Influence of external conditions on the combinatorial processes at agamospermy

doi:10.4236/abb.2013.410A3010

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Advances in Bioscience and Biotechnology, 2013, 4, 89-94 ABB

http://dx.doi.org/10.4236/abb.2013.410A3010 Published Online October 2013 (http://www.scirp.org/journal/abb/)

Influence of external conditions on the combinatorial

processes at agamospermy

Evgenii Vladimirovich Levites, Svetlana Sergeevna Kirikovich

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia

Email: [email protected], [email protected]

Received 10 August 2013; revised 10 September 2013; accepted 10 October 2013

Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the

original work is properly cited.

ABSTRACT

The estimation of the influence of external conditions

on marker enzymes phenotypic classes ratios in aga-

mospermous sugar beet progenies has been carried

out. It has been shown that different ways of flower-

ing sugar beet plant branches isolation lead to differ-

ent ratios of marker enzyme phenotypes in a devel-

oping agamospermous seed progeny. The obtained

data are an additional confirmation of the hypothesis

about the presence of differential chromosomes poly-

teny and its dependence on external conditions.

Keywords: Isozymes; Polyteny; Diminution;

Agamospermy; Sugar Beet

1. INTRODUCTION

Different populational characteristics, such as the degree

of variability in sexual and asexual plant populations [1,

2], were analyzed in numerous experimental and theore-

tical research activities devoted to agamospermy; the le-

vel of apomixis in a plant population [3] was also evalu-

ated. Only in 1994-1996, there were contributions that ini-

tiated studying the mechanisms underlying agamosper-

mous progenies variability [4,5]. According to the con-

clusions made by the authors, the observed ratios are

conditioned by meiosis in polyploid cells of mother plant

capable of agamospermous reproduction. For the cases

when a mother plant was polyploid, such conclusion, on

the whole, can be thought of regular, though a way to

this understanding has turned quite long. In cases when a

mother plant was diploid, the phenotypic classes ratio

was determined by the meiosis that proceeds in tetraploid

cells present as an admixture among the bulk of diploid

cells [5]. For instance, it was shown that, in the agamo-

spermous progeny obtained from diploid sugar beet plants,

the phenotypic ratio on hypocotyl coloring was 11 color-

ed: 3 uncolored; and the phenotypic ratio on isozyme

markers was often equal to 3:8:3, which corresponded to

the tetraploid gametic segregation [5-7]. The process of

such progenies formation was called meiotic agamos-

permy [8].

Isozymes have become a convenient instrument for

studying agamospermy. A wonderful peculiarity of isozy-

mes is their codominant inheritance due to which the hy-

brid plant isozyme spectrum is different from each parent

isozyme spectrum. For instance, one isozyme with fast or

slow electrophoretic mobility, which corresponds to the

genotype of the given locus, is revealed in the electro-

phoregram for the homozygote on the gene controlling

this marker enzyme. But both enzyme allelic variants

(isozymes) and also hybrid isozymes [9,10] are revealed

in the heterozygote. This allows one to reveal all 3 phe-

notypic classes in the progeny of plant heterozygous on

the isozyme locus: two homozygous and one heterozy-

gous. Assisted with isozymes, the case of mitotic agamo-

spermy, at which the progeny developing in diploid sugar

beet plant was monomorphous on the marker enzyme he-

terozygous phenotype, was revealed. This monomorphi-

sm on the heterozygous enzyme phenotype was indica-

tive of the absence of meiotic genome transformations of

cells capable of agamospermous reproduction [11]. At

the same time, the polymorphism of this progeny on the

other marker enzyme indicated the presence of a specific

variability mechanism. To explain this phenomenon, a

hypothesis that implies: a) the presence of differential

chromosome polyteny, i.e. separate chromosome sites

polytenization including those that carry this marker lo-

cus alleles in plant generative organs cells, b) random

equiprobable attachment of two allelic copies (one copy

from each chromosome of two homologous in a diploid

plant) to the nuclear membrane or the nuclear matrix of

the cell before its entering embryogenesis (this allelic

pair then determines the genotype of a developing em-

OPEN ACCESS

E. V. Levites, S. S. Kirikovich / Advances in Bioscience and Biotechnology 4 (2013) 89-94

bryo), c) cell transition to embryogenesis and duplica-

tion of chromosomes attached to the nuclear membrane,

d) first division of embryogenesis and diminution (loss)

of unattached allelic gene copies [12,13] was proposed.

Occasional equiprobable attachment of allelic copies of

chromatide regions is a combinatorial process that im-

plies the existence of a mutual exchange by chromatide

regions among chromosomes.

The data on marker enzymes phenotype ratios in aga-

mospermous progenies of tri- and diploid sugar beet

plants were the confirmation for the statements of this

hypothesis [14,15]. The existence of specific phenotypic

classes ratios in agamospermous progenies of diploid

sugar beet plants has become a weighty argument not

only in favor of the hypothesis about the presence of po-

lyteny, but it also pointed out a mutual exchange of chro-

matide regions among chromosomes in the cell before its

entering embryogenesis [15]. Initially, this hypothesis was

proposed to explain sugar beet seeds phenotypic ratios

obtained by mitotic agamospermy from nucellus somatic

cells or integuments [12,13]. However, it was noticed

that the same hypothesis is applicable also for the analy-

sis of meiotic agamospermy when polyteny occurs in

mother megaspore cells (MMC) [14,16].

To characterize the polytene state of this or that chro-

mosome site, we proposed the term “locus polygeno-

type” and the legend, e.g. FnSm, to describe its allelic

composition, number of chromosomes and chromatides

carrying each of the alleles [14]. The presented legend is

suitable for a diploid cell but, in the case of a tetraploid,

it can be FnFnSmSm.

The polyteny that affects the phenotypic ratio in aga-

mospermous progenies is the result of a big and compli-

cated DNA replication process which, as any enzymatic

process, depends on many conditions. In this connection,

studying the influence of external conditions on the phe-

notypic ratios in agamospermous progenies is of great

interest. Earlier we carried out investigation regarding

this point, and it was shown that colchicine or Triton X-

100 treatment [15,17] affects sugar beet plant pheno-

typic classes ratios.

Earlier, we also obtained the facts that evidence the

non-random distribution of isozyme phenotypes in the

seeds analyzed in the order they set on a sugar beet plant

branch. The non-random phenotypic distribution allowed

us to hypothesize on the influence of external conditions

on the degree of polyteny in the cells capable of entering

embryogenesis and, respectively, on the geno- and phe-

notype ratios of an agamospermous progeny [18]. In the

connection with the above-formulated, it was necessary

to widen the scope of the investigation devoted to the

influence of external conditions on the geno- and pheno-

typic ratios in agamospermous sugar beet progenies, and

that was the aim of this contribution.

2. MATERIAL AND METHODS

The agamospermous progenies obtained from pollen-

sterile sugar beet plants in the pollenless regime were

involved in the investigation. Only plants of phenotype

ms0 and ms1 on Owen classification [19] were left in the

field to create the pollenless regime during flowering;

individual isolators were also used. Two types of isola-

tors were used to estimate the effect of environmental

conditions for each experimental plant; part of plant

branches was covered with an unbleached calico and part

of branches—with parchment isolators.

The ratios of enzyme phenotypic classes of alcohol de-

hydrogenase (ADH1, E.C. 1.1.1.1.), malic enzyme (ME1,

E.C. 1.1.1.40), isocitrate dehydrogenase (IDH3, E.C.

1.1.1.42) were analyzed with the method of electropho-

resis in starch gel with a further isozymes histochemical

staining in electrophoregrams [20,21].

Comparison of marker enzymes phenotypic classes ra-

tios in seeds obtained at various ways of isolation was

carried out using the G-criterion [22].

To determine locus enzyme polygenotypes, the reveal-

ed phenotypic classes ratios were compared to theoretical

calculations obtained for a different polytenized allelic

copies number in heterozygous enzyme loci. Theoretical

calculations were realized, implying the variation of po-

lytenized copies per allele in the interval of 2 - 8.

According to the accepted hypothesis, polymorphism

in agamospermous progenies was determined by the com-

binatorial process based on a random, equiprobable alle-

lic copies attachment to the nuclear membrane [12,13].

This combinatorial process can be described by hyperge-

ometrical probability distribution formulas [23,24]. Ac-

cording to these formulas, the portion of homozygotes is

determined by a number of combinations—two from the

number of the corresponding allelic copies accumulated

as a result of polytenization. For example, if one allele is

presented by n copies in the diploid cell, the other one—

by m copies; then the portion of homozygotes (homoal-

lelic genotypes) on the first allele is determined with the

formula: 22

nnm



, on the second-22

mnm

. Accord-

ingly, the portion of a heterozygous (heteroallelic) geno-

type is determined with the formula 11 2

nm nm

CC C



. These

formulas show the phenotypic ratio in portions from one.

However, these ratios can be expressed also with simple

numbers which are to be determined the following way:

for the first homoallelic genotype—as n(n-1):2, for the

second homoallelic genotype—as m(m-1):2 and for the

heteroallelic genotype—as nm.

The revealed experimental ratios were compared to the

theoretically expected using criterion χ2. The choice of

the polygenotype was made according to the minimal χ2

value.

E. V. Levites, S. S. Kirikovich / Advances in Bioscience and Biotechnology 4 (2013) 89-94

OPEN ACCESS

3. RESULTS AND DISCUSSION

Seed progenies were obtained from all three experiment-

tal sugar beet plants. We consider these progenies as aga-

mospermous on the base of the previous and numerous

data obtained with various methods, which are indicative

of the fact that the growth method we used for pollen-

sterile sugar beet plants in the pollenless regime allows

us to obtain an agamospermous progeny [14-17]. For

example, to prove the agamospermous origin of the pro-

geny, we used unopened buds castration with their fur-

ther isolation [13], natural sampling method consisting in

the analysis of seed phenotypes in the sequence they

were setting on plant branches [18], revealing specific

seed phenotypes ratios explained only by the agamosper-

mous origin of the analyzed progeny [15], obtaining the

genetic proofs for the absence cross-pollination between

growing sterile and semisterile sugar beet plants [17].

Polymorphism on two out of three marker enzymes

—alcohol dehydrogenase (ADH1), malic enzyme (ME1)

and isocitrate dehydrogenase (IDH3) (Table 1)—was re-

vealed in each investigated agamospermous sugar beet

progeny. The presence of polymorphism points out het-

erozygosity of the initial mother plants on the corres-

ponding enzyme loci. The phenotypic ratio on ME1 in

the progeny produced from plant 2 - 7 under the parch-

ment isolator is significantly different from ratio 1:2:1 (χ2

= 7.6; P < 0.05) typical of self-pollinated progenies. Be-

sides, the ratio of the total homoallelic phenotypes por-

tion to that of the heteroallelic phenotype is significantly

different from ratio 1:1 (χ2 = 7.2; P < 0.01) typical of the

progenies produced by self-pollination. This is one more

proof for the agamospermous origin of the progenies we

analyzed. This conclusion allowed us, further on, to eva-

luate the degree of heterozygous locus alleles polyteny in

mother plant cells.

The use of isolators in obtaining sugar beet seed pro-

genies from pollen-sterile plants leads to low seed pro-

ductivity. As a consequence of this, it is not always pos-

sible to obtain big samples (number of seeds) for the ge-

netic analysis.

G-criterion-assisted comparison of the phenotypic

classes ratios of seed progenies obtained at different

ways of isolation, in most cases, did not reveal signifi-

cant differences. This allowed us to integrate the samples

of one and the same plant and to determine marker locus

polygenotypes in mother plant cells on the integrated

samples.

Several values of polygenotypes, but with a different

probability, corresponded to the integrated ratios of phe-

notypes. For instance, several possible polygenotypes—

F4S6 (χ2 = 2.8244); F5S7 (χ2 = 1.9592); F6S8 (χ2 = 1.9120),

out of which the last is the most probable one-corres-

pond to the integrated ratio on ME1 being 22FF:59FS:45SS

in the KA-8 plant progeny. This polygenotype means that

locus Me1 is presented by two chromosomes in mother

plant cells, in one of which allele Me1-F, as a result of

polytenization, is presented by six copies and allele Me1-

S-by eight, respectively. In the same progeny, polyge-

notype F6S5 (χ2 = 0.0044) mostly corresponds to the in-

tegrated ratio on IDH3 (31FF:62FS:21SS).

In the progeny of plant 12 - 2, polygenotype F8S7 (χ2 =

1.6173) mostly corresponds to the integrated ratio ADH1

30FF:46FS:22SS and, in the same progeny, polygeno-

type F8S7 (χ2 = 0.5268) mostly corresponds to the inte-

grated ratio on ME1 equal to 27FF:49FS:22SS.

The sample size of the seeds for ME1 analysis in the

progenies of plant 2 - 7 obtained under different isolators

is also not big. However, the difference in phenotypic

classes ratios is so considerable (G = 220.8436; P <

0.001) that this allowed us to determine the polygeno-

types individually corresponding to each seed group.

Polygenotype F2S2 (χ2 = 2.2) mostly corresponds to the

ratio on ME1, being 1FF:16FS:3SS, revealed in the seeds

obtained under the parchment isolator, and polygenotype

F8S7 (χ2 = 1.4539) mostly corresponds to ratio 10FF:

Ta ble 1. Ratio of marker enzymes phenotypic classes in agamospermous sugar beet progenies and polygenotypes (FnSm) of mother

plant cells capable of embryogenesis.

ADH1 ME1 IDH3

№ of plant Type of isolator

FF:FS:SS FnSm FF:FS:SS FnSm FF:FS:SS FnSm

Parchment 62:0:0 11:35:23 15:40:12

КА-8

Unbleached calico 24:0:0

—

11:24:22

F6S8

16:22:9

F6S5

Parchment 21:22:9 13:27:11 10:0:0

12 - 2

Unbleached calico 9:24:13

F8S7

14:22:11

F8S7

Not analyz.

—

Parchment Not analyz. 1:16:3 F2S2 6:5:3

2 - 7

Unbleached calico 31:0:0

—

10:14:7 F8S7 5:16:5

F6S5

E. V. Levites, S. S. Kirikovich / Advances in Bioscience and Biotechnology 4 (2013) 89-94

14FS:7SS in the seeds from the unbleached calico iso-

lator.

Drastic differences in cell polygenotypes belonging to

the plant branches, being under different isolators indi-

cate, that external (environmental) conditions affect poly-

tenization processes.

It is noteworthy that this influence depends on the ge-

notypic medium, as it was not found in other two plants.

The role of genotypic medium manifests itself also in the

fact that, independent from the type of isolator, the phe-

notypic ratios on ME1 in the progeny of plants KA8 and

12 - 2 are significantly different in the G-criterion (G =

6.9666; P < 0.01) and, hence, these plant polygenotypes

are different (Table 1).

The sample size plays a considerable role in the de-

tection of a weak response to external impacts and, in

case of its (sample size) increase, the differences could,

apparently, have also been revealed in most cases, just as

e.g. in the progeny of plant 12 - 2 in the phenotypic ratio

on ADH1.

Outstanding is the fact that the calculated polyteniza-

tion degree of both locus Me1 alleles in plant 2 - 7 is

considerably lower under the parchment isolator than

that under the unbleached calico. Probably, this is condi-

tioned by the fact that the branch tissues and cells under

the parchment isolator experience a strong stress and

aberration of many biochemical processes as a conse-

quence of the breakdown of light regime, also gas and

temperature exchange. The conditions under the unblea-

ched calico isolator are, probably, a bit close to natural

ones, which contribute more to a normal procedure of bi-

ochemical processes including chromosome sites polyte-

nization.

A more considerable number of polygenotypes, among

which polygenotypes F8S7 (χ2 = 0.0156) and F6S5 (χ2 =

0.1041) are possible, may correspond to the integrated

ratio on IDH3 being 11FF:21FS:8SS in the progeny of

plant 2 - 7 due to a small sample size. Herein, due to a

small sample size, polygenotype F6S5 (χ2 = 0.1041) was

chosen, the same also for ratio 31FF:62FS:21SS on

IDH3 in plant К-8, in which this plant has no differences

in criterion G.

The calculated locus polygenotypes values with an

odd polyteny level, at least of one of the alleles, corre-

spond to the mitotic agamospermy at which the cell,

having not undergone meiotic genome transformations,

enters embryogenesis. This may be, for instance a nucel-

lus or integument cell. At the same time, the phenotypic

ratio that corresponds to polygenotype F6S8, may also

correspond to the other polygenotype: namely F3F3S4S4

which is typical of the mother megaspore cell (MMC). In

this case it is possible to hypothesize about the existence

of such tetraploid MMCs in which one allele is presented

by two chromosomes, each of which, as a consequence

of polytenization, has four chromatides, and the other

allele is presented by the other pair of chromosomes in

which there are only three copies as a result of under-

reduplication. In the entering of such MMC into em-

bryogenesis and a loss of excessive allelic copies, there

emerge diploid gametes developing into individual dip-

loid embryos (plants) at the same ratio as in mitotic aga-

mospermy. The only difference is that, in this case, this

will be a progeny obtained by meiotic agamospermy and

the combinatorial process of the excessive allelic copies

diminution is connected with a combinatorial process of

a two-fold decrease of chromosomes number in the cell.

The obtained data confirm the existing outlook on the

thing that many factors affect the polytenization process.

It was shown with many cytological investigations car-

ried out both in Drosophila and in plants that the level of

chromosome polytenization depends on both internal

conditions (level of inbreeding) [25,26] and external con-

ditions (temperature, daylight length) [27,28]. Our results

and analogous conclusions, unlike those of cited contri-

butions, were obtained only on the base of the data of ge-

netic analysis. Such an unusual approach is justified, on

the one hand, by the impossibility of any other explana-

tion for the specific sugar beet phenotypic classes ratios

and, on the other hand—confirmation of the hypothesis

we use with the data from the field of mammalian ge-

netic, including that of human. Abnormalities based on

the presence of one-parent disomy in an individual of

some chromosome pair or certain regions of homological

chromosomes obtained from only one parent were found

in both human and mice [29,30]. As we mentioned ear-

lier, such phenomenon could appear only as a result of

excessive reduplication of certain regions or whole chro-

matides which further led to an occasional equiprobable

diminution of the excess of genetic material.

The specificity of the problem we investigated consists

in the thing that it is difficult to determine the low po-

lyteny level with the help of cytological methods, but it

may be revealed in embryo sac cells or surrounding tis-

sues only on the base of genetic calculations. Therefore,

our further studies will be aimed at the use of additional

methods for evaluation of the degree of chromosome po-

lyteny in embryo sac cells and surrounding tissues.

The obtained proof for the agamospermous origin of

the progenies we analyzed and additional confirmation of

the hypothesis about the differential chromosomes poly-

teny, and its dependence on external conditions are in fa-

vor of the supposition regarding the role of polyteny in

the record of information about acquired traits.

4. ACKNOWLEDGEMENTS

The authors would like to express their gratitude to Alexander V.

E. V. Levites, S. S. Kirikovich / Advances in Bioscience and Biotechnology 4 (2013) 89-94 93

Zhuravlev for the English version of this article.

REFERENCES

[1] Richards, A.J. (1986) Plant breeding systems. George Al-

len and Uniwin, London.

[2] Kashin, A.S. (2006) Gametophytic apomixis as an unsta-

ble seed reproductive system in flowering plants. Nauch-

naya kniga, Saratov.

[3] Marshal, D.R. and Brown, A.H.D. (1974) Estimation of

the level of apomixis in plant populations. Heredity, 32,

321-333. http://dx.doi.org/10.1038/hdy.1974.41

[4] Maletskii, S.I., Sukhareva, N.B. and Baturin, S.O. (1994)

Sex inheritance in apomictic seedlings of garden straw-

berry (Fragaria ananassa Duch.). Russian Journal of Ge-

netics, 30, 237-243.

[5] Maletskii, S.I. and Maletskaya, E.I. (1996) Self-fertility

and agamospermy in sugar beet Beta vulgaris L. Russian

Journal of Genetics, 32, 1643-1650.

[6] Maletskii, S.I., Levites, E.V., Maletskaya, E.I. and Sha-

vorskaya, O.A. (1997) Autosegregation in the partheno-

genetic offspring of sugar beets (Beta vulgaris L.). Dok-

lady Biological Sciences, 354, 292-293.

[7] Maletskii, S.I., Levites, E.V., Maletskaya, E.I. and Ove-

chkina, O.N. (1998) Autosegregation and linked inheri-

tance in the agamospermous progeny of sugar beet Beta

vulgaris L. Russian Journal of Genetics, 34, 418-424.

[8] Levites, E.V. (2002) New classification of the reproduc-

tion modes in sugar beet. Sugar Technology, 4, 45-51.

http://dx.doi.org/10.1007/BF02956879

[9] Schwartz, D. (1966) The genetic control of alcohol dehy-

drogenase in maize: Gene duplication and repression. Pro-

ceedings of the National Academy of Sciences, 56, 1431-

1436. http://dx.doi.org/10.1073/pnas.56.5.1431

[10] Scandalios, J.G. (1969) Genetic control of multiple forms

of enzymes in plants: A review. Biochemical Genetics, 3,

37-79. http://dx.doi.org/10.1007/BF00485973

[11] Levites, E.V., Shkutnik, T., Ovechkina, O.N. and Malet-

skii, S.I. (1999) Pseudosegregation in the agamospermic

progeny of male sterile plants of the sugar beet (Beta

vulgaris L.). Doklady Biological Sciences, 365, 182-184.

[12] Levites, E.V. (2005) Sugarbeet plants produced by aga-

mospermy as a model for studying genome structure and

function in higher plants. Sugar Technology, 7, 67-70.

http://dx.doi.org/10.1007/BF02942532

[13] Levites, E.V. (2007) Marker enzyme phenotype ratios in

agamospermous sugarbeet progenies as a demonstration

of multidimensional encoding of inherited information in

plants. http://arxiv.org/abs/q-bio/0701027

[14] Levites, E.V. and Kirikovich, S.S. (2011) Autosegrega-

tion of enzyme loci in agamospermous progenies of trip-

loid plants of sugar beet (Beta vulgaris L.). Russian

Journal of Genetics, 47, 836-841.

http://dx.doi.org/10.1134/S102279541107012X

[15] Levites, E.V. and Kirikovich, S.S. (2012) Post-meiotic

apozygotic combinatory process in sugar beet (Beta vul-

garis L.). Advances in Bioscience and Biotechnology, 3,

75-79. http://dx.doi.org/10.4236/abb.2012.31011

[16] Levites, E.V. and Kirikovich, S.S. (2010) Endoreduplica-

tion as a factor of variability in sexual and agamosper-

mous progenies of plants. Developmental Biology: The

Morphogenesis of Reproductive Structures and the Role

of Somatic, Stem Cells at Ontogeny and Evolution. The

Partnership of Scientific Publications KMK, Moscow,

77-80.

[17] Kirikovich, S.S. and Levites, E.V. (2013) Effect of Triton

X-100 on genetic segregation and manifestation of the

trait of mono- and dicotyledonousness in sugarbeet (Beta

vulgaris L.). Russian Journal of Genetics, 49, 517-522.

http://dx.doi.org/10.1134/S1022795413050062

[18] Levites, E.V. and Kirikovich, S.S. (2008) Using the me-

thod of natural samples for studying the variability in su-

gar beat (Beta vulgaris L.) agamospermous seed progeny.

Russian Journal of Genetics, 44, 1296-1303.

http://dx.doi.org/10.1134/S1022795408110070

[19] Owen, F.V. (1945) Cytoplasmically inherited male steril-

ity in sugar beet. Journal of Agricultural Research, 71,

423-440.

[20] Meizel, S. and Markert, C.L. (1967) Malate dehydroge-

nase isozymes of the marine snail Ilyanassa obsolete.

Archives of Biochemistry and Biophysics, 122, 753-765.

http://dx.doi.org/10.1016/0003-9861(67)90185-3

[21] Vallejos, C.E. (1983) Enzyme activity staining. Isozymes

in Plant Genetics and Breeding. Part A. Elsevier, Ams-

terdam, 469-515.

[22] Weber, E. (1986) Grundriss der biologischen Statistik.

Gustav Fischer, Stuttgart.

[23] Haldane, J.B.S. (1930) Theoretical genetics of autopoly-

ploids. Journal of Genetics, 22, 359-372.

http://dx.doi.org/10.1007/BF02984197

[24] Feller, W. (1950) An introduction to probability theory

and its applications. John Wiley and Sons, INC., New

York.

[25] Pokhmel’nykh, G.A. and Shumnyi, V.K. (1984) Nature

of heterochromatin knob regions of maize chromosomes:

2. Nature of changes in the knob regions under inbreed-

ing. Russian Journal of Genetics, 20, 1649-1662.

[26] Bier, K. (1958) Beziehungen zwischen Wachstumsgesch-

nwindigkeit, endometaphasischer Kontaktion und der Bil-

dung von Riesenchromosomen in den Nahrzellen von

Calliphora. Zeitschrift fur Naturforschung, Section A Jour-

nal of Physical Sciences, 136, 80-93.

[27] Nagl, W. (1970) Inhibition of polytene chromosome for-

mation in Phaseolus by polyploidy mitosis. Cytologia, 35,

252-258. http://dx.doi.org/10.1508/cytologia.35.252

[28] Nagl, W. (1973) Photoperiodic control of activity of the

suspensor polytene chromosomes in Phaseolus vulgaris.

Zeitschrift für Pflanzenphysiologie, 70, 350-357.

[29] Yamazawa, K., Ogata, T. and Ferguson-Smith, A.C. (2010)

Uniparental disomy and human disease: An overview.

American Journal of Medical Genetics Part C: Seminars

in Medical Genetics, 154C, 329-334.

http://dx.doi.org/10.1002/ajmg.c.30270

E. V. Levites, S. S. Kirikovich / Advances in Bioscience and Biotechnology 4 (2013) 89-94

OPEN ACCESS

[30] Cattanach, B.M. and Kirk, M. (1985) Differential activity

of maternally and paternally derived chromosome regions

in mice. Nature, 315, 496-498.

http://dx.doi.org/10.1038/315496a0