COMMENTARY Positional order and cellular handedness

A major problem in thinking about asymmetrical patterns in organisms is that of obtaining 'big hands from little hands' (Harrison, 1979). The big hands are our own, whereas the little hands are asymmetrical organic molecules. Since the molecules that make up our left and right hands are of identical asymmetry, the different handedness of these big hands must be specified at some more complex level of organization. For Harrison (1979) and, more recently, Brown and Wolpert (1990), the link between the levels is a tethered macromolecule or macromolecular aggregate, implying a pre-existing structural system within which the tethering takes place. Ciliates are a particularly favorable system for studying organismic handedness. These organisms are pervasively asymmetrical, avoiding the complications resulting from superimposition of asymmetries on a bilaterally symmetrical body plan (see Brown and Wolpert, 1990, and references cited therein). Ciliates are also unicellular, thus reducing the gap between the big and little hands. Among unicellular systems, ciliates have the unique advantage that a specific handedness can be perpetuated across cell generations, making it possible to study the two organizational enantiomorphs separately yet also to analyze the occasional transitions (both genie and nongenic) between them. What I attempt to show here is that reversible intracellular handedness is an emergent property, based neither on local molecular asymmetries nor on local information repositories but rather on more global spatial relations. These relations can be modelled successfully using field equations that suggest a system of interactions of at least two molecular species.