Riv.Biol./B.
Forum, (2002) 95, 259-272.
Was Lysenko (partly) right? Michurinist biology in the view of modern
plant physiology and genetics
Jaroslav Flegr
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: flegr@cesnet.cz
Abstract
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 [1], 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 [3]. 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
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 [3] 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 [7]. 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 [10]. 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 [7]. 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.
Wobbled heritability
Visualisation
of hidden genetic polymorphism could have played a role also in the production
of organisms with "wobbled heritability" [3] 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 [11]. Large part of this polymorphism is hidden
under normal conditions, i.e., it does not contribute to observable phenotypes
[12]. Under abnormal conditions, however, some hidden polymorphisms may
manifest on the level of phenotypes of individual organisms in the population
[13]. 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 [3] p. 223; [21] 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 [21] p.
28-29, [22] 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 [22] 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) [22] 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 [10]. 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 [23], 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 [27]) 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 [30] 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 [3] 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 [31], and often also low heritability of polygenic traits
[32]. 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) [32]. 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 [41].
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.
Conclusions
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.
Acknowledgements
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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