Erwin Baur Or Carl Correns: Who Really Created the Theory of Plastid Inheritance?
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Erwin Baur or Carl Correns: Who Really Created the Theory of Plastid Inheritance? Rudolf Hagemann Historical reviews of the field of non-Mendelian genetics and many other publica- tions credit Erwin Baur and Carl Correns equally for the development of the theory of plastid inheritance. However, a study of the original literature indicates that this conclusion is not correct. Analysis of the relevant articles leads to the conclusion that Baur alone deserves credit for the theory of plastid inheritance. In his classic article on the inheritance properties of white-margined Pelargonium plants, Baur (1909) stated: (1) The plastids are carriers of hereditary factors which are able to mutate. (2) In variegated plants, random sorting-out of plastids is taking place. (3) The genetic results indicate a biparental inheritance of plastids by egg cells and sperm cells in Pelargonium. By contrast, Correns held the view that in variegated plants there is a maternally transmitted labile state of the cytoplasm which switches either to a permanently ‘‘healthy’’ state (allowing the ‘‘indifferent’’ plastids to be- come green chloroplasts) or to a permanently ‘‘diseased, ill’’ cytoplasmic state (causing white plastids and cells). Otto Renner supported Baur’s theory and worked out important characteristics of plastid inheritance in the genus Oenothera. In the 1930s Renner reported many more observations, which established plastid inher- itance as a widely accepted genetic theory. Plastid Genetics as an Integral basic research, plastids have also attract- Part of Current Genetic Research ed the attention of plant biotechnologists due to the recent development of trans- Research involving plastid as well as mi- formation technologies for higher plant tochondrial genetics has contributed to chloroplasts, which enable the expression recent advances in both basic and applied of foreign genes in the plastid compart- research. Over the past 15 years the com- ment (Bock and Hagemann 2000). plete DNA sequences of several plastid ge- In contrast to the general importance of nomes from higher and lower plants have research on plastid genetics, many text- been determined. In addition, extensive books of genetics (irrespective of their studies on the expression of plastid genes, country of origin) almost completely ig- their mutations, their regulation, and in- nore the field of plastid genetics: it is men- teraction with the nucleocytoplasmic tioned on at most two or three pages in a compartment have advanced our knowl- total text of 500 or 800 pages and, more- edge of the role of plastid genes within the over, the text frequently contains errone- genetic system of plants. ous statements. (The situation regarding Recent molecular work also has provid- mitochondrial genetics is slightly—but ed new insights into the evolution of plas- not much—better.) tids from formerly free-living cyanobacte- This article addresses this problem by ria. Nowadays a wealth of genetic, providing a review of the original litera- biochemical, and cytological data support ture from the turn of the 20th century. the idea that the endosymbiotic uptake of This summary of the German literature a cyanobacterium by a pre-eukaryotic cell may also be useful to scientists within the From the Institute of Genetics, Martin-Luther-Universi- ty, Weinbergweg 10, D-06099 Halle/Saale, Germany. I was followed by the gradual transforma- discipline of organelle genetics who have wish to thank Dr. Ralph Bock for valuable discussions tion of the endosymbiont into a plastidlike questions concerning the history of this of the manuscript and his advice for improvement of cell organelle—a process accompanied by field, how this discipline has evolved from the text. Moreover, I thank Dr. Richard Tilney-Bassett and three anonymous referees for critical reading of massive gene transfer from the plastid ge- its very beginning, and who was the dis- the manuscript and many valuable comments. nome to the chromosomes in the cell nu- coverer of the basic principles of plastid ᭧ 2000 The American Genetic Association 91:435–440 cleus. In addition to their importance in inheritance. 435 Discovery of Non-Mendelian green versus white. The F1 progeny con- (Extranuclear) Inheritance by Carl sisted of green, green-white variegated, Correns and Erwin Baur and white seedlings. In many crosses there was a bias in the F toward the phe- In one issue (no. 3) of Volume 1 of the 1 notype of the maternal parent. ‘‘Zeitschrift fu¨r induktive Abstammungs- Thus, in 1909, Baur and Correns simul- und Vererbungslehre’’ (the first interna- taneously discovered and described the tional journal of genetics and the progen- occurrence of non-Mendelian inheritance itor of Molecular and General Genetics), in higher plants. Their conclusion that in Correns and Baur separately published ar- addition to the Mendelian inheritance of ticles on non-Mendelian inheritance of var- genes in the cell nucleus, there are other iegated phenotypes in plants. Correns hereditary factors outside the nucleus (1909a) emphasized in a footnote to his (i.e., in the protoplasm) which exhibit a article: ‘‘The simultaneous publication of non-Mendelian mode of inheritance marks this paper with the following article by E. a milestone in genetics and the date of Baur is based on mutual agreement; how- birth for a new field of research. Although ever, each of us had no knowledge of the credit for the initial observations should contents of the other ones paper.’’ The ti- be shared between Baur and Correns, tles of the two articles are their subsequent theoretical interpreta- Correns, Carl. Vererbungsversuche mit tions distinguish their contributions to the Figure 1. Erwin Baur (1875–1933). blass(gelb)gru¨nen und buntbla¨ttrigen Sip- field. pen bei Mirabilis jalapa, Urtica pilulifera und Lunaria annua. Zeitschr f ind Abst u (from the other parent). In the course of The Foundation of the Theory of Vererbungsl 1909;1:291–329. (Inheritance the subsequent cell divisions, plastids seg- Plastid Inheritance experiments with pale (yellow) green and regate randomly. This random segregation variegated varieties of Mirabilis jalapa, Ur- The authors of numerous monographs, re- regularly results in sorting out of the two tica pilulifera and Lunaria annua.) view articles, and textbooks express the types of plastids and—during ontogenetic opinion that, in 1909, Erwin Baur and Carl growth of the plants—in the formation of Baur, Erwin. Das Wesen und die Erbli- Correns contributed equally to the estab- pure green and pure white areas in one chkeitsverha¨ltnisse der ‘‘Varietates albom- lishment of the theory of plastid inheritance. and the same plant. arginatae hort.’’ von Pelargonium zonale. However, a careful study of the original lit- Baur’s development of this theory is Zeitschr f ind Abst u Vererbungsl 1909;1: erature indicates that this interpretation documented by the following citations 330–351. (The nature and the inheritance does not reflect the history of plastid genet- from his 1909 paper (in English transla- properties of horticultural varieties of Pel- ics correctly. Below, the original sources in tion): argonium zonale having white borders.) the genetic literature are analyzed. For different plant species both authors I have, on the basis of these observations, reported the non-Mendelian mode of in- The Position of Erwin Baur formed a theory which shall serve as a working hypothesis for the following investigations [. .] heritance of green-white or green-yellow The theory of plastid inheritance and of ran- The P. zonale races with white-margined leaves leaf variegations. dom sorting out of plastids. In his article are chimeras with a periclinally divided growing Following crosses between variegated, Baur (1909) was the first to provide the point.. The peripheral two or three cell layers yellow, and green plants (or branches) of explanation that chloroplast defects in P. of the shoot apex have only albino plastids, which entirely lack the capacity of chlorophyll Mirabilis, Urtica, and Lunaria, Correns zonale and their mode of inheritance are formation. The central cells of the shoot apex, found that the leaf color trait (green ver- cases of plastid inheritance: The green however, contain entirely normal plastids ca- sus yellow) is inherited through the moth- and the white shoots of variegated plants pable of turning green. er only, that is, that there is a purely ma- differ in the genetic constitution of their The fertilized egg cell, as generated through ternal inheritance: green branches always plastids (Baur used the term ‘‘chromato- the union of a ‘green’ with a ‘white’ gamete cell, thus contains two types of plastids, green and produced seeds that gave rise to green phores’’). One plastid type is green (nor- white. During the cell divisions leading from the seedlings, seeds from yellow branches mal, nonmutated, capable of becoming egg cell to the embryo, the plastids are distrib- yielded only yellow offspring, while the green during ontogenetic development); uted to the daughter cells entirely randomly. variegated branches produced green, yel- the other type is white (mutated, incapa- Whenever a daughter cell receives only white plastids, this cell subsequently will have only low, and green-yellow variegated seedlings ble of becoming green). white descendent cells, and will give rise to a in widely varying ratios. In contrast, the In his 1909 paper, Erwin Baur (Figure 1) white sector within the mosaic; whenever a pollen-providing parent had no influence explained the green-white variegation of daughter cell receives only green plastids, a sol- on the phenotype of the progeny. seedlings and the formation of branches in id green sector will arise from it. Cells with both Baur found another type of non-Mende- the F plants with different phenotypes types of plastids will be capable of segregating 1 further, and so on.; probably, I need not explain lian inheritance in his crossing experi- (green, variegated, white; periclinal or sec- this in greater detail. If the cell, which will give ments with P.