Summary
The ability to specifically delete the store of maternal α-subtype histone mRNAs stored in the egg pronucleus has allowed us to examine the role of this major fraction of the maternal mRNA in the early development of the sea urchinStrongylocentrotus purpuratus. The egg nucleus was removed by centrifugation, and the resulting enucleate half eggs were fertilized. These haploid andromerogones lacked any stored α-subtype histone mRNAs. However, when grown in parallel with control embryos, they showed identical cleavage cycles, cell numbers, and patterns of cell differentiation. Measurements of the amount of α-histone mRNA in these andromerogones showed that there was no premature synthesis of α-histone mRNAs to compensate for the deleted maternal pool. Instead embryonic synthesis was normal in timing of initiation and duration. the ability of these embryos to develop into highly differentiated larvae without their maternal α-subtype histone mRNA pool suggests that this pool is not a critical component of early development per se. This suggestion is strengthened by the observation that the primitive sea urchinEucidaris tribuloides naturally lacks this maternal histone mRNA store. Evolutionary implications are discussed.
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Angerer LM, DeLeon DV, Angerer RG, Showman RM, Wells DE, Raff RA (1984) Delayed accumulation of maternal histone during sea urchin oogenesis. Dev Biol 101:477–48.
Arceci RJ, Gross PR (1980) Histone variants and chromatin structure during sea urchin development. Dev Biol 80:186–209
Cohen LH, Newrock KM, Zweidler A (1975) Stage specific switches in histone synthesis during embryogenesis of the sea urchin. Science 190:994–997
Cognetti G, Shaw BR (1981) Structural differences in the chromatin from compartmentalized cells of the sea urchin embryo: differential nuclease accessibility of micromere chromatin. Nucleic Acids Res 9:5609–5621
DeLeon DV, Cox KH, Angerer LM, Angerer RC (1983) Most early variant histone mRNA is contained in pronuclei of sea urchin eggs. Dev Biol 100:197–207
Easton DP, Whiteley AH (1979) The relative contributions of newly synthesized and stored messages of H1 histone synthesis in interspecies hybrid echinoid embryos. Differentiation 12:127–133
Harvey EB (1932) The development of half and quarter eggs of Arbacia punctulata and of strongly centrifuged whole eggs. Biol Bull 62:155–167
Harvey EB (1956) The American Arbacia and Other Sea Urchins. Princeton University Press, Princeton, NJ
Herlands L, Allfrey VC, Poccia D (1982) Translational regulation of histone synthesis in the sea urchin,Strongylocentrotus purpuratus. J Cell Biol 94:219–223
Mauron A, Kedes LH, Hough-Evans B, Davidson EH (1982) Accumulation of individual histone mRNAs during embryogenesis of the sea urchinStrongylocentrotus purpuratus. Dev Biol 94:425–434
Maxson Jr, RE, Wilt FH (1982) Accumulation of the early histone messenger RNAs during the development ofS. purpuratus. Dev Biol 94:435–440
Newrock KM, Alfageme CR, Nardi RV, Cohen LH (1977) Histone changes during chromatin remodeling in embryogenesis. Cold Spring Harbor Symp Quant Biol 42:421–431
Poccia D, Salik J, Krystal G (1981) Transitions in histone variants of the male pronucleus following fertilization and evidence for a maternal store of cleavage-stage histones in the sea urchin egg. Dev Biol 82:287–296
Raff RA, Anstrom JA, Huffman CT, Leaf DS, Loo T-H, Showman RM, Wells DE (1984) Origin of a gene regulatory mechanism in the evolution of echinoderms. Nature (Lond) 310:312–314
Salik J, Herlands L, Hoffmann HP, Poccia D (1981) Electrophoretic analysis of the stored histone pool in unfertilized sea urchin eggs: Quantification and identification by antibody binding. J Cell Biol 90:385–395
Schroeder TE (1981) Development of a “primative” sea urchin (Eucidaris tribuloides): Irregularities in the hyaline layer, micromeres, and primary mesenchyme. Biol Bull 161:141–151
Senger DR, Arceci RJ, Gross PR (1978) Histones of sea urchin embryos. Dev Biol 65:416–425
Shaw BR, Cognetti G, Sholes WM, Richards RG (1981) Shift in nucleosome populations during embryogenesis: Microheterogeneity in nucleosomes during development of the sea urchin embryos. Biochemistry 20:4971–4978
Showman RM, Wells DE, Anstrom J, Hursh DA, Raff RA (1982) Message-specific sequestration of maternal histone mRNA in the sea urchin egg. Proc Natl Acad Sci (USA) 79:5944–5947
Showman RM, Wells DE, Anstrom JA, Hursh DA, Leaf DS, Raff RA (1984) Subcellular localization of maternal histone mRNAs and the control of histone synthesis in the sea urchin embryo. In: Malacinski GM, Klein WH (eds) Molecular aspects of early development. Plenum Press, New York, pp 109–130
Simpson RT (1981) Moculation of nucleosome structure by histone subtypes in sea urchin embryos. Proc Natl Acad Sci (USA) 78:6803–6807
Smith AB (1981) Implications of lantern morphology for the phylogeny of post-Paleozoic echinoids. Palaeontology 24:779–801
Wells DE, Bruskin AM, O’Brachta DA, Raff RA (1982) Prevalent RNA sequences of mitochondrial origin in sea urchin embryos. Dev Biol 92:557–562
Wells DE, Showman RM, Klein WH, Raff RA (1981a) Delayed recruitment of maternal mRNA in sea urchin embryos. Nature 292:477–478
Wells DE, Showman RM, Klein WH, Raff RA (1981b) Translational regulation in sea urchin embryos. Biol Bull 161:322
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Wells, D.E., Anstrom, J.A., Raff, R.A. et al. Maternal stores of α subtype histone mRNAs are not required for normal early development of sea urchin embryos. Roux’s Arch Dev Biol 195, 252–258 (1986). https://doi.org/10.1007/BF02438958
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DOI: https://doi.org/10.1007/BF02438958