There is an attempt to explain some evolutionary processes in plants such as saltatory changes on the base of multidimensionality of plant inherited information coding. According to the suggested hypothesis, inherited information is coded by not only a nucleotide sequence but also by chromosome differential endoreduplication. It is supposed that chromosomes compete among each other for the contact with the nuclear membrane, but a change in the endoreduplication degree of various chromosome sites can result in a change of  a competition ability for the contact with a nuclear membrane. A simultaneous increase of chromosome endoreduplication degree of many sites can lead to an increase of nuclear membrane surface and to a change in chromosome competitive interrelations and, respectively, to a change of activity of many genes. Phenotypicaly it may manifest itself as a saltatory change of many traits

Evgenii  Levites

English

Nature Precedings

GENOME STRUCTURAL-FUNCTIONAL PECULIARITIES AFFECTING PLANT 
EPIGENETIC VARIABILITY AND EVOLUTION
Evgenii V. Levites
Institute of Cytology and Genetics, SB RAS, Novosibirsk, Russia, levites@bionet.nsc.ru
Abstract
There is an attempt to explain some evolutionary processes in plants such as saltatory changes on 
the  base  of  multidimensionality  of  plant  inherited  information  coding.  According  to  the 
suggested hypothesis, inherited information is coded by not only a nucleotide sequence but also 
by chromosome differential endoreduplication. It is supposed that chromosomes compete among 
each other for the contact with the nuclear membrane, but a change in the endoreduplication 
degree of various chromosome sites can result  in  a change of  a competition ability  for the 
contact with a nuclear membrane. A simultaneous increase of chromosome endoreduplication 
degree of many sites can lead to an increase of nuclear membrane surface and to a change in 
chromosome competitive interrelations and, respectively, to a change of activity of many genes. 
Phenotypicaly it may manifest itself as a saltatory change of many traits.
Key words:  multidimensionality  of  plant  inherited  information  coding,   endoreduplication, 
nuclear membrane, epigenetic variability, saltatory changes, agamospermy, isozymes
 
Presently most spread ideas about the evolutionary process as a gradual accumulation of 
mutations, their low frequency and negative influence of most mutations on the genotype do not 
allow us to give a  clear  explanation  for the existing  species  diversity  (Schmalhausen,  1946; 
Russell, 1986). Contributions which dwell upon the existence of big complex (saltatory) changes 
of  traits  that  lead  to  evolutionary  transformations  are  a  big  progress  in  the  explanation  of 
evolutionary processes. Here belong such a saltatory change as, e.g., polyploidy, which is the 
genomic (epigenomic) mutation characterized by a change of cell genome number and a wide 
spectrum of  inherited  morphological  and  physiological  traits  (Stebbins,  1950;  Matzke  et  al., 
1999). These changes can be considered as epigenetic due to the absence of changes in DNA 
nucleotide sequences, their high frequency and inheritability. A change of chromosome spatial 
distribution in the cell nucleus (Stegny, 1991) also leads to saltatory changes. New forms that 
appear under saltatory changes differ from those of ancestors in a complex of traits.
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If a wide complex of changes appearing under polyploidisation can be explained by a 
change of  all  genes  dose and the  following dosage  compensation  processes  (excessive  gene 
doses inactivation), then these ideas turn to be insufficient to explain the rest cases of saltatory 
changes. The hypothesis of multidimensionality of plant inherited information coding (Levites, 
2005; 2007) can be one of the basic moments to explain saltatory changes. According to the 
suggested hypothesis, inherited information is coded by not only a nucleotide sequence but also 
by  chromosome  differential  endoreduplication.  Investigations  of  agamospermous  sugar  beet 
progenies  became  the  base  for  this  hypothesis.  Thus,  polymorphism  and  unusual  ratios  of 
phenotypic classes (Levites, 2005, 2007) were revealed in agamospermous sugar beet progenies 
that  arose on  the  base  of  one  parent  genome from cells  that  did  not  undergo meiosis.  The 
hypothesis  that  explains  this  polymorphism  consists  in  the  following.  Chromosomes  are 
endoreduplicated  in  tissue  cells  surrounding  this  embryosac.  Endoreduplication  degree  of 
different sites within one chromosome and homological sites of homological chromosomes can 
be different. Due to this, alleles of heterozygous loci can be presented in a cell by a different 
copies number, i.e. at a different dose. A somatic cell entering embryogenesis by agamospermia 
can have only one copy of every allele. Therefore, excessive allelic copies are eliminated from 
the  genome.  Elimination  of  excessive  chromatide  sites  copies  proceeds  together  with  the 
combinatorial process which consists in the choice of a random pair from a multitude of present 
copies.  Preservation  of  each  pair  of  chromatide  site  copies  in  a  number  of  following 
embryogenetic divisions is determined by the thing that these two copies attach either to the 
nuclear membrane or to the nuclear matrix. If, for instance, one of the alleles of a marker locus is 
endoreduplicated and presented by three copies in the genome and the second one – by only one 
(FFFS), then the theoretical ratio of agamospermous progenies will be 1FF : 1FS. Such ratios 
were observed in our experiments (Levites et al., 1999; 2000).
The hypothesis is based on numerous facts on the effect of colchicine on phenotypic ratio 
in an agamospermous progeny (Levites, 2000 ), existence of diploid sugar beet plants with high 
DNA  content  in  cell  nuclei  (Maletskaya,  Maletskaya,  1999)  capable  of  agamospermous 
reproduction  and dipoid  Allium tuberosum plants  with  endoreduplicational  meiosis  (Kojima, 
Nagato, 1992), high DNA content in nuclei of cell tissues surrounding the embryosac, also in 
cells  of embryosac proper of most plant species number (Ermakov et  al.,;  Morozova,  2002), 
decrease of DNA content to 2C during the first embryonic divisions (Mericle, Mericle, 1970), 
differences in the endoreduplication degree of allelic chromosome sites (Cionini et al., 1982), 
attachment of eucaryotic chromosomes to the nuclear membrane (Mosolov, 1972).
The effect of colchicine (Hassan et al., 1991; Matzke et al., 1999), nutrition level and 
character on DNA content in a cell nucleus (Durrant, Timmis, 1973; Cullis, 1973; Oh, Cullis, 
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2003), mixoploidy of cell populations in a polyploid expressed in the presence of both polyploid 
cells and those of high endoreduplication level in plants (Carvalheira, 2000), also the effect of 
colchicine on the segregation character in plant agamospermous progenies (Levites et al., 2000) 
allow us to consider differential endoreduplication as inherited information coding in the second 
dimension and as a way of registration of inherited information about acquired traits.
To  check  the  hypothesis  on  multidimensionality  of  inherited  information  coding,  the 
effect of detergent TX-100, that can detach chromosome from the nuclear membrane, on the 
expression and inheritance of different traits in wheat and sugar beet was investigated. Triton X-
100 induces inherited changes of plant morphological traits (Makhmudova et al., 2009). Tissue 
differences in sugar beet structural organization of enzyme loci (Vinichenko et al., 2007), which 
may  appear  due  to  the  thing  that  chromosome  sites  carrying  enzyme  loci  are  differently 
endoreduplicated in different tissues, can also be in favor of the suggested hypothesis.
Based on the concept on differential chromosome endoreduplication, also on the known 
facts  about the thing that  chromosomes contact  with the nuclear  membrane  in an interphase 
nucleus, and gene expression depends on this contact,  it  is possible to suggest the following 
hypothesis about the mechanisms of saltatory changes.
Chromosomes are competitive for their contact with the nuclear membrane whose surface 
is limited and tends to minimum according to the laws of physics. Gene functioning can lead to 
an  increase  of  endoreduplication  degree  in  chromosome  sites  carrying  these  genes  and, 
respectively, to higher competition of these sites for their contact with the nuclear membrane. An 
increase of endoreduplication degree in a small number of loci may not affect a genome size and 
that  of  nuclear  membrane  surface.  If  the  number  of  endoreduplicated  regions  exceeds  some 
critical value, then it may lead to an increase of the nuclear surface and, as a consequence, to a 
new activity ratio of different loci expressed as a saltatory change. If such processes affect cells 
of generative organs, then a transfer of saltatory changes to the next generation is possible. The 
Triton X-100-induced inheritance of different traits  that  we observed indicates  the thing that 
changes in nuclear membrane-chromosome interaction and, obviously, states of membranes are 
inherited. We referred Triton X-100-induced changes to those of epigenetic.
The suggested hypothesis well accords with the ideas about a huge role of dosage effects 
in genome functioning. Dosage effects can be considered as an evolutionarily established, at the 
supermolecular level, an action of chemical law according to which the rate of chemical reaction 
is determined by the concentration of agents entering into it.  Gene dosages, in this case, are 
analogous to agent concentrations in elementary chemical reactions.
Comparing the two reasons for saltatory changes – increase of genome dosage and a 
change of chromosome spatial  distribution – it  is  possible  to hypothesize that  the change of 
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chromosome  spatial  distribution  is  also  determined  by  dosage  effect,  as  there  may  be 
competition between and among chromosome sites having a different endoreduplication degree 
for the contact with the nuclear membrane. A change of chromosome spatial distribution and 
gene expression may arise as a result of changes of interchromosome competitive abilities for the 
contact with the nuclear membrane.
The suggested hypothesis is based on the fact that dosage relations play a huge role in 
genome  reorganization;  they,  due  to  their  dependence  on  environmental  conditions,  are  an 
effective  way of epigenetic  changes  and a powerful  acceleration  mechanism of evolutionary 
process.
This research was financed with Grant N 99 on SB RAS integrative project  for 2009-2011. 
I  would  like  to  express  my  huge gratitude  to  Alexander  V.  Zhuravlev,  SB RAS Executive 
Interpreter.
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Cell cycle during development of male and female gametophytes

Colchicine-induced heritable variation in cell size and chloroplast number in the leaf cells of inbred ryegrasses (Lolium perenne,

Comparison of homologous polytene chromosome in Phaseolus cocineus embryo suspensor cells: morphological, autoradiographic and cytophotometric analyses //

Cytochemical investigation of DNA during ovule development and early embryogenesis

Diplosporous embryo-sac formation and the degree of diplospory in Allium tuberosum // Biomedical and Life Sciences,

DNA differences between flax genotrophs

Factors of evolution (theory of stabilizing selection)

Genetic control of environmentally induced changes in Linum //

Labile DNA sequences in flax identified by combined sample representational difference analysis (csRDA) // Plant Molecular Biology,

Marker enzyme phenotype ratios in agamospermous sugarbeet progenies as a demonstration of multidimensional encoding of inherited information in plants // on-line: http://arxiv.org/abs/q-bio/0701027 10.

New approach to the solving of the problem of chromosomes space arrangement in the interphase nucleus (polar model of interphase nucleus)

Nuclear DNA complement in young proembryos of barlei

Plant polytene chromosomes //

Rapid structural and epigenetic changes in polyploidy and aneuploid genomes //

Sugarbeet plants produced by agamospermy as a model for studying genome structure and function in higher plants

Systemic genome reorganization under speciation // In: Problems of genetics and evolution theory.

The nuclear DNA mass variability in embryo root cells of sugarbeet

Tissue distinctions in the organization of sugar beet locus Adh1 // Achievements and problems of genetics, breeding and biotechnology (Collection of paper).

Triton X-100 induces heritable changes of morphological characters in Triticum aestivum

Variation and Evolution in Plants // New York: Columbia University. N a t u r e P r e c e d i n g s : h d l : / n p r e

Genome Structural-Functional Peculiarities Affecting Plant Epigenetic Variability and Evolution

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Genome Structural-Functional Peculiarities Affecting Plant Epigenetic Variability and Evolution

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