Stochasticity in the symmetric division of plant cells: when the exceptions are the rule

Abstract

Long before most of the molecular aspects of cell division were uncovered, L. V. Heilbrunn remarked that: “it is easier to make a new theory of cell division than to test an old one” and promised his readers to limit his treatment of cell division to “the factual facts regarding the physical changes which take place during mitosis” (Heilbrunn, 1928). Heilbrunn's barb was directed, first and foremost, to the theories or empirical rules put forward to explain how cells select a plane of division. A perusal of the cell biology literature in the decades preceding Heilbrunn's comment suffices to appreciate the author's cynicism toward cell division theories. By the end of the nineteenth century, at least five different rules had been formulated to predict how cells select a division plane. Of these, the most widely cited rules for plant cells were the Rectangular Section formulated by Sachs (1878) and the Principle of Minimal Area promoted by Berthold (1886) although often attributed to Errera (1888). The presence of exceptions to these rules led to many more “improved” rules and fueled a heated debate that spilled well into the twentieth century.

An intriguing feature of this story is that despite the explosion of cell biology research in the twentieth century, the nineteenth century obsession with cell division rules rapidly receded; and ultimately vanished before the tests Heilbrunn so eagerly desired were performed. Although many biologists have cited this early work in reviews (e.g., Smith, 2001; Kwiatkowska, 2004; Dumais, 2007), the classical division rules have laid essentially dormant for a full century. The reasons why these rules were never tested must be sought in the particular mind-set of twentieth century biology. The most important factor is probably the geometrical nature of the rules which did not resonate well with the molecularly-oriented biology of the last century. Certainly, reducing cell division to a geometrical problem adds little to the “factual facts regarding the physical changes which take place during mitosis.” Yet, it is probable that even the most abstract division rule would not have been neglected for so long if it had predicted with great accuracy the selection of division planes in plant cells. Thus, another factor seems to have played an important role: the fact that even within the confine of a specific tissue, cell division seems to escape the determinism embodied by the classical rules. The frequent exceptions to the predicted division planes must have invalidated the division rules to the eye of most biologists. We recently argued that these exceptions may in fact be confirmation of another, more subtle, division rule (Besson and Dumais, 2011). Here we briefly retrace the history leading to this new rule while, at the same time, highlighting the strange turn of events that greatly delayed the acceptance of stochasticity in this particular area of cell biology.