Controlling Size in Multicellular Organs: Focus on the Leaf

Unsolved Mystery L eaf size depends on cell number and size. However, leaves are not simply the sum of cell size and number; rather, they are under the control of an unknown, organ-wide integration system. The existence of such a system is strongly suggested by two mysterious phenomena: compensation and high-ploidy syndrome. Compensation is characterized by cell enlargement triggered by a significant decrease in cellular proliferation, while plants with high-ploidy syndrome have more than eight sets of homologous chromosomes (8C), resulting in an increase in cell volume, but smaller leaves. Determining the mechanisms underlying these phenomena will provide important insight into the mechanism of multicellular organogenesis. In 1998, I noticed an unusual phenomenon in plants involving a decrease in the number of cells in the leaf lamina with a consequent increase in cell volume. I called this phenomenon " Hosho-sayou, " which is Japanese for " compensation " [1], because I considered the inverse relationship (a decrease in cell number with an increase in cell volume) to be the most important feature, although the effect on leaf area was often incomplete. At that time, a limited number of examples were available to support the existence of such a relationship; however, additional evidence continues to accumulate. In 2002, having become convinced of the generality of the relationship, I adopted the English word " compensation " [2]. Gerrit Beemster of Ghent University (Belgium) also named this phenomenon compensation the following year [3]. We have since found that compensation occurs specifically in leaves and related lateral organs with a determinate fate (i.e., those organs that are under strict control in terms of when organogenesis starts and finishes), and not in indeterminate organs such as roots [4]. This likely reflects the presence of an unknown integration system that oversees cell division and expansion in determinate organs [5]. The details of this system are, at present, entirely unknown. Understanding the mechanism of multicellular organogenesis, many aspects of which remain mysterious, is one of the major goals of modern biology. The mechanisms that integrate cellular proliferation with organ size in animals are also not yet understood [6,7]. As is widely known (even in Greek mythology), the size of the human liver is strictly controlled, and if most of the liver is surgically removed, it will regenerate to the proper size. Researchers have hypothesized a " total-mass checkpoint " mechanism(s) to explain this phenomenon [7], but, again, …