Anecdotal , Historical and Critical Commentaries on Genetics Edited by James F . Crow and William F . Dove Sonneborn and the Cytoplasm

IN the late 1930s when Tracy Sonneborn was in graduate school and just starting his work on the genetics of protozoa, classical studies on genetics were almost finished. The second edition of Principles of Genetics by E. W. Sinnott and L. C. Dunn (1932) that appeared in that period was quite sophisticated, containing a good account of chromosome theory, segregation ratios produced by complex gene interactions, chromosome and genetic maps, polyploidy, aneuploidy, multiple factor inheritance, sex determination, and evolution. The authors argued strongly that virtually all inheritance was ascribable to nuclear genes. Only Correns’s work on plastid inheritance was cited as an example of cytoplasmic inheritance, and it was pointed out that this should be considered only a minor exception to the general rule that chromosomal genes determine the hereditary characters of the organism. Other biologists, particularly cell physiologists such as L. V. Heilbrunn at the University of Pennsylvania, were not so sure. They thought that classical genetics dealt only with superficial characters and that the fundamental characters of organisms such as membrane permeability, metabolism, etc., were controlled by the cytoplasm. It is not clear what Sonneborn thought of this controversy, but from what I know about Sonneborn, he must, at least, have had an open mind about the matter. All classical genetics was based on multicellular organisms, in which characters were seen after a complex developmental process. Once Sonneborn had discovered mating types in the protozoa it became possible to carry out classical genetic studies with the protozoa and study their inheritance without an intervening period of somatic development. Perhaps the genetics of singlecell organisms, the protozoa, would prove to be a bit different from the classical picture. The inheritance of mating types: Sonneborn (1937) made mixtures of numerous isolations of different lines of Paramecium and found that certain lines mated with each other, but never with themselves. See Preer (1997) for a Perspectives on much of the work of Sonneborn. A careful look at the pattern ofmatings revealed that there were a number of different mating types, I mating with II, III mating with IV, etc. Each pair of mating types determined a different mating group or species as they are now called. After discovering mating types, the first character that Sonneborn investigated was mating type itself. His findings were summarized later (Sonneborn 1975). Early on he found a single segregating locus that controlled mating type, but its effect was layered over what he called caryonidal inheritance, a phenomenon clearly at odds with the classical picture of genetics. In caryonidal inheritance, mating type is fixed when the two macronuclei formed in each cell after autogamy or conjugation are each determined for one or the other of the two segregating mating types. These two independently determined nuclei are later segregated into clones that he called caryonides. Since cytological studies showed that the nuclei of these two caryonides are derived from one homozygous nucleus, an extraordinarily high mutation rate at a particular stage in the life cycle would be required to explain the results according to classical genetics. Surprisingly, Sonneborn found that while mating types in some species of the Paramecium aurelia group were inherited caryonidally, in other species mating type followed the cytoplasm of each mating partner. He even found that in one species mating type was controlled by a simple Mendelian factor. Simple Mendelism clearly was not the whole explanation. Life-cycle changes: A look at the life cycle turned up more deviations from Mendelism. It had been known for many years that, after conjugation, Paramecium undergoes a period of immaturity for a variable number of fissions when cells are unable to mate ( Jennings Author e-mail: [email protected]