1062-3590/05/3203- © 2005 Pleiades Publishing, Inc.0234

Biology Bulletin, Vol. 32, No. 3, 2005, pp. 234–239. Translated from Izvestiya Akademii Nauk, Seriya Biologicheskaya, No. 3, 2005, pp. 287–293.Original Russian Text Copyright © 2005 by Klimov, Astakhova, Alieva, Sal’nikov, Trunova, Morozova, Semenov.

Stability of winter wheat yield depends on manyfactors, among which the genetic factor determiningstability processes holds the leading position(Zhuchenko, 1988). The genetic system of higherplants includes blocks of co-adapted genes and otherintegrated gene complexes, which determine the pat-tern of adaptive characters. Cytoplasmic determinants,i.e., the set of all extrachromosomal hereditary ele-ments of the cell (plasmon), also have considerableeffect on the pattern of ontogenetic adaptation of plants.The genetic systems of the cytoplasm control manifes-tation of numerous economically important charactersin ontogeny. It deserves further investigation as a poten-tial factor of genetic variability of flowering plants(Wilkie, 1964). For instance, Cal and Obendorf (1972)demonstrated the role of the maternal cytoplasm indetermination of maize

F

1

hybrid resistance to frost andlow temperature. According to Khristolyubova (1974),differential winter hardiness of seedlings of wheat andgoatgrass as well as their hybrids was due to the prop-erties of mitochondria.

Production of complex taxonomically differenthybrids combining useful growth properties of cerealspecies or even genera is a promising approach to pro-duction of novel plant types with higher hardiness, pro-duction, and efficiency of plastic processes (Meister,1927; Vavilov, 1935; Dorofeev, 1981; Shulyndin,1981). In the present-day practice, such selection canbe illustrated by production of wheat–rye, wheat–goat-grass, and alloplasmic forms.

Alloplasmic wheats produced by backcrossing rep-resent a novel synthetic type of plants where the

nucleus of

T. aestivum

is functioning in the alien cyto-plasm. Investigation of such hybrids has both theoreti-cal and practical importance (Harris, 1970; Sager,1974; Semenov, 1978, 2000; Low

et al

., 1978; Pao andFleming, 1980; Kofoid and Maan, 1980; Tymms andScott, 1990). Production of nucleocytoplasmic geneticsystems opens new possibilities to change functioningand expression of the nuclear genome by the replace-ment of the cytoplasm as a component of the system.Such systems include alloplasmic wheat

T. aestivum

with the cytoplasm of wild cereals. Such forms wereproduced at the Russian University of Peoples’ Friend-ship; the best of them were put through competitive andfield tests (Semenov, 2000). The alien cytoplasm couldprovide for a set of important biological and economi-cal characters absent in the parental wheat cultivars.Studies of biological and physiological properties ofalloplasmic wheats produced at the Russian Universityof Peoples’ Friendship were initiated in 1976 and stillgo on. In 1976–1981, morphogenesis of the alloplasmichybrid and parental forms of winter wheat cultivarIgen-3 and

Aegilops

was studied. From 1998, the effectof the alien cytoplasm of

Aegilops

on winter hardinessand biological production of the reciprocal hybridsbetween an alloplasmic hybrid (

T. aestivum

genomeand

Ae. ovata

cytoplasm) and winter wheat cultivarsStuart and Liwilla.

The data presented below illustrate the analysis ofthe cytoplasm–nucleus interactions in alloplasmicwheats at the level of the organism and lower structurallevels.

Effect of Alien Cytoplasm of Goatgrass on Biological and Physiological Properties of Alloplasmic Wheats

V. V. Klimov*, N. V. Astakhova*, G. P. Alieva*, E. B. Sal’nikov*, T. I. Trunova*, Z. A. Morozova**, and O. G. Semenov***

* Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul. 35, Moscow, 127276 Russiae-mail: ifr@ippras.ru

** Biological Faculty, Moscow State University, Vorob’evy gory, Moscow, 119992 Russiae-mail: wmur@hitbox.24

*** Russian University of Peoples’ Friendship, ul. Miklukho-Maklaya 6, Moscow, 117198 Russiae-mail: sog480@yandex.ru

Received November 16, 2004

Abstract

—Long-term studies of the cytoplasm–nucleus interactions in alloplasmic hybrids with the nucleus of

Triticum aestivum

functioning in the alien cytoplasm of

Aegilops ovata

are reviewed. The interaction of heter-ologous genome and cytoplasm affects the balanced mechanisms of developmental control of the parentalforms. The changes are observed at all levels of physiological and morphological processes. Alloplasmicwheats produced by backcrossing represent a novel type of synthetic plant different from the

T. aestivum

typeand are of great interest to breeders.

BOTANY

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EFFECT OF ALIEN CYTOPLASM OF GOATGRASS 235

MATERIALS AND METHODSExperiments were carried out on self-fertile winter

alloplasmic hybrid of wheat

T. aestivum

(cultivar Igen-3)with the cytoplasm of

Ae. ovata

produced byMedvedeva and Semenov (1969, 1972) at the Instituteof Applied Molecular Biology and Genetics.

Four reciprocal hybrids of foreign cultivars Stuartand Liwilla and self-fertile alloplasmic wheat hybridproduced in 1969 as a source of

Aegilops

cytoplasmwere used. Thus, the studied hybrids and cultivars hadeither monogeneric nucleus and plastome (genome andplasmon) from

T. aestivum

or had an alien plastome(plasmon) from

Ae. ovata.

These forms were used toreveal the effect of the alien cytoplasm on winter hardi-ness and certain aspects of biological production of thehybrids.

Morphogenesis of the alloplasmic hybrid as well asof winter cultivar Igen-3 and

Aegilops

were studied in1976–1981 at the experimental plot of the Institute ofApplied Molecular Biology and Genetics (YamskoiState Farm, Domodedovsk District, Moscow Region).Starting from the stage of seed swelling, 10–20 plantsof compared forms were taken from experimental plotsand subjected to complete morphological analysis(Serebryakova, 1961). The plant habitus and its lifeform is determined by the following factors: the rhythmof the phyllogenetic activity of the apical meristem ofthe gemma; the rate and rhythm of transformation ofthe metameric meristem elements into mature function-ing organs (leaf primordia, into leaves; axillary buds,into shoots; and intercalated disks, into nodes and inter-nodes); and overall level and specific pattern of bio-rhythmic growth of the plant as a whole. These pro-cesses go differently in wheat and

Aegilops.

Studies of plastic processes in wheat cultivar Igen-3,the hybrid, and

Aegilops

allowed us to determine spe-cific cytoplasm–nucleus interaction in the studied allo-plasmic wheat as well as its effect on the rhythm ofmorphogenetic processes.

Starting from 1998, complex physiological studiesof the dependence of winter hardiness on the plasmonas well as of production on the genome–plasmon inter-actions were carried out in the Laboratory of WinterHardiness (Timiryazev Institute of Plant Physiology,Russian Academy of Sciences). These studies were per-formed on reciprocal hybrids of winter wheat cultivarsStuart and Liwilla as well as on the alloplasmic hybrid,the morphogenesis of which is described below.

Plants were grown in boxes filled with sod-podzolsoil under natural conditions of an open greenhouse. Insome experiments, the plants were preliminarily cold-hardened. In this case, tillered plants were left in non-heated glass greenhouse at naturally decreasing tem-perature.

In some experiments, plants were grown in specialvegetation chambers in Hoagland-Arnon nutrient solu-tion N1. Cold-hardening was performed as describedfor the soil culture.

Winter hardiness of plants was evaluated by directfrosting in a climatic chamber KTLKA-1500 (Ger-many) at constant temperature for 1 day, defrosting at0

°

C for 1 day, subsequent growth in a vegetation cham-ber, and counting the proportion of survived plants.

Winter hardiness of leaf tissues was evaluated fromelectric conductivity of water extracts from the tissuesof frozen and boiled plants as described elsewhere (Kli-mov

et al

., 2000).

Gas exchange evaluations included the rate of thereal CO

2

assimilation determined during the transitionfrom light to darkness and the rate of dark respirationdetermined 10–15 min after switching off the light. Thereal CO

2

assimilation represented an apparent CO

2

assimilation plus respiration in the light, which wasdetermined from the CO

2

“release” during the first 3 to5 min after the light was switched off. The measure-ments were carried out on an open device with a URAS2T infrared gas analyzer (Hartmann and Braun, Ger-many) and the corresponding equipment of the samecompany. The detailed description of the technique canbe found elsewhere (Klimov, 2003).

Tables present the arithmetic means of three mea-surements and their standard errors. Each measurementwas made on 4–10 tillered plants. Data interpretationsrely on the differences between the experimental vari-ants significant at the 95% confidence level.

RESULTS AND DISCUSSION

Morphogenetic analysis of the alloplasmic hybrid.

Before we proceed to morphogenesis of the alloplasmichybrid, let us briefly describe the morphogenesis ofwheat and the cytoplasm donor

Ae. ovata.

CultivarIgen-3 and the hybrid are winter crops, while

Aegilops

is a spring form.

The morphogenesis of winter wheat was describedin detail elsewhere (Morozova, 1986; Morozova andSandukhadze, 2002). In autumn, winter wheat demon-strates relatively active growth of all organs at the initialdevelopmental stages. A relatively complex vegetativesphere is formed in winter wheat in autumn; plants haveone to five stools and considerable number of auxiliarybuds. When spring vegetation starts, plants rapidlycome to the generative phase. Rudimentary spikes startformation on the main shoot and stools; generative pri-mordia appear on the apical cone; and all buds becomemixed.

Aegilops

is a spring crop with slow development inearly ontogeny, while it accelerates at later stages. Budsremain viable for a long period and are slowly trans-formed into shoots.

Aegilops

demonstrates asynchro-nous transition of the shoots to the generative phase andthe absence of the main shoot dominance over shootand bud development typical for wheat. In the field, theplants demonstrate considerable variability by vigorand tillering.

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The alloplasmic hybrid is a winter crop. Compari-son of growth, development, and morphogenesis in thehybrid and parental forms exposes the effect of

Aegilops

cytoplasm on the whole rhythm of morpho-genesis in the hybrid. During autumn vegetation, thehybrid resembled wild plants; they had narrow leaves,although the apical cones were usually larger as com-pared to wheat (Table 1). The growth rate of the hybridin autumn was similar to that of wheat. In spring, par-ticularly, during the generative phase, the cytoplasm–nucleus interaction became even more pronounced.Hybrid plants with large wide leaves became more vig-orous as compared to wheat. Both the hybrid and wheatstarted the generative phase simultaneously; however,larger apical cones in the hybrid were maintained. Atthe background of the wheat type of development, thecytoplasm had a sharp effect on the regulation of forma-tion and development of the generative sphere. Thedevelopment of the generative sphere of the main shootand stools was clearly unbalanced. The transition to thegenerative phase was elongated. Growth of primordialspikes lagged behind growth of their main shoot. Earformation on shoots was elongated and unsynchro-nized.

Field populations of the alloplasmic hybrid at theinitial stages demonstrated different degrees of interfer-ence of the initial forms as indicated by various aspectsof structural formation of the plants.

The cytoplasm–nucleus interaction between thewheat genome and

Aegilops

cytoplasm disbalancedformer morphogenetic mechanisms intrinsic to theparental forms. The rhythm and timing of the vegetativesphere formation were similar at the initial stages in thehybrid and wheat. Late ripeness of the hybrid was dueto the alterations of the morphogenetic control mecha-nisms during formation of generative organs. Forma-tion of the generative sphere of the plant decelerated.Apparently, this affected the coordinated developmentof the whole organism and resulted in decelerated agingof the lower parts of shoots, high viability of buds, andaltered pattern and rhythm of their own morphogenesis.

Altogether, this formed a plant type different fromwheat.

Analysis of winter hardiness and biological produc-tivity of reciprocal hybrids of alloplasmic wheats andwinter wheat cultivars Stuart and Liwilla.

Experimentson winter hardiness of the reciprocal hybrids were car-ried out on more genetically complex objects as com-pared to the previous experiment. In two hybrids (Stu-art

×

alloplasmic wheat and Liwilla

×

alloplasmicwheat), the nucleus and plastome (genome and plas-mon) belonged to different cultivars of the same species

T. aestivum

. Two more hybrids (alloplasmic wheat

×

Stuart and alloplasmic wheat

×

Liwilla) had alien plas-tome (plasmon) of

Ae. ovata.

The results of the experi-ments are shown in Tables 2 and 3. Before proceedingto interpretation of the obtained data, note the clearlymanifested role of the winter wheat genome. All winterhardiness tests demonstrated the difference of the recip-rocal hybrids involving Stuart and Liwilla cultivars.

According to direct freezing tests, winter hardinessof the hybrids with the alien cytoplasm was lower ascompared to the normal hybrids involving the genomeof winter wheat cultivar Liwilla (Table 2). However, nosuch difference was observed for the hybrids involvingcultivar Stuart; their winter hardiness was higher andthey withstood the freezing temperature of

–

14

°

C with-out damage. The integral pattern of the damaging effectof freezing was inferred from the proportion of plantsthat survived and produced fertile progeny at the sametime. The proportion of tillered hybrids with the aliencytoplasm was lower as compared to the normalhybrids for both parental cultivars of winter wheat. Thedifference in this index was more pronounced in culti-var Liwilla. Similar data were obtained for winter har-diness of the hybrids using the method of biomassincrement after freezing. This test also demonstratedlower winter hardiness of the hybrids with the aliencytoplasm. This effect was particularly pronounced inthe hybrids involving Liwilla cultivar, where it reached60%.

In addition to these tests, we used other methods toevaluate winter hardiness of the hybrids. For instance,

Table 1.

Apical cone size in cultivar Igen-3 and alloplasmic hybrid

Forms and shoots Igen-3 cultivar Alloplasmic hybrid

Shoots Cone length, mm Cone width, mm Cone length, mm Cone width, mm

Main shoot 0.46 0.22 0.54 0.22

Secondary shoots:

Coleoptile shoot 0.26 0.20 0.23 0.19

1st leaf shoot 0.28 0.19 0.40 0.24

2nd leaf shoot 0.50 0.21 0.46 0.26

3rd leaf shoot 0.57 0.23 0.50 0.26

4th leaf shoot 0.45 0.20 0.54 0.26

5th leaf shoot 0.46 0.24 0.63 0.28

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it was evaluated from the capacity of plants to maintainphotosynthesis and respiration after first autumn frosts.The ratio of photosynthetic rate at light saturation to therate of dark respiration was used as a test for winter har-diness. This ratio determined at near zero temperatureswas previously used as a test for frost hardening capac-ity of plants (Klimov and Trunova, 1999; Klimov,2003). Thus evaluated winter hardiness did not signifi-cantly differ for the hybrids involving cultivars Stuartand Liwilla. At the same time, the hybrids with the aliencytoplasm had notably lower winter hardiness in thecase of hybrids involving both Stuart and Liwilla culti-vars (by 0.18 relative units).

Two complementary tests (visual evaluation of frostdamage and evaluation of electric conductivity of leaftissues affected by frost) were used to estimate winterhardiness of the hybrids involving Liwilla cultivar. Thehybrids with the alien cytoplasm had a higher winter

hardiness as compared to the normal hybrids, whichwas confirmed by visual differences in frost damage(by one point out of five, i.e., by 20%) and by electricconductivity of tissues (the differences were not signif-icant since only nonfrozen leaf parts were analyzed andtheir proportion in the alloplasmic wheats with the aliencytoplasm was lower as compared to the normalhybrids).

Overall, a steady pattern was revealed despite differ-ent nuclear genomes of winter wheat were used to pro-duce the alloplasmic hybrids as well as despite differenttests for winter hardiness: the hybrids with the aliencytoplasm of

Aegilops

had a lower winter hardinessthan the normal hybrids. In other words, the cytoplasmof spring

Aegilops

decreased winter hardiness of winterwheat. Analysis of biological productivity of the allo-plasmic hybrids is shown in Table 3. Dark respirationrates were indistinguishable in the hybrids with the

Table 2.

Winter hardiness of reciprocal hybrids of alloplasmic wheats and wheat cultivars Stuart and Liwilla according todifferent tests

Parameters of winter hardiness accordingto different tests

Cytoplasm of

Aegilops

Wheat (Stuart)

Aegilops

Wheat (Liwilla)

Survival rate of regrown prehardened plants after frosting at – 14

°

C for 24 h 100 100 34 78

Proportion of eared plants in total number of regrown after frosting

1

7 23 0 71

According to plant regrowth after frosting

2

27 32 26 87

According to the aftereffect of low temperature on CO

2

exchange in plants

3

1.04 1.24 1.06 1.24

According to electric conductivity of water extracts from frozen leaf tissues

4

– – 83 89

According to visible damage of the above-ground part of plants

5

– – 2.8 3.8

Notes:Minus sign indicates the absence of data.

1

Winter hardiness = (number of eared plants/total number of plants prehardened at –3, –8, and –14

°

C for 24 h that regrew afterfrosting), %.

2

Winter hardiness = (weight of plants regrown after frosting at –10

°

C/weight of plants regrown after nondamaging frosting at –6

°

C), %.

3

Winter hardiness = (rate of the real CO

2

assimilation at light saturation/dark respiration rate in frost-hardened plants as measuredat 20

°

C); both values were determined as mg CO

2

per g leaf dry weight per h.

4

Winter hardiness = [(

E

D

–

E

L

)/

E

D

], %, where

E

is electric conductivity of boiled (

E

D

) or frozen (

E

L

) leaf tissues.

5

Winter hardiness = rank of visible damage of the above-ground part of plants: 5 points, intact plant; 4 points, damaged top of the1st leaf; 3 points, considerable damage of the 1st leaf; 0 points, no damage.

Table 3.

Biological productivity and its components in reciprocal hybrids of alloplasmic wheats and wheat cultivars Stuartand Liwilla

Parameters

Cytoplasm of

Aegilops

Wheat(Stuart)

Aegilops

Wheat(Liwilla)

CO

2

exchange of frost-hardened plants as determined at 20

°

C

Dark respiration, mg CO

2

per g leaf dry weight per h 5.0 5.1 6.4 6.3

Visible photosynthesis, mg CO

2

per g leaf dry weight per h 0.17 1.23 0.37 1.53

Visible photosynthesis of the whole plant, mg CO

2

/day 0.13 0.50 0.23 0.50

Mean dry weight of one shoot, mg 370 527 859 342

Number of stools per plant 3.72 3.44 3.43 3.75

Whole plant dry weight, g 1.38 1.81 2.95 1.28

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alien and normal cytoplasm; in the alloplasmic hybridsinvolving cultivar Liwilla they were higher as com-pared to the hybrids involving cultivar Stuart. Great dif-ferences in the visible photosynthetic rate wereobserved: in the alloplasmic hybrids with the aliencytoplasm it was 4 and 6 times lower as compared to thecommon hybrids. This can be attributed to a clearlygreater frost damage of the photosynthetic apparatus inthe hybrids with the alien cytoplasm of

Aegilops.

As aresult, photosynthesis was inhibited in these hybrids at

20°C

and the effect of negative temperatures was morepronounced. Similar although not so sharp differencesbetween the alloplasmic hybrids were demonstrated bycalculation of the whole plant photosynthetic rate. Notehowever that the presented values of CO

2

exchangeresult from its inhibition by frost, while an inverse trendto high gas exchange rate in the alloplasmic hybridswith the

Aegilops

cytoplasm could be observed undertemperature conditions optimal for growth. The indicesof biological productivity such as dry weight of oneshoot, number of stools, and plant dry weight variedambiguously in the alloplasmic hybrids involvingLiwilla (they were higher in the hybrids with the

Aegilops

cytoplasm) and Stuart (they were higher in thehybrids with the normal cytoplasm) cultivars.

Thus, introduction of the alien cytoplasm of

Ae. ovata

into the cell of soft winter wheat(

T. aestivum

) decreased its winter hardiness, whichcould still be compensated by the capacity for springregrowth (Semenov, 2000).

Physiological parameters in the studied reciprocalhybrids depend on the combined effect of both theirplasmon and genome. The response of the hybrids withthe Stuart genome and the cytoplasm of either

Aegilops

or wheat differed from the response of the hybrids withthe Liwilla genome. Overall, a relatively stable patternwas revealed: the hybrids with the alien cytoplasm of

Aegilops

had a lower winter hardiness as compared tothe hybrids with the wheat cytoplasm. Still, such com-bination of winter hardiness and biological productivityin the alloplasmic hybrids can be optimal for the maxi-mum yield in conditions of the global warmingobserved in the northern hemisphere in winter.

The obtained data demonstrate a new synthetic planttype produced by backcrossing, alloplasmic wheats,different from the wheat type. The cytoplasm–nucleusinteraction of the

T. aestivum

genome and

Ae. ovatacytoplasm affects the balance of former mechanisms ofdevelopmental control specific for the parental formsand establishes new ones. This model represents a liv-ing laboratory where new plant types are produced. Thechanges are observed at all levels of both physiologicaland morphological processes. Selection can use and isactually using the benefits of this plastic process to gen-erate more productive forms.

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