Riv.Biol./B. Forum, (2002) 95, 259-272.
Was Lysenko (partly) right? Michurinist biology in the view of modern plant physiology and genetics
Address: Department of Parasitology and Hydrobiology, Faculty of Science, Charles University, Viničná 7, Prague 2, CZ 128 44, Czech Republic tel.: +(4202) 21953289, fax: +(4202) 24919704, E-mail: email@example.com
Soviet lysenkoism can be considered the darkest period in the history of modern science and its main product - the Michunirist biology - a collection of absurd theories, usually based on anecdotal observation or on few badly designed experiments without proper controls or statistical evaluation of results. However, in the thirties and early forties, lysenkoists also described (and misinterpreted) some interesting observations which could have been real and which might inspire modern biologists. It is rather a serious ethical problem whether the scientific works of criminals who are responsible for destruction of whole branches of science and carriers and often even lives of people in the Soviet Union should be ignored or not. It should be, however, argued that by avoiding the topics and the areas of science that were in the centre of attention of these people we actually allow them to shed malice even long after their physical or political death.
The term lysenkoism is usually used to denote the political, social and prerogative activities of Lysenko and his followers which resulted in practical destruction of whole branches of science and carriers and often even lives of their representatives in the Soviet Union and partly also in its political satellites. The roots and impacts of these activities have been thoroughly analysed [1,2]. The term lysenkoism, however, has also a second meaning: A genetic and evolutionary theory, termed "Michurinist biology" or "Soviet creative darwinism" by its proponents, promoted by Lysenko and his followers from the early thirties to the late sixties. Michurinist biology is based on the presumption of completely "soft" heredity. Properties of organisms can be easily influenced by the environment, and the environmentally induced changes can be (and mostly are) transmitted genetically to the offspring. These ideas were in contradiction with the body of knowledge of standard genetics even in the thirties. Although we can suspect that the primary motif of lysenkoists' decision to abandon classical genetics in favour of a "new and better" (i.e., "progressive and proletarian") genetics was to replace "official" geneticists in their posts in the scientific management, we cannot exclude the possibility that Lysenko s views could have been influenced by his agrotechnical experience. Although Lysenko's empirical evidence supporting his theory would not stand critical review by nowadays' (or even his time's) standards , we cannot a priori exclude the possibility that some of the described phenomena were real and only insufficient scientific erudition of Lysenko and his co-workers caused that they were misunderstood and misinterpreted.
I would like to present an explanation of some phenomena described by Lysenko compatible with the knowledge of modern biology. I would intentionally ignore the possibility that these phenomena never existed and that the results were fabricated by Lysenko or his co-workers. In the late thirties, Michurinist genetics coexisted with standard Mendelian genetics, and therefore the chance of data fabrication was lower than after the official triumph of Lysenkoism in the forties. I will therefore focus my attention especially on the older papers included in the Agrobiology, the basic textbook of Michurinist genetics . In particular, I will concentrate on the problems of vegetative hybridisation, wobbled heritability, heritability of adaptive modifications and intravarietal hybridisation of self-fertilising plant cultivars.
Vegetative hybridisation (grafting) in plants has been always appreciated by plant-breeders as a powerful tool for production and propagation of interspecies hybrids (with low or null fertility) and rare recombinants with useful properties (whose offspring loses these useful properties during sexual reproduction due to genetic segregation). Michurinists, however, claimed that vegetative hybridisation could be used also for many other purposes. They asserted that young branches grafted on an old tree of a different sort or even species acquire some properties of the stock, and that some of such acquired properties can be sexually transmitted into next generation. For example a branch of a tomato variety with yellow fruit grafted on a red fruit tomato variety provided some fruits with a reddish tint, and some plants grown from the seed of these reddish-tint fruits gave yellow, reddish and occasionally red fruits  p. 279-280, 405. As Lysenko did not fail to stress out, assimilates but not chromosomes from the stock can enter into the scion. Similar experiments have been repeated with the same results in sixties and seventies by Japanese authors [4-6].
How to explain this phenomenon without assuming the theoretically possible but not very likely participation of retroviruses transferring genes from stock into a scion? It is not very surprising that the properties of stock influence the properties of the scion. Not only low molecular weight molecules but also proteins and RNA can easily move through phloem and therefore also enter from the stock into the scion . Current experience with transgenic plants shows that regulation of gene expression is integrated across the whole body of a plant [8,9]: overproduction of a transgene product in one part of a plant often results in gene inactivation (e.g. by a methylation of regulatory sequences of the gene) in all tissues of the transgenic plant. The red colour of tomato fruits in experiments of Michurinists and the Japan authors, however, has been transmitted to the next generation by seeds. Today we know that individual organs and tissues of a plant do not have to be phenotypically or even genetically identical. Genomes of their cells might differ due to somatic mutations, somatic recombination (results of relatively common mitotic crossing over), or due to hereditary (but often reversible) modifications (mostly methylations) of the genome . Under normal conditions differences between parts of a plant are very difficult to observe because transported molecules synthesised in other parts of the organism influence both ontogeny and physiology (and therefore phenotype) of a particular plant tissue. If a branch of a tomato plant has a genetic predisposition to produce reddish instead of yellow fruits, we might be unable to recognise it, as the pigment intermediates or pigment-synthesising enzymes, or the gene expression regulators are mixed due to mobility of molecules within the whole plant . The same branch grafted on a red-fruit tomato may obtain some of these molecules from the stock; therefore at least some fruits may be reddish, and we may be able to select the fruits with the highest predisposition for a red colour. The procedure of grafting and selection of most reddish fruits can be repeated several times (as was described by Lysenko), until we finally obtain a plant which gives red fruits without the grafting.
Visualisation of hidden genetic polymorphism could have played a role also in the production of organisms with "wobbled heritability"  p. 289, 335, 415-417. According to Lysenko's definition, heritability is an ability of a living body to demand for its development specific conditions and react these or different conditions in a specific way. Therefore, growing the plants under conditions which they are not used to (for example out of their normal geographic range), can result into development of plants with so called "wobbled heritability" that could be than used e.g. for breeding of new varieties. While the normal range provides the plants just the conditions demanded for normal development, the foreign range provides alien conditions, and the plants react to them in an abnormal way. The nature of these individual reactions is often heritable, i.e., could be transmitted to the offspring.
What used to be called "wobbled heritability" could well be the visualisation of hidden genetic polymorphism, this time, however, on the level of a population. Current molecular biology clearly shows that a large fraction of genes in populations is polymorphic; they exist in any given population in several relatively common forms . Large part of this polymorphism is hidden under normal conditions, i.e., it does not contribute to observable phenotypes . Under abnormal conditions, however, some hidden polymorphisms may manifest on the level of phenotypes of individual organisms in the population . The intrapopulation variability sharply rises. A variance of quantitative traits increases, and forms of qualitative traits that are absent or extremely rare under normal conditions appear. Observed "homogeneity" of populations under normal conditions is at least partly caused by "genetic canalisation", - genetic and epigenetic processes which can mask an influence of genetic differences among of individual organisms on the phenotype level [14-18]. The best known process contributing to genetic canalisation is genetic dominance, the ability of a dominant allele to mask the presence of a recessive allele. Phenotypical expression of many genes is also affected by epistasis, i.e., by activity of modificators, genes that influence the extent of out-manifestation of alleles in other loci [19,20]. Due to complex and often rather indirect nature of their action, the modificators may work properly only under normal conditions, i.e., in the environment in which they were originally selected for. Under abnormal conditions many of these genes-modificators have lover capacity to mask the genetic differences, the hidden polymorphism becomes apparent and produces phenotypic polymorphism that could be used in selecting organisms with new properties.
Heritability of adaptive changes in plants
Certain category of results described in the lysenkoist literature suggest the existence of a phenomenon rarely accepted by modern biologists, namely the possibility of an intraindividual selection of somatic cell lines that can result even into heritable adaptation of individual organisms to local conditions in organisms lacking the Weissmann barrier (e.g. in plants). For example, the outcome of vegetative hybridisation was substantially dependent on the age of the donor of the scion. A branch (even a young one) originating from an old tree remains stable and provides fruits with properties of the donor, while a branch from a young tree acquires the properties of the stock and produces fruits with changed properties  p. 223;  p. 22-23).
Plant age was also claimed to play a role in pollen compatibility. A young tree (sometimes only in its first season of fertility) can be fertilised with pollen from foreign varieties (or even species), while the spectrum of potential pollen donors for the same tree in next seasons becomes much narrowed  p. 28-29,  p. 198). Hybrids of two different garden varieties of perennial cabbage provide in the first season seeds which give hybrids with combinations of properties of both parents, in the next seasons the same plants produce hybrids more and more similar to kale, the original wild parent of both garden varieties  p. 188-189).
Even more important was the observation concerning the influence of environmental conditions on heritable properties of plants. Many plants are self-incompatible - they cannot be fertilised by their own pollen. Pollen incompatibility extents also to clones obtained from the same individual by vegetative reproduction (e.g. by cutting a stool or a bulb). According to Michurinists, this incompatibility within the clone can be evaded if two clones of the same plant are grown in divergent conditions (e.g., one in dry, one in moist)  p. 138).
To explain such results we must accept the possibility of existence of frequent genetic or stable epigenetic changes in the somatic tissues of plants . The relatively rare (and undirected) "traditional" mutations are a rather unlikely candidate. A far more feasible source of such changes may be paramutations, i.e., programmed and often reversible modifications of regulatory elements of genes , or somatic recombination due to crossing over between two homologous chromosomes during a normal mitotic cycle. Unlike meiotic recombinations, somatic recombinations occur many times during the life of individual plant. In somatic recombinants, total DNA contents remains unchanged, while the context of some genes changes, as some sequences from chromosomes of paternal origin are exchanged for homologous sequences from chromosomes of a maternal origin. This can result in a phenotypic change of the recombinant cell and its progeny due to so called position effect [24-26], i.e., a change in gene activity caused by changes in cis-acting elements in the vicinity of affected genes. Somatic recombinations can result into gradual breakdown of well-tried combinations of genes (i.e., linkage groups of genes, supergenes ) during the life-span of a hybrid plant (which can explain the result of cabbage experiment). From the point of view of general biology more important is the fact that hereditary differences in the phenotype exist between cells of different parts of a single plant. These differences can serve as a basis of intraindividual competition and selection. Individual cell lines (and therefore individual branches) might be more or less adapted to the existing conditions, which could result in differences in growth rates or differentiation competency of these lines. In the latter stages of the plant life only cell lines best adapted to the local conditions will participate in the development of germinal organs. Also the resistance of different apical meristems to local adverse conditions (which my manifest itself in the efficiency of pollen and fruit production) may vary within the plant. This could be a principle underlying genotrophs and similar phenomena recognised by nowadays' botany [28,29] and also the heritable adaptations in plants described (and misunderstood) by Michurinists.
Lets now return to the problem of pollen incompatibility between clonal plants grown under same conditions, and compatibility between the same plants grown under dissimilar conditions. Regardless of the stochastic nature of somatic recombination, the selection operating on cell lines and its results are more or less determined by environmental conditions. Therefore, the genetic (and epigenetic) information of germinative cells of two plants developed in identical conditions will be more similar to each other than that of two plants developed under dissimilar conditions. Such intraindividual selection-induced (both genetic and epigenetic) differences between clonal plants grown under dissimilar conditions can result into an improvement of pollen compatibility.
It is worthwhile to mention here an analogical phenomenon operating on the level of populations. Charles Darwin in his intraspecies variability-book  Part II - p. 115-117, 127, 143) described a phenomenon of gradual long-term deterioration of beneficial properties of pure races of domestic animals. He claimed that this process can be prevented and even reverted by crossing the animals with those of the same race from herds reared under dissimilar conditions. From the point of view of genetic textbook-knowledge such recommendation seems to be rather bizarre; there is no reason to recommend herds reared under dissimilar conditions. However, if we take into consideration the possibility of different conditions selecting for different alleles combination, Darwin's recommendation can be quite reasonable.
Intravarietal crossing of self-fertilising plants
Intravarietal crossing of self-fertilising plants was originally recommended by Lysenko for wheat varieties, later the same technique was tried also with other species of self-fertilising plants. Lysenko pointed out that in contrast to varieties of rye (out fertilising plant), the varieties of self-fertilising wheat were highly unstable, gradually losing their beneficial properties. Many established varieties of rye are being cultivated for long time on large areas, while most of the varieties of wheat disappear from fields and from catalogues of seed companies within thirty years  105, 111). According to Lysenko, old varieties of wheat must be continuously being substituted by new ones because the self-fertilising plants are unstable and their good properties (for which they have been originally selected) are getting lost during long-term cultivation. He claimed that this process can be stopped and reverted by artificial outcrossing between the plants of the same variety.
Although this technique seems to be groundless on the first glance, it could be a mistake to reject the idea without closer examination. Current theoretical analyses suggest the existence of a large difference in evolutionary plasticity between sexual and asexual organisms. While the asexual (and more or less also the self-fertilising) organisms can easily evolve under selection pressure by a classical Darwinian mechanism, the same is not true for sexual species [12,31]. The primary obstacle for evolution by natural selection is a low heritability of biological fitness , and often also low heritability of polygenic traits . The fitness of an organism is determined by its phenotype. However, the influence of particular phenetic traits on fitness is highly "context specific", i.e., the same trait in the context of certain traits can be useful, in the context of other traits harmful. Similarly, the influence of a particular gene on the phenotype is often context specific (this time genotype-context specific). Due to epistatic interactions between genes, the effect of an allele on the phenotype depends on the context of the alleles of other genes [12,33-35]. In asexual organisms the genotype of organisms is transmitted between generations in an unchanged form. Therefore, a particular allele has the same influence on the phenotype (and fitness) of both parent and progeny. In sexual organisms, the genotypes of offspring arise every generation "de novo" by mixing genes from two parents. Therefore, the same allele (mutation) occurs in every generation in the context of a different genotype, and its influence on the phenotype and fitness might dramatically differ. It makes the evolutionary response of sexual species on selection pressure difficult. While asexual (and partly self-fertilising) populations are as a rule evolutionarily plastic for the whole time of their existence, the populations of sexual species are plastic only under conditions of low genetic polymorphism (when alleles occur in every generation in the same or very similar context) . Such situation occurs for example after a bottleneck-including speciation event [36,37] or in experiments with small or inbred populations [38-40]. Under normal conditions, the response of a population to selection is only slow and mostly transient, i.e., after termination of the selection and breeding program the phenotypes return toward original values. The frozen plasticity of sexual species can be responsible for observed coupling of anagenesis with speciation, i.e., for punctual nature of evolution of most multicellular species in paleontological record .
The self-fertilising varieties of wheat are evolutionarily plastic for the whole duration of their existence. Therefore, they can gradually collect mutations that increase their fitness but at the same time decrease their agricultural value. On the other hand, out-crossing varieties of rye have much lower capability to evolve, since the same mutation occurs in every generation in a different context, therefore its selection coefficient can oscillate between positive and negative values. To prevent a deterioration of a rye variety, we only need to avoid contamination by pollen (or seeds) of foreign varieties. On the other hand, a variety of wheat (or of other self-fertilising plant) must be continuously subjected to a selection pressure for its useful properties, or it must be from time to time substituted by a new variety. Theoretically, it might also help to prepare seed for sowing by forced outcrossing (as has been recommended by Lysenko), although one may doubt the economical feasibility of this procedure.
The theories of lysenkoists are so crazy that their experiments nobody else has done before, and their reputation is so bad that no well-informed and decent scientist is willing to read their works or repeat their experiments. Despite this, interesting data and observations that might inspire a biologist to construct testable hypotheses might be buried in the body of Michurinist literature. It is rather an ethical problem whether the scientific works of criminals should be ignored or not. It should be, however, argued that by avoiding the topics and the areas of science that were in the centre of attention of these people we actually allow them to shed malice even long after their physical or political death.
I wish to thank Fatima Cvrčková for critical reading of the manuscript. The work was supported by the grant 107/1998 GAUK.
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