Erwin Baur Or Carl Correns: Who Really Created the Theory of Plastid Inheritance?

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. zonale. He crossed green torial chimeras) by the theory that somat- rise to cotyledons and the growing point, re- and periclinal chimeric white-margined ic segregation and sorting out of plastids ceives only green plastids during one of the first plants (or white shoots from otherwise had occurred: variegated plants devel- divisions, then a seemingly pure green hybrid will be produced. If only white plastids segre- white-margined plants). Reciprocal cross- oped from zygotes containing two distinct gate into that cell, seemingly white progeny will es revealed a biparental, but non-Mende- types of plastids, namely green plastids be generated, etc. Furthermore, a simple con- lian, inheritance of the leaf color trait (from one parent) and white plastids sideration—which I need not explain through

436 The Journal of Heredity 2000:91(6) lengthy or detailed writing—leads us to realize [Original German text in Baur (1909:350) and in that, after a large number of divisions, cells with Hagemann (2000:103).] both types of plastids will decrease in percent- age as compared to cells with only one type of plastid. In his following publications, Baur This hypothesis is well in accordance with all (1911, 1919) described several additional facts that, thus far, have been determined em- experiments and observations from his pirically; it will have to be tested by further in- studies with Pelargonium zonale which vestigations which, however, I do not at all wish to reserve for myself. were in full agreement with his initial sug- gestions outlined in the article of 1909. [Original German text in Baur (1909:349–351) Studies on green-white variegated plants and in Hagemann (2000:102). Baur always used of Antirrhinum majus. Simultaneously with the term ‘‘chromatophores,’’ which has been translated into ‘‘plastids.’’] the Pelargonium studies, Baur performed experiments with green-white variegated plants of snapdragon (Antirrhinum majus) Hypothesis of biparental transmission of (Baur 1910a,b). In this species he found plastids in Pelargonium. In the first decade (by conducting reciprocal crosses) the of the 20th century, among botanists, the same mode of non-Mendelian inheritance opinion was held that in higher plants the as Correns (1909a,b) had described for plastids are transmitted to the next gen- Mirabilis jalapa:InA. majus, the difference eration only by the mother plant. Baur im- between green and white is inherited mediately realized the inconsistency of his through the mother only: green branches experimental genetic findings with this give rise to green seedlings only, white Figure 2. Carl Correns (1864–1933). widely held opinion. Trusting his experi- branches produce only white offspring, mental results he proposed that his cross- while the variegated branches produce es might indicate that, in Pelargonium, green, white, and variegated seedlings in gument was based on the terms ‘‘healthy’’ plastids are transmitted biparentally to widely varying ratios. The genetic consti- and ‘‘ill’’ (‘‘diseased’’). In his articles of the next generation (i.e., by the female as tution of the pollen had no effect on the 1909 (a,b), he expressed the view that the well as by the male parent): phenotype of the progeny. factor determining green or yellow (or Initially Baur only pointed out the ac- white) plastids was due to the relative The hypothesis makes—to emphasize this once cordance of his findings with the results health of the cytoplasm: ‘‘The basis of the again—just one assumption, that is not yet that Correns had obtained for Mirabilis. white leaf color is a diseased state of the proven, namely that the fertilized egg cells gen- However, in the third edition of his text- cytoplasm, a non-infectious chlorosis.’’ erated through fusion of a ‘white’ with a ‘green’ book of genetics, Baur (1919) clearly stat- gamete cell, carry two types of plastids: white Correns assumed the existence of two ones and green ones. [. . .] According to the cur- ed that the examples of green-white var- types of cytoplasms, a healthy cytoplasm rently dominant scientific dogma, the plastids iegation in Pelargonium (biparental and an ill one. When (indifferent) plastids of the fertilized egg cell descend only from the inheritance) as well as in Antirrhinum, Mir- are introduced into a healthy cytoplasm, mother; whether or not this is really absolutely abilis, and Primula (maternal inheritance) they develop into normally green chloro- certain, shall remain undiscussed here. If the are cases of plastid inheritance. Baur re- plastids should indeed always come only from plasts; however, when they are introduced the mother and, hence, if the currently domi- ferred to, accepted, and supported the into an ill cytoplasm, then they remain (or nant opinion is correct, then we are faced here view of O¨ . Winge (1919) that variegation in become) white or yellow. ‘‘Thus, the cell with extremely curious modes of inheritance. It the aforementioned species are examples nuclei of the whole plant would be uni- then must be the case that, in a white ϫ green of plastid inheritance. The only difference cross, part of the white plastids of the egg cell form and healthy. However, the cyto- are converted into green plastids under the in- is that in the case of maternal inheritance, plasms, depending on the mosaic, ill or fluence of the male sexual nucleus, and, in the the plastids are transmitted only by the healthy. [Original German text in Correns reciprocal cross, part of the green plastids of egg cells, whereas, in the case of biparen- (1909a:322).] the egg cell must turn into white plastids under tal inheritance (Pelargonium), the plastids Correns was well aware of Baur’s con- the influence of the male sexual nuclei stem- are transmitted by both the egg cells and ming from a white plant. Of course, theoretical- trasting argument (1) that the plastids ly, something like that can be imagined, how- the sperm cells of the pollen. Baur held themselves are the carriers of the genetic ever, to the best of my knowledge, there is no this view in all of his later publications on differences between ‘‘green’’ and ‘‘white’’ inheritance phenomenon known which would this issue. and (2) that, in Pelargonium, pollen and be analogous to this in any respect. Although Thomas Hunt Morgan was But should it—in contrast to the hitherto rul- egg cells transmit plastids to the next gen- ing doctrine—turn out that the male sperm very skeptical regarding many reports on eration, while in Antirrhinum and Mirabilis, cells are also able to transmit plastids into the the phenomenon of ‘‘cytoplasmic inheri- only the egg cells transmit plastids. How- egg cells, then the hereditary processes of the tance,’’ in his book The Physical Basis of ever, he was reluctant to accept Baur’s white-margined plants (of Pelargonium) would Heredity, Morgan (1919) expressed his view. ‘‘I cannot believe that the two exper- be fully understandable. agreement with the theory that plastids Only further investigations will enable dis- imental organisms (Pelargonium—Mirabi- crimination among these possibilities. It is def- are carriers of hereditary factors. lis) should behave so fundamentally differ- initely necessary that the developmental pro- ently in this respect’’ (Correns 1909b:340). cesses regarding the plastids of higher plants The Position of Carl Correns In some publications, Correns (1909b, have to be carefully studied with newer meth- ods in a continuous series from the sexual cell By contrast with the interpretations of 1928) even compared the ‘‘illness of the (through the developing organism) to the sex- Baur, Carl Correns (Figure 2) developed a cytoplasm’’ in such variegated plants with ual cell of the next generation. rather different hypothesis. His line of ar- the action of the agents causing tubercu-

Hagemann • Baur or Correns: Who Really Created Plastid Genetics? 437 losis or with spirochetes. In his later arti- necio); already after one of the first divisions of cles on non-Mendelian inheritance, Cor- the embryo a decision could be made leading to a clear mosaic. rens (1922, 1928) added to his hypothesis one important new idea: He assumed that [Original German text in Correns (1928:144–145) and in Hagemann (2000:111, 113).] in plants that later will become green- white variegated, the cytoplasm of the ‘‘embryonic cells’’ (i.e., the zygote and One of the main arguments of Correns early meristematic cells) is in a ‘‘labile cy- against Baur’s theory was the presumed toplasmic state.’’ During early develop- lack of ‘‘mixed cells’’ within variegated ment of the seedlings, this ‘‘labile state’’ leaves. If somatic segregation of green and switches either to a normal, permanently white plastids would take place at ran- ‘‘healthy state’’ (allowing the formation of dom, one has to expect (according to green chloroplasts) or to a permanently Baur’s theory) not only cells with green ‘‘diseased state’’ (causing white plastids plastids and those with white plastids, but and cells). also cells that contain both types of plas- Correns summarized his view in his lec- tids. Unless the two plastid types are mu- ture for the Fifth International Congress of tually exclusive, ‘‘mixed cells’’ (Mischzel- Genetics in Berlin (September 1927). He len) should be found containing both held this opinion until his death in 1933. green chloroplasts and white plastids side by side within one and the same cell. Correns repeatedly stated that such Instead of attributing the primary cause for the different colors to the chloroplasts and as- ‘‘mixed cells’’ had not been found in a suf- suming that the healthy green and the ill white ficient quantity or not at all. However, Cor- plastids are located in a cytoplasm which would rens cited three authors who had reported be neutral in this respect, one could search for the finding of ‘‘mixed cells’’; among them Figure 3. Otto Renner (1883–1960). the cause in the cytoplasm itself that then would occur in two different states, a healthy was his coworker Funaoka (1924) who ob- one in which the chloroplasts can turn green, served ‘‘mixed cells’’ in variegated leaves leaves, whereas most of them caused and an ill one which prevents them from green- of Stellaria media ‘‘relatively frequently’’ white plastids and leaves). ing. This assumption would let us understand (Correns and F. von Wettstein 1937:17, 22). Starting in 1922, Otto Renner (Figure 3) the absence of ‘mixed’ cells, particularly in ma- Later, such ‘‘mixed cells’’ were found by ture tissue, because the behavior of all plastids published numerous articles on plastid in- always would be determined by the cell cyto- light microscopy and by electron micros- heritance. He performed crosses between plasm. Besides this, single exceptions that oc- copy in many species. I have summarized different species of the genus Oenothera cur more or less frequently, depending on the these findings, including all relevant ref- (subgenus Euoenothera). Their analysis specific cytoplasm, probably can be explained. erences, in several previous reviews (e.g., However, this theory would have to refrain led him to the discovery of a new phenom- from explaining the mosaic of the final differ- Hagemann 1964, 1965). enon in plastid genetics: hybrid (plastid) entiated stage by tracing it back to a mosaic in deficiency (‘‘Bastardbleichheit’’). Different a single cell. Even though we could assume the species of the genus Oenothera do not presence of the two types of cytoplasm in the The Foundation of the Theory of initial cell, an unequal distribution of them ac- Plastid Inheritance only differ in their genotypes, but also in cording to that of the two types of chloroplasts the genetic constitution of their plastids is too improbable, a mixing would be expected In view of these original statements by (the plastome). Evolution involved not to occur all too soon. Baur and Correns in their publications only mutations in the genome complexes, By contrast, the cytoplasm of the embryonic from 1909 to 1933, we must come to a cells (in such albomaculata-colored plants) but also a genetic diversification of the could be in a labile state, capable of adopting clear conclusion concerning the founda- plastomes. The differences in the plasto- the healthy or the ill state as a consequence of tion of the theory of plastid inheritance: mes are manifested by specific plastid reasons that we call ‘random’ (1922). The ge- The only founder of the theory of plastid types being unable to green when inter- nome would remain unaltered; however, a cell inheritance was Erwin Baur (cf. Hagemann acting with certain genome complexes; that once would be differentiated in the one or 2000). With his classic article on P. zonale the other way, would retain its characteristic however, when interacting with their na- cytoplasm [. . .] It can and will undergo further in 1909 he laid the groundwork for the cur- tive genome complexes, these plastids de- divisions: depending on whether the decision rently flourishing discipline of ‘‘plastid ge- velop into normal green chloroplasts. about it is made sooner or later, here or there, netics.’’ Here, occurrence of a chlorophyll defi- closer to or farther away from the definitive state of the organ, it will give rise to a larger or ciency is clearly not due to a plastid ‘‘loss a smaller area of white or green tissue, from en- The Further Development of the mutation.’’ Instead, during evolution of the tire branches down to single cells. genus Oenothera, ‘‘differentiation muta- The purely maternal transmission would oc- Theory of Plastid Inheritance by Otto Renner tions’’ (‘‘Differenzierungs-Mutationen’’) oc- cur through the cytoplasm (which is subject to curred that led—paralleled by nuclear mu- constant changes) and would give rise to en- tirely green and completely white seedlings. Baur’s experiments with Pelargonium were tations during species evolution—to Plastids that are transmitted with the sperm nu- based on so-called loss mutations (‘‘De- genetic differences in the interactions be- cleus would adjust to the egg cytoplasm and fekt-Mutationen’’), plastid mutations caus- tween the nucleus and the plastids. The depending on that would become either healthy ing an inability of the plastids to become genetic details of these interactions be- or ill. [. . .] The colored seedlings, however, would stem from egg cells that were still in the green (in any nuclear background that tween different nuclear genomes and five labile state (which would be in accordance with had been tested); some of these plastid different types of wild-type plastids sub- their position in mosaics of Taraxacum and Se- mutations led to yellow plastids and sequently were defined by Renner’s for-

438 The Journal of Heredity 2000:91(6) mer student and coworker W. Stubbe cause we do not see the plastids creeping out dent element. Furthermore Renner (1936) tries (1960). Moreover, Renner (1936) and of the pollen tube into the egg cell. That we can- to show that the other cases of non-Mendelian not see this transition means, as compared to variegation are consistent with this explanation. Schwemmle (1940) also found ‘‘plastid the significance of the variegation phenomena, The differences result primarily from the mode loss mutations’’ in Oenothera which almost as little as the invisibility of the chro- of transmission of the plastids by the pollen caused white plastids (comparable to the mosomes in mature germ cells as compared to tube. It seems that a broad range of plastid white plastid mutants studied by Baur in the significance of the chromosome number transmission is possible from cases with ample during the division of the zygote nucleus. transmission of plastids by the pollen tube to Pelargonium and Antirrhinum). Skepticism is good, but should be measured! those in which no paternal plastids are donated All results of crosses in the genus Oen- The development of the chromosome theory to the egg cell. The sorting-out occurs with dif- othera convincingly proved the biparental of Mendelian inheritance has shown that sci- ferent speeds, which may be due to different inheritance of plastids. In Oenothera (and entists were on the right track that, after having properties of the cytoplasm. [. . .] According to also in Hypericum), reciprocal crosses be- reached a certain body of evidence, did not fur- all results that have been published thus far, I ther question every aspect of the importance of (ϭ F. von Wettstein) have come to the conclu- tween green and white plants or branches the chromosomes, but believed in the theory. sion that the explanations of Renner are well lead to distinct reciprocal differences with From their experimental data, these believers founded for many cases; many reservations, a strong bias toward the plastids of the have erected the foundation of the current the- which Correns expounded, can be dispelled maternal parent. Crosses of green ϫ white ory of inheritance, to which the doubters have now. contributed nothing significant ever since. yield variegated, many green, and (almost) In my opinion, this evidence for the autono- [Original German text in Correns and von Wett- no white seedlings; whereas crosses of my of plastids is nowadays so well supported stein (1937:42, 45) and in Hagemann (2000:123– white ϫ green yield variegated, many that it is worth formulating a theory on this au- 124).] white, and (almost) no green seedlings. tonomy and taking this theory as the basis for These results were confirmed with both further deductive treatments of this problem. This statement indicates that Fritz von From the experiences with the sudden ap- Wettstein had decided to revise Correns’ white plastome mutants and hybrid defi- pearance of colorless tissue areas in lines that cient plastids. had been purely green for generations, one has position and to accept the convincing re- In several papers and reviews from 1922 to conclude that the plastids can change their sults and the clear arguments of Renner to 1937, Renner dealt with different as- constitution by themselves, without an influ- thus agreeing on Baur’s theory of plastid ence of the nucleus. This change is practically inheritance. pects of plastid inheritance. He always em- irreversible and I do not know any reason why phasized that his results are in full accor- one should not call this process plastid muta- dance with the theory of plastid tion. The Way to Molecular Genetics of inheritance as formulated by Erwin Baur. [Original German text in Renner (1934:243, 251) Plastids Renner (1934) expressed his view in a con- and in Hagemann (2000:124–125).] vincingly lucid and expressive style: The foundation and refinement of the the- ory of plastid inheritance was based on In the years 1934–1937, the concept of clear-cut genetic results, that is, large- The explanation provided by E. Baur (1909) for plastid inheritance as founded and es- scale reciprocal crosses in several spe- the inheritance pattern of the green-white-var- poused by Baur and Renner became a ful- iegated Pelargonium plants is very straightfor- cies, their careful analysis as well as in- ward and persuasive: The non-nuclear-condi- ly established and generally accepted ge- tense cytologic investigations that tioned reactions that lead to chromatophores of netic theory. This was demonstrated ultimately provided important supportive different colors are attributed right from the be- impressively by the statements of Fritz evidence. This classical work has been ginning to the plastids themselves. A variega- von Wettstein (1937), who was a former tion ( ϭ a variegated plant) arises by the pollen summarized in detail in a number of com- tube introducing plastids into the egg upon fer- coworker and admirer of Correns and be- prehensive reviews (Hagemann 1964, tilization; those plastids differ significantly in came his successor as the director of the 1965; Kirk and Tilney-Bassett 1967, 1978). their properties from the plastids of the egg Kaiser-Wilhelm-Institute of Biology in Ber- At the end of the 1950s a number of re- and, during the course of development, the two lin. F. von Wettstein took over the respon- searchers reported the identification of types of plastids are distributed among different sibility for the posthumous publication of cells and, consequently, among different tissue specific DNA in plastids. Since 1963–1964, areas. In the green-white variegated Pelargoni- the book Nicht mendelnde Vererbung (Non- it generally has been accepted that plas- um plants, under the conditions of the experi- Mendelian Inheritance) which Correns tids contain their own organelle-specific ments, only one type of plastid is healthy and had intended to publish as a volume of the genetic information (plastid DNA) which capable of greening, the other one is always ill Handbuch der Vererbungswissenschaft and incapable of forming chlorophyll. provides the material basis for the hered- That is to say: In Baur’s hypothesis, all details (Handbook of Hereditary Science). He ed- itary factors of the plastids, termed plas- of the variegation phenomena of the Pelargoni- ited the manuscript very carefully and al- tome (Kirk 1986). um type are brought to such a perfect agree- ways tried to do this in accordance with In the following decades, the plastid ment with the developmental history of the the initial intentions of Correns. However, DNAs of many plant species were intense- shoot that one could deduce the cell division to the chapter on non-Mendelian variega- processes at the shoot apex—if they were not ly characterized regarding their buoyant known—from the variegation patterns. In turn, tion, he added the following postscript: density, GC content, contour length, phys- if only the cell division processes were known ical size (kbp) and renaturation behavior. and the chromatophores were submicroscopi- In the 1970s, the discovery of restriction cally small, one could infer from the phenomena The publications of Renner (1922, 1924, 1929, of colored-leaf plants, the existence of distinct and above all 1936) have informed us of a huge enzymes and the growing methodological carriers of the chlorophylls. amount of experimental material and results on spectrum of gene technologists paved the How happy would we be if, in other cases, we this subject; the details are dealt with there. way for the rise of plastid molecular ge- would see only half as clearly the relationship These results make it clear that the plastids netics. Over the past two decades our between the hereditary material of the germ possess characteristic and specific traits and a cell and the phenotype of the mature organism! specific make-up, which guarantee their genetic knowledge concerning all aspects of plas- And this clarity would be clouded by the intro- independence of the nucleus. Renner has tid biology has benefited immensely from duction of a labile state of cytoplasm just be- coined the term ‘‘plastome’’ for this indepen- the power of molecular genetics.

Hagemann • Baur or Correns: Who Really Created Plastid Genetics? 439 Erwin Baur investigated—as mentioned earli- Baur E, 1910a. Untersuchungen u¨ber die Vererbung von Herrmann FH, Schumann B, Bo¨rner T, and Knoth R, er—green-white variegations of Antirrhinum ma- Chromatophorenmerkmalen bei Melandrium, Antirrhi- 1976. Struktur und Funktion der genetischen Informa- jus which exhibited a purely maternal inheri- num und Aquilegia. Ztschr f ind Abstamm u Verer- tion in den Plastiden. XII.. Die plastidalen Lamellarpro- tance. Our plastid research group at the bungsl 4:81–102. teine der photosynthesedefekten Plastommutante en: gilva-1 (‘‘Mrs. Pollock’’) und der Genmutante ‘‘Cloth of University of Halle studied several of such var- Baur E, 1910b. Vererbungs- und Bastardierungsversu- Gold’’ von Pelargonium zonale Ait. Photosynthetica iegated lines. We obtained one line from Profes- che mit Antirrhinum. Ztschr f ind Abstamm u Verer- (Praha) 10:164–171. sor Hans Stubbe, Gatersleben, who was a PhD bungsl 3:34–98. student and coworker of Erwin Baur. The mu- Kirk JTO, 1986. The discovery of chloroplast DNA. Baur E, 1911. Einfu¨hrung in die experimentelle Verer- BioEssays 4:36–38. tant plastids of this line, designated en:alba-1, bungslehre. 1. Aufl. Berlin: Gebru¨der Borntraeger. carry a specific deficiency in photosystem I, Kirk JTO and Tilney-Bassett RAE, 1967. The plastids. and thus have a total block in photosynthesis. Baur E, 1919. Einfu¨hrung in die experimentelle Verer- Their chemistry, structure, growth and inheritance. bungslehre. 3. Aufl. Berlin: Gebru¨der Borntraeger. The combination of PCR and SSCP (single- London: W.H. Freeman. strand conformation polymorphism) analysis, Bock R and Hagemann R, 2000. Extranuclear inheri- Kirk JTO and Tilney-Bassett RAE, 1978.The plastids. followed by DNA sequencing, revealed that this tance: plastid genetics: manipulation of plastid ge- Their chemistry, structure, growth and inheritance, plastome mutant has—as compared with the nomes and biotechnological applications. Progress in 2nd ed. Amsterdam: North Holland. botany, vol. 61. Berlin: Springer Verlag; 76–90. wild-type—a single base-pair substitution at co- Morgan TH, 1919. The physical basis of heredity. Phil- don 136 (TAT→TAG) within the plastid gene Correns C, 1909a. Vererbungsversuche mit bla␤(gelb) adelphia: J.B. Lippincott. gru¨nen und buntbla¨ttrigen Sippen bei Mirabilis jalapa, psaB. This point mutation in plastid DNA pro- Renner O, 1922. Eiplasma und Pollenschlauchplasma Urtica pilulifera und Lunaria annua. Ztschr f ind Abs- duces a new stop codon that leads to a trun- bei den Oenotheren. Ztschr f ind Abstamm u Verer- tamm u Vererbungsl 1:291–329. cated PsaB protein, which prevents the assem- bungsl 27:235–237. bly of a functional photosystem I complex Correns C, 1909b. Zur Kenntnis der Rolle von Kern und Renner O, 1929. Artbastarde bei Pflanzen. (Handbuch (Schaffner, Laasch, and Hagemann 1995). Plasma bei der Vererbung. Ztschr f ind Abstamm u Ver- der Vererbungswissenschft, Bd. IIA). Berlin: Gebru¨der Comparable investigations were performed erbungsl 2:331–340. Borntraeger. with the yellow-margined variety ‘‘Mrs. Pollock’’ Correns C, 1922. Vererbungsversuche mit buntbla¨ttri- of Pelargonium zonale which had been used al- Renner O, 1934. Die pflanzlichen Plastiden als selbsta¨n- gen Sippen. VI. Einige neue Fa¨lle von Albomaculatio. dige Elemente der genetischen Konstitution. Ber Ver- ␤ ready by Erwin Baur’s PhD student Ludwig Roth Sitzungsber Preu Akad Wiss 33:460–471. handl Sa¨chs Akad Wiss Leipzig Math-phys Kl 86:241– (1927). This yellow plastome mutant also exhib- ¨ 266. its a deficiency in photosystem I (Hagemann Correns C, 1928. Uber nichtmendelnde Vererbung. Ztschr f ind Abstamm u Vererbungsl, Suppl. Bd. I:131– Renner O, 1936. Zur Kenntnis der nichtmendelnden 1979; Herrmann et al. 1976). 168. These examples show that the plastome mu- Buntheit der Laubbla¨tter. Flora 130:218–290. tants, initially investigated by Baur and his co- Correns C and von Wettstein F 1937. Nicht mendelnde Renner O, 1937. Zur Kenntnis der Plastiden- und Plas- workers, have become—after many decades— Vererbung. (Handb. Vererbungswiss, Bd. II H). Berlin: mavererbung. Cytologia Fuji Jub Vol, Pars II, 644–653. Gebru¨der Borntraeger. valuable tools for studies in the field of plastid Roth L, 1927. Untersuchungen u¨ber die periklinal bun- molecular genetics. Funaoka S, 1924. Beitra¨ge zur Kenntnis der Anatomie ten Rassen von Pelargonium zonale. Ztsch f ind Abs- panaschierter Bla¨tter. Biol Zentralbl 44:343–384. tamm u Vererbungsl 45:125–159. Molecular research on plastid biology Hagemann R, 1964. Plasmatische Vererbung. Jena: Gus- Schaffner C, Laasch H, Hagemann R, 1995. Detection of tav Fischer Verlag. point mutations in chloroplast genes of Antirrhinum continues to produce exciting findings and majus L. I. Identification of a point mutation in the psaB to generate stimulating ideas (Hagemann et Hagemann R, 1965. Advances in the field of plastid in- gene of a photosystem I plastome mutant. Mol Gen heritance in higher plants. In: Genetics today. Proceed- Genet 249:533–544. al. 1981–1998). As this research proceeds, it ings XI International Congress of Genetics (Geerts SJ, should be borne in mind that this whole de- ed). Oxford: Pergamon Press; 3:613–625. Schwemmle J, 1940. Plastidenmutationen bei Eu-Oen- otheren. Ztschr f ind Abstamm u Vererbungsl 79:171– velopment is founded on the brilliant clas- Hagemann R, 1979. Genetics and molecular biology of 187. sical genetic analyzes and the visionary plastids of higher plants. Stadler Genetics Symposia. Columbia: University of Missouri; 11:91–115. Stubbe W, 1960. Untersuchungen zur genetischen Ana- ideas of Erwin Baur and Otto Renner. lyse des Plastoms von Oenothera. Ztschr f Botanik 48: Hagemann R, 2000. Erwin Baur (1875–1933). Pionier der 191–218. Genetik und Zu¨chtungsforschung. Seine wissenschaf- ¨ tlichen Leistungen und ihre Ausstrahlung auf Genetik, Winge O, 1919. On the non-Mendelian inheritance in variegated plants. Compt Rend Trav Labor Carlsberg References Biologie und Zu¨chtungsforschung von heute. Eichenau: Verlag R. Kovar. 14:1–20. Baur E, 1909. Das Wesen und die Erblichkeitsverha¨lt- Received February 21, 2000 nisse der ‘‘Varietates albomarginatae hort.’’ von Pelar- Hagemann R, et al. 1981–1998. Extranuclear inheri- Accepted August 30, 2000 gonium zonale. Ztschr f ind Abstamm u Vererbungsl 1: tance: plastid genetics (reviews in:) progress in botany, 330–351. vol. 43, 45, 47, 49, 51, 55, 57, 59. Berlin: Springer Verlag. Corresponding Editor: David B. Wagner

440 The Journal of Heredity 2000:91(6)