ascidian cell lineage. This 1886) examined cleavage patterns in eggs of several asci- lineage was determined from direct observations of the dian species and determined the history of the embryonic fate of individual cells during embryogenesis. With the cells up to the 44-cell stage. Their description of the cell advent of modern cell tracing techniques, Conklin's cell lineage of Clavellina rissoana (van Beneden and Julin, lineage has been refined and extended. In this review, we 1886) revealed a clear understanding of the relationships discuss features ofthe classic cell lineage, recent revisions between early cleavage and symmetry of the embryo. to this cell lineage, qnd the possible mechanisms deter- Ascidians cleave bilaterally (Fig. 1) with the first and sec- mining cell fate in ascidian embryos. ond cleavages meridional (through the animal-vegetal axis) and the third cleavage equatorial, dividing the em- Ascidians are protochordates whose life cycle includes bryo into quarters of approximately equal sized cells. After motile larval and sessile adult stages. The larval stage is the 32-cell stage, the cleavage pattern becomes asynchro- called a tadpole because of its superficial resemblance to nous in different parts of the embryo. Gastrulation is an amphibian tadpole. A diagram of an ascidian tailbud- initiated between the 64- and 76-cell stage, and morphoge- stage embryo illustrating the organization of the tadpole netic movements of presumptive notochord and muscle larva (Katz, 19831 is shown in Figure 5A-B. The larva is cells bring about formation of the tail following neurula- divided into a head and a locomotory tail. The head con- tion. Cells formed during cleavage show a constant rela- tains a dorsal nervous system consisting of an anterior ti.onship to the animal-vegetal axis of the egg and the brain with two pigmented sensory cells (the ocellus and subsequent bilateral symmetry of the embryo. The future otolith), a brain stem, and a posterior spinal cord. The head dorsal region of the embryo is derived from the vegetal he- also contains undifferentiated anlagen of adult tissues in- misphere of the egg, while the future ventral region of the cluding the mesenchyme cells, putative precu rsors of adult embryo is derived from the animal hemisphere (Fig. 1C). mesodermal derivatives, and the endodermal cells, which give rise to the adult alimentary tract. The tail contains the By the turn of the century, ascidian development had caudal portion of the spinal cord, a central not-ochord, been studied extensively (Kowalevsky, 1866; van Oebeden lateral bands of muscle cells, and a ventral extension of the and Julin, 1885; 1886; Seeliger, 1885; Samassa, 18941. Ho- endoderm known as the endodermal strand. The entire wever, Castle (1896) noted that considerable differences of larva is surrounded by a layer of epidermal cells. opinion existed concerning the derivation of the primary Cell jilte ill I/s..it/il/II ('III"".""S 199 A C Ventral ~.. 0 ~~n u ~~0 ~"- Dorsal Fig. 1. Early development of the ascidian embryo showing cefllineage nomenclature. A. Two-cell embryo viewed from the posterior pole. B. Four. cell embryo viewed from the animal pole. C. Eight-cell embryo viewed from right side. D-E. Sixteen-cell embryo viewed from the animal (0) and vegetal (E) poles. F-G. Thirty-two.cell embryo viewed from the animal (F) and vegetal (G) poles. H.I. Sixty-four-cell embryo viewed from the animal (H) and vegetal (I) poles. In the 64-cell embryo only vegetal cells mentioned in the text are labe. led. The cells on the right side of the embryo (C-I) are not underlined in this diagram after the 4-cell stage. germ layers. Castle believed that this disagreement was Conklin (1905a) was fortunate to have selected the the result of errors sustained in orienting the embryo. He ascidian Styela partitafor his investigations. The eggs and examined cell fate in Ciona intestinalis em-bryos, but mis- early em bryos of this species contain pigmented cytoplas- takenly identified the vegetal pole region as the future mic regions which segregate into different blastomeres ventral side of the embryo and labeled the animal pole re- during cleavage so that the embryonic cells can be distin- gion as the dorsal side. His results. however. were in guished by color. Consequently, Conklin observed the de- agreement with those of Seeliger (1885) and Samassa velopmental history of the embryonic cells with unprece- (1894). whose orientations of the embryo were also inver- dented clarity and constructed a detailed cell lineage up to ted. These inversions can be attributed to the lack of visible the 64-cell stage. His observations also led to a theory of markers in most ascidian embryos and a shape change that embryonic determination in which specific "organ.form- occurs in animal and vegetal hemisphere cells between the ing" substances localized in the egg were proposed to 32- and 76-cell stage. At the 32-cell stage, animal pole cells direct the differentiation of laval tissues after their segre- are columnar, but by the 76-cell stage they flatten. and the gation into the early blastomeres. vegetal pole cells become columnar (Conklin, 1905a). These cell shape changes were docu-mented correctly by The nomenclature for ascidian cell lineages devised by van Beneden and Julin, but escaped Castle, who assumed Conklin (1905al is still used by modern embryologists. Two that van Beneden and Julin had inverted the embryo. letters are required for the entire cell lineage, A for the 200 J.M. \'1'11111;and \\'R. Jeff;'ry member of the fourth generation (Fig. 1CI. A B c It is easiest to understand ascidian cell lineage nomenclature if one refers to different stages of the early embryo (Fig. 1). The two blastomeres that arise from the first M Ch cleavage are designated AB2 and A82 because they repre- sent the second generation of cells (Fig. 1AI. The second cleavage divides the embryo into two third-generation M E 84.1 A4.1 anterior blastomeres, designated A3 and A3, and two third- generation posterior blastomeres, designated B3 and 83 (Fig. 1BI. The third cleavage divides the embryo into ani- Fig. 2. Schematic diagram of colored cytoplasmic regions ofStyela mal and vegetal quadrants, with fourth generation cells egg. A. One-cell embryo after completion of the first phase of designated as A4.1, B4.1, a4.2, b4.2 on the left side and ooplasmic segregation. B. One-ceJl embryo after completion of the second phase of ooplasmic segregation. C. Eighr-cell embryo show- A4.1, 84.1, a4.2 and b4.2 on the right side (Fig. lCI. Sub- ing the distribution of cytoplasmic regions between the 84.2, b4.2, sequently, the progeny of each division can be identified A4.

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