Diploid-like Meiosis Research Articles

Meiosis in Polyploids and Implications for Genetic Mapping: A Review.

Plant cytogenetic studies have provided essential knowledge on chromosome behavior during meiosis, contributing to our understanding of this complex process. In this review, we describe in detail the meiotic process in auto- and allopolyploids from the onset of prophase I through pairing, recombination, and bivalent formation, highlighting recent findings on the genetic control and mode of action of specific proteins that lead to diploid-like meiosis behavior in polyploid species. During the meiosis of newly formed polyploids, related chromosomes (homologous in autopolyploids; homologous and homoeologous in allopolyploids) can combine in complex structures called multivalents. These structures occur when multiple chromosomes simultaneously pair, synapse, and recombine. We discuss the effectiveness of crossover frequency in preventing multivalent formation and favoring regular meiosis. Homoeologous recombination in particular can generate new gene (locus) combinations and phenotypes, but it may destabilize the karyotype and lead to aberrant meiotic behavior, reducing fertility. In crop species, understanding the factors that control pairing and recombination has the potential to provide plant breeders with resources to make fuller use of available chromosome variations in number and structure. We focused on wheat and oilseed rape, since there is an abundance of elucidating studies on this subject, including the molecular characterization of the Ph1 (wheat) and PrBn (oilseed rape) loci, which are known to play a crucial role in regulating meiosis. Finally, we exploited the consequences of chromosome pairing and recombination for genetic map construction in polyploids, highlighting two case studies of complex genomes: (i) modern sugarcane, which has a man-made genome harboring two subgenomes with some recombinant chromosomes; and (ii) hexaploid sweet potato, a naturally occurring polyploid. The recent inclusion of allelic dosage information has improved linkage estimation in polyploids, allowing multilocus genetic maps to be constructed.

Meiotic Chromosome Stability and Suppression of Crossover Between Non-homologous Chromosomes in xBrassicoraphanus, an Intergeneric Allotetraploid Derived From a Cross Between Brassica rapa and Raphanus sativus.

Hybridization and polyploidization are major driving forces in plant evolution. Allopolyploids can be occasionally formed from a cross between distantly related species but often suffer from chromosome instability and infertility. xBrassicoraphanus is an intergeneric allotetraploid (AARR; 2n = 38) derived from a cross between Brassica rapa (AA; 2n = 20) and Raphanus sativus (RR; 2n = 18). xBrassicoraphanus is fertile and genetically stable, while retaining complete sets of both B. rapa and R. sativus chromosomes. Precise control of meiotic recombination is essential for the production of balanced gametes, and crossovers (COs) must occur exclusively between homologous chromosomes. Many interspecific hybrids have problems with meiotic division at early generations, in which interactions between non-homologous chromosomes often bring about aneuploidy and unbalanced gamete formation. We analyzed meiotic chromosome behaviors in pollen mother cells (PMCs) of allotetraploid and allodiploid F1 individuals of newly synthesized xBrassicoraphanus. Allotetraploid xBrassicoraphanus PMCs showed a normal diploid-like meiotic behavior. By contrast, allodiploid xBrassicoraphanus PMCs displayed abnormal segregation of chromosomes mainly due to the absence of homologous pairs. Notably, during early stages of meiosis I many of allodiploid xBrassicoraphanus chromosomes behave independently with few interactions between B. rapa and R. sativus chromosomes, forming many univalent chromosomes before segregation. Chromosomes were randomly assorted at later stages of meiosis, and tetrads with unequal numbers of chromosomes were formed at completion of meiosis. Immunolocalization of HEI10 protein mediating meiotic recombination revealed that COs were more frequent in synthetic allotetraploid xBrassicoraphanus than in allodiploid, but less than in the stabilized line. These findings suggest that structural dissimilarity between B. rapa and R. sativus chromosomes prevents non-homologous interactions between the parental chromosomes in allotetraploid xBrassicoraphanus, allowing normal diploid-like meiosis when homologous pairing partners are present. This study also suggests that CO suppression between non-homologous chromosomes is required for correct meiotic progression in newly synthesized allopolyploids, which is important for the formation of viable gametes and reproductive success in the hybrid progeny.

Genetic regulation of meiosis in polyploid species: new insights into an old question

Precise chromosome segregation is vital for polyploid speciation. Here, we highlight recent findings that revitalize the old question of the genetic control of diploid-like meiosis behaviour in polyploid species. We first review new information on the genetic control of autopolyploid and allopolyploid cytological diploidization, notably in wheat and Brassica. These major advances provide new opportunities for speculating about the adaptation of meiosis during polyploid evolution. Some of these advances are discussed, and it is suggested that research on polyploidy and on meiosis should no longer be unlinked.

Cytological diploidization and rapid genome changes of the newly synthesized allotetraploids Cucumis × hytivus

We used a newly synthesized allotetraploid between C. sativus (2n = 2x = 14, n gametic chromosome number, x haploid chromosome number) and C. hystrix (2n = 2x = 24) to study the genomic events in its early generations. Results from cytological characterization of the F(1) and the allotetraploid progenies showed that the rate of bivalents in meiotic metaphase I of the F(1) was greatly improved by chromosome doubling, and further improved during the selfing process of allopolyploid resulting into relatively diploid-like meiosis. Extensive genomic changes were detected by amplified fragment length polymorphism analysis. The changes mainly involved loss of parental restriction fragments and gaining of novel fragments. The total detectable changes were from 11.1 to 32.1%, and the frequency of losing parental fragments was much higher than that of gaining novel fragments. Some of the changes were initiated as early as in the F(1) hybrid, whereas others occurred after chromosome doubling (polyploid formation). No significant differences were detected in the reciprocal F(1) hybrids and S(0) generations. But the data showed that the frequency of sequence losing in C. sativus was about two times higher than in the C. hystrix. Our results demonstrated that the sequence elimination was the major event of genomic changes, and it might provide the physical basis for the diploid-like meiotic behavior in the diploidization of the newly formed allopolyploids. Moreover, the results suggest that the sequence elimination was not caused by cytoplasmic factors, and might relate to genomic recombination and to the numbers of parental chromosome.

Molecular cytogenetics and allotetraploidy in the red vizcacha rat, Tympanoctomys barrerae (Rodentia, Octodontidae)

The theoretical impossibility of polyploidy in mammals was overturned by the discovery of tetraploidy in the red vizcacha rat, Tympanoctomys barrerae (2 n = 102). As a consequence of genome duplication, remarkably increased cell dimensions are observed in the spermatozoa and in different somatic cell lines of this species. Locus duplication had been previously demonstrated by in situ PCR and Southern blot analysis of single-copy genes. Here, we corroborate duplication of loci in multiple-copy (major rDNAs) and single-copy ( Hoxc8) genes by fluorescence in situ hybridization. We also demonstrate that nucleolar dominance, a large-scale epigenetic silencing phenomenon characteristic of allopolyploids, explains the presence of only one Ag-NOR chromosome pair in T. barrerae. Nucleolar dominance, together with the chromosomal heteromorphism detected in the G-banding pattern and synaptonemal complexes of the species’ diploid-like meiosis, consistently indicates allotetraploidy. Allotetraploidization can coherently explain the peculiarities of gene silencing, cell dimensions, and karyotypic features of T. barrerae that remain unexplained by assuming diploidy and a large genome size attained by the dispersion of repetitive sequences.

Putative diploid ancestors of 80-chromosome Glycine tabacina

The objective of this study was to discover the diploid progenitors of 80-chromosome Glycine tabacina with adventitious roots (WAR) and no adventitious roots (NAR). Three synthetic amphiploids were obtained by somatic chromosome doubling. These were (i) (G. latifolia, 2n = 40, genome B1B1,) × (G. microphylla, 2n = 40, genome BB) = F1(2n = 40, genome BB1) – 0.1% colchicine treatment (CT) – 2n = 80, genome BBB1B1; (ii) (G. canescens, 2n = 40, genome AA) × G. microphylla, 2n = 40, genome BB) = F1 (2n = 40, genome AB) – (CT) – 2n = 80, genome AABB; (iii) (G. latifolia, 2n = 40, B1B1) × G. canescens, 2n = 40, AA) = F1 (2n = 40, genome AB1) – (CT) – 2n = 80, genome AAB1B1. The segmental allotetraploid BBB1B1 was morphologically similar to the 80-chromosome G. tabacina (WAR), but meiotic pairing data in F1 hybrids did not support the complete genomic affinity. Despite normal diploid-like meiosis in allotetraploids AABB and AAB1B1, AABB was completely fertile, while pod set in AAB1B1 was very sparse. Morphologically, allotetraploid AABB was indistinguishable from the 80-chromosome G. tabacina (NAR) but in their F1 hybrids, the range of univalents at metaphase I was wide (4–44). The allotetraploid AAB1B1 did not morphologically resemble the 80-chromosome G. tabacina (NAR). However, the F1 hybrid of AABB × AAB1B1 showed normal meiosis with an average chromosome association (range) of 1.7 I (0–4) + 39.2 II (38–40). Based on this information, we cannot correctly deduce the diploid progenitor species of the 80-chromosome G. tabacina (NAR). The lack of exact genome homology may be attributed to the geographical isolation, natural mutation, and growing environmental conditions since the inception of 80-chromosome G. tabacina. Thus, it is logical to suggest that the 80-chromosome G. tabacina (NAR) is a complex, probably synthesized from A genome (G. canescens, G. clandestina, G. argyrea, G. tomentella D4 isozyme group) and B genome (G. latifolia, G. microphylla, G. tabacina) species, and the 80-chromosome G. tabacina (WAR) complex was evolved through segmental allopolyploidy from the B genome species.Key words: Glycine spp., allopolyploidy, colchicine, genome, intra- and inter-specific hybridization, polyploid complex.

Chromosomal Interchanges in Six Hexaploid Oat Genotypes

Intercultivar chromosomal interchanges in oat, 2n = 6x = 42, Avena sativa L., have not been extensively investigated. The objective of this research was to determine the occurrence of chromosomal interchanges among several cultivars of spring oat. Five oat cultivars (Andrew, Gopher, Hazel, Ogle, Otee) and one experimental breeding line (PA12422) included in this study carried expected 2n = 6x = 42 chromosomes, showed diploidlike meiosis with 2111 and set normal seeds. All the intercultivar F1 hybrids were vigorous and completely pollen‐ and seed‐fertile. Meiotic chromosome pairing at diakinesis of F1 hybrids revealed the following information: (i) Gopher and Otee contain similar chromosome structures and are differentiated from Andrew by a single chromosomal interchange; (ii) Hazel and Ogle possess identical chromosome structure and differ from Gopher and Otee by a single chromosomal interchange and by double interchanges from Andrew; and (iii) breeding line PA 12422 differs from Hazel and Ogle by two different interchanges, but the two interchanges involve the same chromosome giving a 1VI + 18II chromosome configuration. Thus, multivalents occurred frequently in the hexaploid spring oat F2 hybrids studied.

Ancestors of 80- and 78-chromosome Glycine tomentella Hayata (Leguminosae)

The objective of this study was to determine the progenitors of 80- and 78-chromosome tomentellas of the subgenus Glycine. Wide geographical distribution, aggressive and vigorous growth habit, diploid-like meiosis in the accessions, and meiotic pairing in intraspecific and interspecific hybrids suggested that both cytotypes (2n = 80, 78) evolved through allo-polyploidization. Two synthetic amphidiploids were obtained by somatic chromosome doubling ((G. tomentella, 2n = 40, genome DD) × (G. canescens, 2n = 40, genome AA) = F1, (2n = 40, genome AD), which was treated with colchicine, giving 2n = 80, genome AADD; (G. tomentella, 2n = 38, genome EE) × (G. canescens, 2n = 40, genome AA) = F1, (2n = 39, genome AE), which was treated with colchicine, giving 2n = 78, genome AAEE). These amphidiploids, which exhibited gigas effect, diploid-like meiosis, and normal pollen and seed set, were hybridized with 80- and 78-chromosome tomentellas. On the basis of morphological characteristics and meiotic pairing in F1 plants, G. tomentella (2n = 40, DD) and G. canescens (2n = 40, AA) are concluded to be the ancestors of 80-chromosome tomentellas (AADD) from Queensland, Australia. One of the ancestors of 80-chromosome tomentellas from Northern Territory and Western Australia, Australia, and Papua New Guinea is G. canescens; the second progenitor species was not determined. In addition, it is apparent that both 40- and 38-chromosome tomentellas gave rise to 78-chromosome G. tomentella (DDEE).Key words: allopolyploidy, colchicine, genome, intraspecific and interspecific hybridization, polyploid complex.

Diploid-like meiotic behavior in synthesized amphiploids of the genus Glycine Willd. subgenus Glycine

Six amphiploids consisting of one allotetraploid (2n = 4x = 80), four allohexaploids (2n = 6x = 120), and one allooctoploid (2n = 8x = 160) were synthesized by doubling the chromosomes of F1 interspecific hybrids of the following parents: one diploid (Glycine latifolia 2n = 2x = 40 × G. clandestina, short pod (Sp), 2n = 2x = 40); four triploids (G. clandestina, Sp, 2n = 2x = 40 × G. tabacina 2n = 4x = 80), (G. tabacina 2n = 4x = 80 × G. canescens 2n = 2x = 40), (G. tomentella2n = 4x = 80 × G. canescens 2n = 2x = 40 and its reciprocal); and one tetraploid (G. tomentella2n = 4x = 80 × G. tabacina 2n = 4x = 80). Chromosomal chimerism was observed in the C1 generation. Pod set was recorded in all the colchicine-treated hybrids except in the tetraploid hybrid of G. tomentella × G. tabacina. In C2 generation plants, chromosomal instability was noticed only in the allohexaploid of G. tabacina × G. canescens. All of the amphiploids showed diploid-like meiosis in the majority of the sporocytes and did not exhibit expected multivalent associations, a classical example of allopolyploidy. This was attributed to strong preferential pairing between homologous chromosomes which may be under genetic control.Key words: Glycine, synapsis, interspecific hybrids.

Studies on the control of diploid-like meiosis in polyploid taxa of Chrysanthemum

Chromosome pairing during meiosis was studied in colchiploids of Ch. japonense 6X and Ch. boreale 2X. In both species chromosomes paired predominantly as bivalents, even though because of complete homology they possess the ability to pair as multivalents. Multivalent formation is prevented by restriction of pairing initiation to a single site (=zygomere) per chromosome. Multivalent suppressor systems in polyploids may evolve through gradual reduction in number of zygomeres, and differentiation in their homology recognition and regulation system.

GENETIC REGULATION OF HETEROGENETIC CHROMOSOME PAIRING IN POLYPLOID SPECIES OF THE GENUSTRITICUM sensu lato

Polyploid species of Triticum sensu lato were crossed with Triticum aestivum L. em. Thell. cv. Chinese Spring monotelodisomics or ditelosomics that were monosomic for chromosome 5B. Progeny from these crosses were either euploid, nullisomic for 5B, monotelosomic for a given Chinese Spring chromosome, or nullisomic for 5B and monotelosomic simultaneously. The Chinese Spring telosome in the hybrids permitted the evaluation of autosyndesis of chromosomes of the tested species. In addition, several Chinese Spring eu- and aneuhaploids were produced. Genotypes of T. cylindricum Ces., T. juvenale Thell., T. triunciale (L.) Raspail, T. ovatum (L.) Raspail, T. columnare (Zhuk.) Morris et Sears, T. triaristatum (Willd.) Godr. et Gren., and T. rectum (Zhuk.) comb. nov. were all shown to have suppressive effects on heterogenetic pairing in hybrids lacking 5B or 3AS, whereas T. kotschyi (Boiss.) Bowden had no effect. It was concluded that diploid-like meiosis in these species is due to genetic regulation. A number of these genotypes promoted heterogenetic pairing in the presence of 5B. A model is presented to explain this dichotomous behavior of the tested genotypes. Monotelosomic-3AL haploids had a greater amount of pairing than did euhaploid Chinese Spring, which substantiated the presence of a pairing suppressor(s) on the 3AS arm. Evidence is presented that shows that T. juvenale does not have a genome homologous with the D genome of T. aestivum.

Studies on the control of diploid-like meiosis in polyploid taxa of Chrysanthemum. III. Decaploid Ch. crassum Kitamura.

Studies on the control of diploid-like meiosis in polyploid taxa of Chrysanthemum. III. Decaploid Ch. crassum Kitamura.

Studies on the control of diploid-like meiosis in polyploid taxa of Chrysanthemum. II. Octoploid Ch. ornatum Hemsley.

1) In Ch. ornatum (Akune strain) with 2n=8x=72 the following meiotic configurations were frequently observed; 2 IV+32 II, 1 IV+34 II, 36 II and 35 II+2 I. Seventy-two chromosomes at mitotic metaphase varied in length from 5.1μm to 2.8μm and in arm ratio from 1.0 to 6.5. Five satellite chromosomes and seven small chromosomes with the extreme subterminal centromeres were well distinguishable. Karyomorphologically this strain is not an autooctoploid.2) One androgenetic polyhaploid with 2n=4x+1=37 was obtained by artificial ovary culture after hybridization with the diploid Ch. Makinoi. The following meiotic configurations were frequently observed; 1 IV+1 III+15 II, 1 IV+1 III+14 II+2 I, 1 IV+16 II+1 I, 1 III+17 II and 18 II+1 I. A pentavalent association and a chromosome fragment were also observed rarely. The chromosomes derived from Ch. ornatum (Akune strain) paired homoeologously. The data of quadrivalent frequency conform to the theoretical Poisson expectation based on the random hypothesis.3) In Ch. ornatum (Yakushima Isl. strain) with 2n=8x=72, 36 II was the main meiotic configuration and 3 IV+30 II, 2 IV+32 II, 1 IV+34 II and 35 II+2 I were rarely observed. Seventy-two chromosomes, at mitotic metaphase, varied in length from 6.0μm to 3.2μm and in arm ratio from 1.0 to 4.6. Ten satellites chromosomes and five small chromosomes with extreme subterminal centromers were well distinguishable. Karyomorphologically this strain is not an autooctoploid.4) Three F1-hybrids with 2n=5x=45 between diploid Ch. boreale and Ch. ornatum (Yakushima Isl. strain) were obtained by ovary culture. The following meiotic configurations were frequently observed; 1 IV+19 II+3 I, 5 III+12 II+6 I, 2 III+17 II+5 I, 21 II+3 I and 20 II+5 I. The chromosomes derived from Ch. ornatum (Yakushima Isl. strain) paired homoeololgously.5) The genetic control system for the suppression of multivalent formation in octoploid, its polyhaploid and pentaploid F1-hybrid must be the restriction of pairing initiation at one of two sites per chromosome. This restriction seems to be under the polygenic control which leads to the super-suppression in accompany with the increase of gene dosage. This system tends to act in a relatively more harmonious fasion in the even-numberd polyploid than in the odds.

Studies on the control of diploid-like meiosis in polyploid taxa of Chrysanthemum. I. Hexaploid Ch. japonense Nakai.

Chromosome pairing during meiosis was studied in colchiploids of Ch. japonense 6X and Ch. boreale 2X. In both species chromosomes paired predominantly as bivalents, even though because of complete homology they possess the ability to pair as multivalents. Multivalent formation is prevented by restriction of pairing initiation to a single site (=zygomere) per chromosome. Multivalent suppressor systems in polyploids may evolve through gradual reduction in number of zygomeres, and differentiation in their homology recognition and regulation system.

THE CONTROL OF DIPLOID-LIKE MEIOSIS IN POLYPLOID TAXA OF <i>CHRYSANTHEMUM</i> (COMPOSITAE)

Genetic stabilisation of diploid-like meiosis occurs in hexaploid, octoploid and decaploid taxa of Chrysanthemum. This stabilisation is ineffective in F1-hybrids between diploids and the several polyploids which have been obtained by ovary culture. The suppression of multivalent formation is effective in even-ploid hybrids although they are amphihaploid. A significant frequency of trivalents occurs in odd-ploid hybrids.

Genetic control of diploid-like meiosis in hexaploid tall fescue.

ALLOPOLYPLOIDY has played a vital role in the evolution of plant species useful to man. Hybridisation between related species followed by chromosome doubling has given rise to some of our most important grain, forage and fibre crops. The successful establishment of a sexually reproducing polyploid would, however, depend on the integration of the constituent genomes into a meiotically and, hence, reproductively stable form which could be achieved only by means of a precise diploidising mechanism. In the case of bread-wheat it has been conclusively demonstrated that diploid-like meiotic behaviour is genetically controlled1,2 and there is a strong indication of a similar control in other crop species, for example, hexaploid oats3 and tetraploid cottons4.

Genetic regulation of diploid-like chromosome pairing in the hexaploid species, Festuca arundinacea Schreb. and F. rubra L. (Gramineae)

The basis of diploid-like chromosome pairing in hexaploid (2n=6x=42) Festuca arundinacea Schreb. and hexaploid F. rubra L. has been investigated. On the combined evidence derived from chromosome pairing in some euploid (2n=42) and monosomic (2n=41) hybrids from a diallel set of crosses between ten geographically diverse ecotypes of tall fescue, intergeneric hybrids involving tall fescue as well as red fescue, and euploid (2n=56) and aneuploid (2n=52, 53, 54, 55) amphiploids between Lolium multiflorum and F. arundinacea, it is concluded that diploid-like meiosis in these hexaploid species as well as in other natural polyploid species of Festuca is under genetic control. It is further inferred that this diploidizing gene(s) system must at least be disomic in dosage to be effective in suppressing homoeologous pairing and, therefore, had no influence upon pairing in haploid complements of the hybrids, i.e., it is haplo-insufficient or hemizygous-ineffective. — It has also been shown that sterility in hybrids between some geographically isolated ecotypes of tall fescue results from irregular meiosis due to the breakdown of the regulatory mechanism, rather than from chromosomal differentiation of the parental ecotypes as widely believed so far. The evolutionary significance of such a gene-repressing effect of certain genotypes or genes is indicated. — It is further suggested that the hemizygous ineffectiveness of the genetic control of bivalent pairing is of evolutionary significance and could have major implications on the cytogenetic relationships and the breeding of the entire Lolium-Festuca complex.