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101 on: How we understand polyspermy functions and defenses after E.E. Just's 1919 study

2020; Wiley; Volume: 87; Issue: 3 Linguagem: Inglês

10.1002/mrd.23326

1098-2795

Harvey M. Florman,

Seed Germination and Physiology

January 1919 was a busy month. Hostilities of World War I ended in November 1918 but a state of war persisted. On January 8, 1919, Woodrow Wilson enumerated the postwar aims of the United States in his 14 points and this was followed later in the month by the opening of the Paris Peace Conference. Despite this, widespread chaos continued. Consider Europe, there were bloody street battles in Berlin and elsewhere in Germany from January 5 to 12, 1919 between Spartacist militias on one side and Freikorps and government units on the other. Attempted coups were mounted in the Balkans and Poland. In Ireland, the First Dail issued a “Message to the Free Nations of the World” on January 21, 1919, in which independence was declared from Great Britian, and fighting began the same day with the Soloheadbeg Ambush. Glasgow saw the Battle of George Square between striking labor groups on one side against police and military units on January 31, 1919. Ongoing conflicts included the Baltic wars of independence from Russia, as well as the Russian civil war between White and Red forces. And It was not only Europe: there was, for example, the Semana Tragica (January 7–14, 1919) in Argentina, with fighting between Anarchist and Communist forces on one side against federalist police. For cell and developmental biologists that January of 1919 was also notable for the monthly issue of The Biological Bulletin. It included three articles by Ernest Everett Just which considered various aspects of fertilization in Echinarachnius parma, the common sand dollar. The first of those reported details of the egg's cortical response to insemination, including a dissection of the functional consequences of this reaction (Just, 1919). That paper marks a conceptual turning point in our still-emerging understanding of how the egg limits sperm entry. Why this was the case requires some background. Let us look further back another 40 years. The last several decades of the 19th century were a critical period for cell and developmental biology. New methods of fixation and staining of tissues were developed and disseminated; some of these approaches were particularly well known, such as the Golgi “black reaction” (Peters, 2007), but in fact, a large number of techniques first became available to the general community (Lee, 1885). In addition, advances in optics and glass chemistry—notably from Jena (then in the Duchy of Saxe-Weimar-Eisenach and today in the Federal State of Thuringia in Germany) by the commercial collaboration of Carl Zeiss, Otto Schott, and Ernst Abbe—lead to the development of immersion apochromatic lenses of high numerical aperture and of advanced condensers. The result was a light microscope of then-unparalleled resolution and clarity. These technological developments contributed to an era of conceptual advances in histology and cytology. It was at this time that two students of Ernst Haeckel-Oscar Hertwig and Hermann Fol—are generally credited with independently discovering the fertilization of animal eggs by sperm, although this history may be more complex than is often presented (Briggs & Wessel, 2006). Both observed the fusion of echinoderm pronuclei although Fol went further and actually described sperm entry into eggs (Fol, 1877, 1879; Hertwig, 1877). In addition, he first articulated the difference between physiological and pathological polyspermy; in taxa of the former group normal development occurs in the presence of multiple sperm-derived pronuclei with the egg cytoplasm, while in the latter group multiple sperm pronuclei result in a halting of development. This distinction provided a valuable tool for the analysis of cellular processes: for example, studies with polyspermic eggs provided Boveri with essential data leading to the development of the chromosome theory of inheritance (Baltzer, 1964; Laubichler & Davidson, 2008; Opitz, 2016; Wilson, 1925). Finally, Fol described the elevation of the fertilization envelope in detail and, importantly, concluded that this provided a cellular mechanism for the block to polyspermy (Fol, 1877, 1879). Experimental proof for a link between the expansion of the fertilization envelope and the block to polyspermy was soon provided by the pharmacological experiments of Oscar and Richard Hertwig (Hertwig & Hertwig, 1887). The role of the fertilization envelope in the prevention of polyspermic fertilization was widely (Heilbrunn, 1913; Lillie, 1919; Wilson, 1925), though not universally (Loeb, 1915a, 1915b), accepted. It is here that Just enters the story. His insight, based on careful experimental design and meticulous animal maintenance, was that the elevation of the fertilization envelope was too slow to account for the block to polyspermy (Just, 1919; as noted by a sharp-eyed reviewer of this essay, Just suggests in a footnote on page 7 of that 1919 report that Oskar Hertwig may have anticipated a role for the egg cortex in the block to polyspermy as early as 1878.) From here we trace the distinction between the cell surface and egg coat blocks to polyspermy. This also provided an experimental approach that permitted examination of underlying mechanisms. The cell surface block, which is often termed the “fast block,” was studied extensively in the following decades (Clark, 1936; Gray, 1922; Rothschild, 1954; Rothschild & Swann, 1952; Tyler, 1948), culminating in Jaffe's landmark demonstration of the role of egg membrane potential in the control of egg fertilizability (Jaffe, 1976; Nuccitelli & Grey, 1984). Yet, some taxa, including mammals, have egg surface blocks that are not mediated by membrane potential (Florman & Fissore, 2015; Jaffe, Sharp, & Wolf, 1983), and in those cases, a cellular mechanism is not yet understood. A slower block mediated by the egg coat was also the subject of intense interest in a range of taxa, including mammals (Austin & Braden, 1953a, 1953b), and subsequently shown to be based on biochemical modifications in the egg coat (Bleil, Beall, & Wassarman, 1981; Burkart, Xiong, Baibakov, Jimenez-Movilla, & Dean, 2012; Foerder & Shapiro, 1977; Wong & Wessel, 2006). What follows is a consideration of our understanding of polyspermy regulation today. Just's work provides a rationale for this thematic issue, as it definitively established a role for the egg cortex in the echinoderm block to polyspermy (Just, 1919). Yet this is not intended as a retrospective on Just. Byrnes does conside the role of Just in the history of biology, and readers interested in more details about this remarkable man and scientist are referred to other work by Byrnes (Byrnes, 2009; Byrnes & Newman, 2014), as well as available articles and monographs (Crow, 2008; Manning, 1985). Rather, our focus here is on the consequences of Just's report. Wozniak and Carlson discuss new information on the egg surface ion channels that drive the block to polyspermy, while the egg surface and egg coat blocks are reviewed by Evans and by Fahrenkamp et al., respectively. As discussed previously, Fol had noted that in some taxa polyspermy is compatible with development. This is explored in animals by Iwao et al. and in plants by Tekleyohans and Groβ-Hardt and by Toda and Okamoto. The author declares that there are no conflict of interests.