Evening Primroses in Early Modern Science

Missouri evening primrose, Oenothera missouriensis

Evening primroses are a group of moderately obscure North America wildflowers (genus Oenothera, evening primrose family, Onagraceae). Unrelated to primroses or roses, evening primroses are pretty and easy to grow, so they have played a solid role in the development of genetics and plant biology.

If you ask, "why do botanists study some plants and not others?" the answers are all very human. Does it grow where they work? Or at a spectacular location where they would like to work? Do they know the plant? That gives showy flowers an edge. Can it be grown easily? Having as many plants as you want allows much better experiments.

Evening primroses do most of those well, so they were noticed by botanists long ago. Which led to publications about their biology, and to more study.

common evening primrose, Oenothera biennis

The common evening primrose, Oenothera biennis, was taken to Europe before 1600. Europeans ate it as a vegetable; you'll hear it called German rampion. (Rampion without the word German is Campanula ranunculus, in the bellflower family Campanulaceae. Historically, rampion roots were eaten.) As they were discovered, other evening primrose species were carried to Europe as well. The characteristics of growing easily and producing lots of seeds made it no surprise that common evening primroses escaped from cultivation to grow in "waste ground and open habitats, road verges, railway embankments, and sand dunes" all over Europe.

common evening primrose Oenthera biennis 
as a lawn weed in Stockholm, Sweden

Thus, Dutch botanist Hugo DeVries noticed evening primroses in an abandoned potato field behind his house in Amsterdam in the 1880s. DeVries wanted to understand inheritance in plants. At the time, Gregor Mendel's papers, to which we give credit for elucidating the laws of inheritance (genetics), published in 1866, were not generally known. (In 1970, I found Mendel's papers difficult reading because he had to invent the terms he used, and genetics today uses different words link).

DeVries crossed evening primroses with different characteristics, planted their seeds, and compared the generations. He observed, like Mendel, that genes acted as units, passed down between generations, concealed or expressed depending upon the other copy of that gene (allele) in the individual. In searching the literature, DeVries discovered Mendel's papers and, simultaneously with Karl Correns and Erich Tshermak elsewhere in Europe, publicized Mendel's work. (link). 

From his own work, DeVries developed a theory of evolution that featured mutation, sudden appearance of novel characters, as the cause of change. This was in contrast to Darwin's view that natural selection--survival of the fittest--caused plant and animal characters to evolve. DeVries' view was based on his observations crossing lots and lots of evening primroses, where sudden and unexpected changes happened and were passed on. But evening primroses are unusual. 

common evening primrose, Oenothera biennis, in Basel, Switzerland

In the 1920s, American botanists were squashing plant cells to look at cell division under the microscope. Deeply-stained chromosomes paired during sexual cell division (meiosis) and went half to each daughter cell, at random. Since they carry the genes, this resulted in recombination (scrambling) of parental characters among offspring. This was normal. But when they looked at evening primrose cells-- again because the evening primroses were available and easy to study--they found that in some species the 7 pairs (total 14) chromosomes did not behave normally. In the common evening primrose, just before division, the chromosomes were seen as two rings, one containing 6 chromosomes, the other with 8. Inheritance was weird too, because many traits stayed together and did not segregate. For example if a tall plant with a red stem was crossed with a dwarf with a green stem, the progeny would all be tall with red stems OR dwarf with green stems, never tall with green stems or dwarf with red stems. That violated the rules of Mendel worked out and made a serious problem for early 20th century geneticists. 

Detailed study of evening primrose chromosomes, by Hooker, Renner, Cleland, and others, ultimately showed that sections of the chromosomes had been exchanged (translocated), so that in order to pair at meiosis, multiple chromosomes had to link up. I made diagrams, but they are long, so they are appended to the end of this blog. When a plant was a translocation heterozygote, having all the genes but in two different chromosome arrangements, that constrained the possible recombinations. Two pairs of chromosomes should create 4 x4 = 16 pairwise combinations but in a translocation heterozygote there would be only 4 combinations (see diagrams). 

Some species of evening primrose showed more recombination than others, because of the number chromosomes with translocations varied. At the extreme, all 14 chromosomes formed a single ring, as in Hooker's evening primrose, Oenothera elata subspecies hookerii. These plants produce only four combinations of genes (see diagrams) not the 2,197 unique combinations expected of seven pairs chromosomes. Mendelian genetics worked in evening primroses but only if you considered the position of the genes on the chromosomes.

Evening primroses taught botanists a lot about genes, chromosomes, and inheritance, although, at the beginning, they were really puzzling. What DeVries' saw as evolution by mutation was translocations blocking and releasing evening primrose genetic variation. Once the role of translocations (and chromosomes) was understood, the strange behavior of genes in evening primroses was integrated into the developing understanding of evolution. What I'd says today is that mutations are required for genetic variation, then natural selection selects among the variants (mutations) for more fit combinations. Both are required and their interaction can be quite complex, depending on things like, for example, chromosomal translocations. 

common evening primrose with visiting native bee

Evening primroses aren't important in genetic studies today, but they still are pretty, easy to grow, make ring chromosomes, and pass on reduced numbers of genetic combinations. 

Comments and corrections welcome.

Supplemental material: 

Terms that slipped in, if you haven't thought of them recently, or ever: 

homozygote - both copies of the gene or chromosome are the same; 

heterozygote the two copies of the gene or chromosome are not the same

gamete - general term for sperm or egg (sex cell)

zygote -earliest new individual (union of sperm and egg), approximately the same as embryo

allele is the copy of the particular gene, so alleles for pink and white flowers are variants of the flower-color gene. 

Diagrams of chromosome mechanics in evening primroses

Crossing two plants each with the standard chromosome arrangement will, if you think of the second ABCDE (#1-2) as slightly different, say A'B'C'D'E' (A makes pink petals and A' white petals, B makes oval leaves and B' round leaves, etc.) and the second FGJKL as F'G'J'K'L' (#2-2) create 4 combinations of chromosomes in the gametes: 1-1 and 2-1; 1-1 and 2-2; 1-2 and 2-1; 1-2 and 2-2. There four gametes, combining randomly form 16 combinations (1-1 1-1 2-1 2-1  to 1-2 1-2 2-2 2-2) in the embryos that are produced. Those 16 will be 9 unique combinations if both parents had the same chromosomes, up to 16 unique combinations if the mother and father are carrying different genes (alleles). In either event, there is substantial genetic variation in the offspring because the two chromosomes are randomly combined in the gametes and the gametes randomly combine in the embryos.

How translocation heterozygotes have to align at meiosis:

In my diagram it looks like a cross, but chromosomes in meiosis look like long pieces of string and the visual image under the microscope is of a looped and messy ring. (link Fig. 19.3)

The translocation heterozygote can produce 6 kinds of gametes, but only 2 have all the genes and are viable:

When the two viable types of gametes combine in the four possible pairs, the outcome is a ration of 1 plant with the standard chromosome arrangement (A) to 2 plants which are translocation heterozygotes (C&D) to 1 which is homozygous for the translocation (B). The plants grown from seeds from translocation heterozygotes have much less expressed genetic variation than the progeny of plants that are homozygous for the translocation. This stumped botanists like DeVries until the chromosome rings were observed and translocation understood.

Final Note: Some evening primrose plants breed true via seeds. The plants are exactly like their parents, despite the genes apparently recombining during meiosis. This is a very special case where each translocation contains a different recessive lethal gene.  In heterozygous form, that is, combined with a healthy dominant form of this gene, these have no effect. They are only expressed when two copies are present in the cell, but are deadly then, killing the cell. In the example below, on genes A and L there are recessive lethals. The result is only the translocation heterozygotes survive (C &D), the homozygous combinations die, leaving sexually-produced offspring that are identical to the parents. That took a while to work out!

References
Blamey,  M. and C. Grey-Wilson. 1989. The Illustrated Flora of Britain and Northern Europe. Hodder and Stoughton. London.

Cantor, M, and E. Buta. 2008. Oenothera-ornamental crop and medicinal plant. Hameiul si Plantele Medicinale 31: 1-2.
Darlington, C.D. 1929. Ring-Formation in Oenothera and Other Genera. Journal of Genetics. 20: 345-363.

Books on evening primrose genetics 

Cleland, R. E. 1972. Oenothera, Cytogenetics and Evolution. Academic Press. New York. 

Gates, R. R. 1958. Taxonomy and Genetics of Oenothera: Forty Years Study in the Cytology and Evolution of the Onagraceae (Monographiae Biological, Vol. 7). Springer Verlag. Berlin.

Harte, C. 1994. Oenothera. Contributions to Plant Biology. Monographs on Theoretical and Applied Genetics Vol. 20. Springer Verlag. Berlin.

Or see a history of genetics book.