Specific features of meiosis in the Siberian fir (Abies sibirica Ledeb.) artificial populations

ISSN 1062-3604, Russian Journal of Developmental Biology, 2007, Vol. 38, No. 4, pp. 246–252. © Pleiades Publishing, Inc., 2007.Original Russian Text © E.V. Bazhina, O.V. Kvitko, E.N. Muratova, 2007, published in Ontogenez, 2007, Vol. 38, No. 4, pp. 299–306.

246

In the case of artificial planting, plants are adaptedto new life conditions. Analysis of the development oftraits and adaptive reactions in new plantings is essen-tial for elaboration of the general theory of ontogenyand study of the mechanisms underlying realization ofthe genetic program of ontogenetic adaptation. Studiesof animals and plants during artificial breeding haveshown that new life conditions often exert stress effectsand different organisms respond to them in differentways.

Of great interest in this respect is the study of meio-sis in cultured species. Meiosis is one of the most vul-nerable and susceptible to the environmental factorsperiods of ontogeny (Christiansen, 1960; Mergen andLester, 1961; Kantor and Chira, 1965; Eriksson, 1968;Ekberg et al., 1972; Kozubov, 1974; Romanova andTret’yakova, 2005). At the same time, it is controlled byhundreds of genes (Golubovskaya, 1975, 1985; Sosni-khina et al., 1994a, 1994b; Bogdanov, 2003). Chromo-some behavior in meiosis as a function of environmen-tal conditions is also determined genetically (Shkutina,1975).

The results of studies of several coniferous speciesunder the conditions of introduction suggest that meio-sis proceeds in the direction of stabilization, on the onehand, and high degree of its disturbance, on the other(Muraya et al., 1988; Butorina et al., 1989; Gavrilovand Butorina, 2005). So far, meiosis has been insuffi-ciently studied in artificially planted trees. The aim ofthe present work was to study meiosis in the Siberian fir(

Abies sibirica

Ledeb.) cultures in the arboretum of theSukachev Institute of Forest.

MATERIALS AND METHODS

Studies were carried out on Siberian fir trees grow-ing in the arboretum of the Sukachev Institute of Forest.The arboretum is located in the forest-park zone ofAkademgorodok (Krasnoyarsk) on a high (275 mabove sea level) terrace of the left Yenisei bank on theplace of an islet region of sod-cereal mountain steppe(Mamaev et al., 1993). The climate of this region issharply continental and the arboretum is referred to theEast-Siberian variant of the south-taiga subzone. Thesoil in the arboretum is sod-carbonate, weakly alkaline(close to neutral pH) with low humus content and nitro-gen mobility.

Siberian fir saplings were brought to the arboretumof the Institute of forest from the nursery of theResearch Institute of Fruit Growing of Siberia (Bar-naul) in 1977. Saplings were obtained from seeds of thelocal (Altai) origin (Loskutov, 1993). The selected treesmay be referred to the best category according to thecomplex of economically important traits, such as habi-tus, seed production, resistance against diseases, etc.

Studies of meiosis were carried out during threeyears (2002–2004). The developing male generativebuds were used for these studies. Microstrobils werefixed daily from April 23 until May 13. The materialswere kept in an alcohol-acetic acid mix (3 : 1) for oneto two days and then stored in 70% alcohol and stainedby acetohematoxylin. A total of 14256 microsporocytesat different stages of meiosis were analyzed, as well as11170 developing pollen grains. The total numbers ofnormal meiocytes and cells with various anomalies ofchromosome behavior were counted at each stage ofmeiosis. Studies were performed under an MBI-6microscope and phases of meiosis were photographed

GAMETOGENESIS

Specific Features of Meiosis in the Siberian Fir(

Abies sibirica

Ledeb.) Artificial Populations

E. V. Bazhina, O. V. Kvitko, and E. N. Muratova

Sukachev Institute of Forest, Siberian Branch of the Russian Academy of Sciences, Akademgorodok, Krasnoyarsk, 660036 Russia

E-mail: [email protected]

Received February 27, 2006; in final form, May 3, 2006

Abstract

—Meiosis was studied in the Siberian fir (

Abies sibirica

Ledeb.) at the arboretum of the SukachevInstitute of Forest. Specific features of meiosis in planted trees have been described. Both general and specifictypes of irregularities have been identified. The range of irregularities under the arboretum conditions was muchwider than in natural ecosystems.

DOI:

10.1134/S1062360407040078

Key words

: conifers, artificial reproduction, Siberian fir, microsporogenesis, meiosis, chromosomes, meioticanomalies.

RUSSIAN JOURNAL OF DEVELOPMENTAL BIOLOGY

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SPECIFIC FEATURES OF MEIOSIS 247

on a Mikrat film. In addition, some preparations wereanalyzed under an Axioskop 20 microscope (CarlZeiss, Germany) with a videotape recorder connectedto a Sony Multiscan G200 monitor.

RESULTS

The results obtained suggest that meiosis in theSiberian fir started and terminated in spring both in thearboretum and in natural populations. During the thirdten-day period of April, rounded microsporocytes

(mother cells of pollen) at prophase I could be seen inthe microsporangia (Fig. 1). Their diameter is, as a rule,1.5 times that of surrounding tapetum cells: 57.3

±

1.12and 43.3

±

0.81

µ

m, respectively. All stages of prophaseI could be found in fir trees growing in the arboretum:leptotene, zygotene, pachytene, diplotene, and diakine-sis. The meiocytes contained up to four nucleoli, one ofwhich was, as rule, larger, and better stained. In theSiberian fir growing both in the arboretum and naturalplantings, meiosis proceeds according to the classicaltype with the formation of 12 bivalents, which regularly

(j) (k) (l)

(g) (h) (i)

(d) (e) (f)

(a) (b) (c)

Fig. 1.

Meiotic division and pollen grain formation in the Siberian fir at stages: (a) leptotene, (b) pachytene, (c) diplotene, (d) diak-inesis, (e) metaphase I, (f) anaphase I, (g) telophase I, (h) prophase II, (i) metaphase I, (j) anaphase II, (k) tetrad of microspores,(l) microspore. Here and in Figs. 2 and 4, magnification: 10

×

100.

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BAZHINA et al.

disjoin to the opposite poles (Fig. 2a). The morphologyof bivalents is determined by the position and numberof chiasmata. Most studied trees, like in the naturalplantings, had up to three chiasmata per bivalent (theirnumber reached five only in one case). The fir treesgrowing in the arboretum possessed all previouslydescribed species specific features: asynchrony, rapidprogression through telophases I and II, and distinctlyidentifiable prophase II (Bazhina et al., 2003).

Asynchronous development of meiocytes is, on thewhole, inherent in coniferous plants (Kozubov, 1974;Rozhdestvenskii, 1974; Nekrasova and Ryabinkov,1978; Muraya et al., 1988; Muratova, 1995), includingthe Siberian fir. However, if in the natural fir popula-tions microsporocytes at different stages of meiosis I orII occurred in the same microsporangium (Bazhinaet al., 2003), in the arboretum, cells at prophase I, tet-rads, and even developing pollen grains could be found(Fig. 2b). In the microsporangia located in the lowerstrobil part, meiosis proceeded at a higher rate than inthe upper part.

Distinctly identifiable prophase II is a specific fea-tures of the Siberian fir and, possible, of the genus

Abies

as a whole (Mergen and Lester, 1961). It is absentin other coniferous species and metaphase II follows,

like, for example, in the Scots pine (Butorina et al.,1982; Muratova, 1995).

We established that meiosis in the Siberian fir underthe arboretum conditions was characterized by signifi-cant duration: 18 to 21 days in different years (Fig. 3).In 2002-2003, the first meiotic divisions were recordedalready on April 24, while in 2004, only on May 5. Thisdifference in the timing of divisions was, possibly, dueto the long and cold spring 2004. The postmeioticdevelopment of pollen continued until May 11–13 in2002–2003, while in 2004, meiosis still proceeded onMay 13. At the same time, in the natural plantings, mei-osis started later (on May 5–7) and proceeded very rap-idly: within one to two days (Bazhina et al., 2003).

In the arboretum, in addition to the normal orienta-tion of spindles, their parallel and linear arrangementswere also seen at different stages of meiosis II. The fre-quency of meiocytes with such features amounted to0.3–20.5% in different trees and in different years.Some authors believe (Mok and Peloquin, 1975; Buto-rina et al., 1985a) that in meiosis II, the spindles shouldbe normally oriented at an angle of 60

°

to each other.Parallel orientation of the spindles could lead to fusionof the groups of chromosomes on the opposite polesand formation of pollen grains with diploid chromo-some sets. However, the fusion of parallel spindles

(d) (e) (f)

(a) (b) (c)

Fig. 2.

Specific features of meiosis during microsporogenesis of the Siberian fir in the arboretum: (a) diakinesis, (b) asynchronousdevelopment of microsporocytes, (c, d) chromatin agglutination and ejection of nucleoli in the cytoplasm, (e) bridge at anaphase IIpreserved from the first division (f) union of nuclei in dyad.


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depends to a great extent on the influence of environ-mental factors (Veileux et al., 1982).

In most studied cells, meiosis proceeded rather reg-ularly, but deviations were found at practically allstages. Their spectrum in the trees growing in the arbo-retum was very wide. Some irregularities, such as chro-matin agglutination, residual nucleolus atprometaphase I and complete chromosome agglutina-tion into a ring at metaphase I, tripolar configurationand chromosomes outside of division spindles at ana-telophase I, nuclear union in dyad, chromosome elon-gation, and their chaotic arrangement at metaphase II,were noted only in the trees growing in the arboretumand were never seen in the trees growing in the naturalecosystems in the vicinity of Krasnoyarsk.

The frequency of meiotic irregularities at individualstages varied in different trees and in different years(table). Note that in 2004 an elevated frequency ofanomalies at different meiotic stages was noted in alltrees, as compared to the preceding years of observa-tions. The number of irregularities was especially highin meiosis I: 6.8 to 42.8% in different trees. In addition,in all studied trees, development of microsporocyteswas arrested at prophase I. In such cells, chromatin wasagglutinated and nucleolus was often ejected in thecytoplasm (Figs. 2c and 2d). These cells appeared tohave degenerated subsequently. The amount ofmicrosporocytes with this anomaly was 0.20 to 2.21%in different trees.

In 2004, some specific developmental irregularitieswere also noted in the arboretum, such as segregation ofchromosomes delaying at telophase into micronuclei.Bridges at anaphase I were sometimes preserved also inmeiosis II and could cause full or partial fusion of chro-mosome groups (Figs. 2e and 2f).

Analysis of abnormal meiocytes has shown thatboth common and specific types of anomalies wereobserved. The common anomalies included ejections ofchromosomes beyond the limits of chromosome plate,chaotic disjunction of chromosomes to the poles anddelaying chromosomes, and bridges, including multi-ple and tripolar configurations at anaphase II. The fre-

quency of these anomalies varied from 0.1 to 25.6%from the total number of meiocytes analyzed at a givenstage. Specific types of anomalies included polyvalentassociations in diakinesis, fragmentation, chromosomeagglutination in a ring at metaphase II, pentapolar con-

2520151050

–5–10–15

23.IV–6.V.2002

20.IV

30.IV

10.IV

10.V 20.V 30.V

20

15

10

5

0

–5

–10

–15

23.IV–9.V.2003

20.IV

30.IV

10.IV

10.V 20.V 30.V

2520151050

–5–10–15

25.IV–13.V.2004

20.IV

30.IV

10.IV

10.V 20.V 30.V

30

Fig. 3.

Timing of meiosis ( ) in the Siberian fir as a func-tion of air temperature (ordinate,

°

C) in different years.

Frequency of cells with meiotic anomalies from the total number of analyzed cells in 2004, %

Ordinal number of tree

Totalnumber

of analy-zed cells

First division

Total Dyads

Second division

Total TetradsMaturepollengrain

prophaseI (diaki-nesis)

meta-phase I

anaphase I–telophase I

meta-phase II

anaphase II–telophase II

1 3765 17.93 11.31 26.06 17.12 0 27.50 18.13 23.83 6.12 1.13

2 1960 – – – – 2.08 7.46 13.16 10.49 5.59 0.67

3 3701 0 6.83 26.01 13.59 0 8.02 11.00 9.56 2.96 0.50

4 2475 0 22.92 41.54 26.89 0.58 12.80 28.42 17.92 7.93 0.22

5 3620 0 15.42 42.82 25.66 1.23 10.92 10.11 10.65 3.03 0.36

6 3443 9.63 13.07 16.09 12.59 0 8.80 18.22 13.61 4.17 0.08

250


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figurations at anaphase II, and micronuclei in dyad andtetrad (Figs. 4a-4e). The frequency of theses anomaliesvaried significantly in different trees: in one of them,16.6% of meiocytes had specific anomalies at differentmeiotic stages, while in another, up to five chiasmatawere observed in some microsporocytes and a nucleo-lus with irregular shape was preserved at the stage ofdiakinesis in 8.5% of cells (Fig. 4f).

In all trees, multiple anomalies were noted atanaphases I and II (0.5 to 3.6% of microsporocytes).Bridges, ejections, delaying chromosomes, and chaoticdisjunction of chromosomes in different combinationswere usually observed. Note one more interesting andvery rare type of anomalies: asynchronous divisionwithin the same meiocyte: for example, prophase II andmetaphase or anaphase II on different poles. The fol-lowing combinations were also noted: anaphase I—metaphase II, metaphase II—anaphase II, dyad—anaphase II, telophase II—tetrad, anaphase II—tetrad.

Meiotic anomalies were usually eliminated at thestage of interkinesis (in dyads, or tetrads) and hardlyaffect the pollen viability. During microsporogenesis,in addition to the normal microspores with two air sacs,microspores with one or three air sacs were found, butthe frequency of such anomalies was rather low: nomore than 2.04%.

DISCUSSION

Morphology of meiosis is determined by the inter-action of genotypes, chromosome structure, and envi-ronment (Sosnikhina et al., 1994b). When saplingsobtained from sites of the natural species range aregrown in botanical gardens and arboreta, changes in thenatural-climatic conditions may provoke ecologicalstress and growth and developmental anomalies andlead to increased intraspecific differentiation anddecreased productivity (Nekrasov, 1971; Mamaev andAndreev, 1996). Special sensitivity to new conditions ischaracteristic for the juvenile stage of ontogeny andbeginning of reproductive phase, when sporo- andgametogenesis become to fit new temperature and lightregimes (Shkutko, 1983; Gavrilov and Butorina, 2005).And, each tree is characterized by a certain level ofanomalies, although their number depends on varyingenvironmental conditions. The increased duration ofmeiosis in the Siberian fir appears to be a response tonew life conditions. A similar phenomenon wasobserved in the Scots pine under stress conditions(Rozhdestvenskii, 1974; Butorina et al., 1985b).

The probability of unfavorable influences increasesdue to the lengthened meiosis duration, thus elevatingthe number of abnormal cells. Most meiotic stages inconiferous plants are very sensitive to changes in tem-perature and other environmental factors (Christiansen,1960; Chandler and Mavrodineanu, 1965; Eriksson, 1968;Ekberg et al., 1972; Kozubov, 1974; Kruklis, 1974;

(d) (e) (f)

(a) (b) (c)

Fig. 4.

Specific anomalies of meiosis in the Siberian fir: (a) polyvalent associations at prometaphase I, (b) “elongation” of chromo-somes at anaphase I, (c) chaotic arrangement of chromosomes at metaphase II; (d) micronucleus in dyad, (e) micronucleus in tetrad;(f) residual nucleolus in diakinesis.


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Luomajoki, 1977; Yakovlev, 1978). For example, in theSiberian fir, the level of abnormal meiocytes under theconditions of industrial pollution is 2.5 to 6.5 times thatunder the control conditions and the spectrum of struc-tural deviations is much wider: fragmentations, chromo-some bridges, ring chromosomes, and chromosome ejec-tion and agglutination (Presnukhina and Kalashnik,2003).

The results obtained suggest that the range of mei-otic irregularities in the fir in artificial plantings is muchwider than in the natural populations; in addition tocommon irregularities, specific and multiple irregulari-ties were recorded. This may be due to genetic featuresof the studied trees, such as mutations, since meiosis isunder the genetic control (Khvostova and Yachevskaya,1975; Golubovskaya, 1975, 1985; Sosnikhina et al.,1994a, 1994b; Bogdanov, 2003). The presence of chro-mosome mutations in the Siberian fir, including ringchromosomes, was already reported (Muratova andMatveeva, 1996).

Anomalies of chromosome behavior during meiosisare, as a rule, eliminated even before the tetrad stageand practically do not affect the quality of developingpollen grains. However, some irregularities, such aschromatin agglutination, may be reflected in pollen het-erogeneity by the size and shapes of pollen grains anddecrease its fertility (Pozhidaeva et al., 1985). In addi-tion to the normal pollen grains, small grains and grainswith abnormal numbers of air sacs were found. Appar-ently, the described deviations in microsporogenesiscould explain a high level (68–92%) of sterility in theSiberian fir trees growing in the arboretum.

Thus, the analysis of mcirosporogenesis in the Sibe-rian fir during its artificial breeding has revealed somespecific features of meiosis, such as increased durationand wider spectrum of anomalies, as compared to the firtrees in the natural populations.

ACKNOWLEDGMENTS

This study was supported by the Siberian Branch ofthe Russian Academy of Sciences, project no. 12.1, andKrasnoyarsk District Science Foundation—RFBR“Enisei-2005,” project no. 05-04-97717.

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Documents

Specific features of meiosis in the Siberian fir (Abies sibirica Ledeb.) artificial populations