Hans Ris proposed in 1961 that chloroplasts might be highly derived endosymbiotic microorganisms, originally related to blue-green algae. Evidence from 1966 and earlier is reviewed to test this proposal. Elegant experiments using the unique genetic system offered by Oenothera (the evening primroses) clearly show that plastids carry heritable characters not under nuclear control. Two or even three distinctive kinds of plastids may coexist and retain their identities in a single line of heteroplastidic cells. The distinctive characters of a line of plastids were even maintained in contact with a foreign nuclear genome for more than 10 generations of reproduction of the host plant. Studies in Epilobium, corn, tobacco, and other plants further demonstrate the heritability and mutability of an independent plastid genome. Time-lapse micro-cinematography, electron microscopy, histochemistry, cell fractionation, tracer and biochemical studies, and DNA hybridization all show that plastids are reproduced only from pre-existing plastids, that they contain DNA differing in many traits from nuclear DNA, that they contain their unique ribosomes, and that even when isolated in vitro or in enucleated cells they still synthesize their own DNA, transcribe at least some RNA, and synthesize some protein. In all of these characters plastids more closely resemble complete blue-green algea than they do other parts of the eukaryote cell.
What do these findings imply for ideas about the origins and early evolution of cells? There are two major anomalies in the previously accepted dogma that all eukaryotes trace from phytoflagellates, which are supposed in turn to derive from blue-green algae:
These anomalies vanish if chloroplasts evolved independently, and only secondarily united in a symbiosis with eukaryote cells. It follows that each type evolved independently from the primordial organic soup. Chloroplasts derive from a line of "producers" which evolved stereochemically complex systems of coupled electron transfer reactions to cope with a decline in the quality of the soup. Cytoplasmic motility would be incompatible with coupling the systems stereochemically. Eukaryotes trace from early "consumers" which evolved simple cytoplasmic motility to sop up adsorbed building blocks, and then graduated to phagocytosing "producers." The cytoplasmic shearing forces provided strong selection pressures for the evolution of nucleoprotein chromosomes and nuclear membranes. More complexly specialized motility apparatuses trace easily from a generalized cytoplasmic motility based initially on only a few different kinds of molecules.
The manuscript was first submitted in Hampton L. Carson's Genetics and Evolution course at Washington University, St. Louis., May 3, 1966. It was revised Summer, 1966, in hopes of finding a sponsor for its publication. It was shown at the cell biology meetings in Ames, Iowa, with no result, and since then I have had no time to update the presentation. The typescript includes 26 pages of text, and 66 references. Although old, and certainly not current with the literature, I have decided to try submitting the MS as is to Evolutionary Theory. Many of the ideas are still fresh and deserve further development.
The 1979 abstract and comment was included on a version of the paper distributed with job applications for biology positions in 1979-80. As things transpired, I failed to find the kind of academic position that allowed me to continue my career in biology.
The version here was scanned, OCRed and converted to HTML in 2004 from a photocopy of the summer 1966 version included in 1979-80 job applicatoins. The only changes made from the raw OCRed text were to correct OCR conversion and spelling errors and to add HTML markup and links.
It is interesting to compare my 1966 MS with Lynn Sagan/Margulies's 1967 article, On the Origin of Mitosing Cells", J. Theoretical Biology, p. 225 and 1970 book, Origin of Eukaryotic Cells, Yale University Press. To me, the most significant indicator that chloroplasts had an independent genetic system was the phenotypic evidence for the inheritance of plastid features in ways that could not be explained by inheritance via genetic systems based on nuclear chromosomes. The other area where our analyses differed significantly was in the origin of the flagellar motility apparatus. My theory is that flagellar locomotion of eukaroyotic cells is a directly evolved extension of an already motile cytoplasm, where Sagan/Margules hypothesized that the flagella evolved through the endosymbiosis of spirochaete bacteria. There is now overwhelming evidence that endosymbiosis of chloroplasts and mitochondria certainly occurred, and in fact, may have occurred more than once.
Had I succeeded in finding a sponsor for the paper at the 1966 cell biology conference, I have no doubt that it would have become a classic paper in cell and evolutionary biology. However, given that I had no perceptible qualifications in cell biology, that I was only a masters degree student in a university that had no accredited masters degree program, and that the study was a distraction my research program on chromosomal evolution and speciation in lizards, I did not persevere in trying to publish it following the lack of interest at the cell biology conference. It took all of my intellectual effort to move from the non-existent graduate program at Southern Illinois University, Edwardsville to Harvard University's PhD program.