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Variability of rDNA loci in dioecious Rumex acetosa L. detected by fluorescence in situ hybridization
Abstract
Rumex acetosa is a dioecious plant with a XX/XY1Y2 sex chromosome system. The molecular cytogenetic organization of the 5S rDNA and ITS rDNA on the chromosomes of male and female plants of R. acetosa was investigated by multi-color fluorescence in situ hybridization (McFISH). Different patterns of the FISH signals were observed between the male and female plants depending on the probes, 5S and 17S rDNA. In the female plants, two distinctive types of signals were observed based on the number of 17S rDNA signals, showing one or two pairs on the somatic metaphase chromosomes. In contrast, the signals in the male plants were observed on one of the homologous chromosomes or between the homologous chromosomes with a different size. One pair of 5S rDNA signals was commonly observed in both the male and female plants. This is the first report to identify the diversity of the rDNA FISH patterns in dioecious plants.
... The fluorescent staining allowed the identification of repetitive sequences (AT-rich, GC-rich and rDNA) in chromosomes of R. acetosa and provided a starting point for comparative studies of other Rumex species [Ruiz Rejon et al., 1994;Shibata et al., 1999Shibata et al., , 2000aLengerova and Vyskot, 2001;Koo et al., 2004;Mosiołek et al., 2005;Navajas-Pérez et al., 2006;Cuñado et al., 2007]. In the research described here, C-banding/DAPI and CMA 3 /DA/ DAPI were used for the first time for making a detailed characterization of the karyotype structure in R. thyrsiflorus . ...
... It has been shown that in plants NORs were almost always CMA 3 -positive [Guerra, 2000]. The presence of 45S rDNA sites on the fifth autosome pair has been demonstrated in R. acetosa by, among others, Koo et al. [2004] and Mosiołek [2005]. Moreover, Lengerova and Vyskot [2001] revealed that rDNA located on this chromosome is hypermethylated and inactive. ...
... In R. thyrsiflorus , the GC-rich chromatin was also observed on the longer arm of the fourth autosome. In R. acetosa , 2 loci of 5S rDNA were evidenced in this chromosome arm [Koo et al., 2004;Mosiołek, 2005]. It is also interesting that segments of AT-rich chromatin in the smallest autosomes, though polymorphic or absent in R. acetosa [Wilby and Parker, 1988b; our observations], appear to be a permanent element of the R. thyrsiflorus genome, which resembles the situation described in R. papillaris [Navajas-Pérez et al., 2009a]. ...
The object of this work was to analyze the karyotype structure of Rumex thyrsiflorus using differential fluorescent methods of chromosome staining (C-banding/DAPI and CMA3/DA/DAPI) and molecular sex markers. The results obtained were compared with data on the structure of the sex chromosomes and autosomes in R. acetosa, a model species in studies of sex determination and sex chromosome evolution in plants with an XX/XY1Y2 system. A high level of similarity was found in the sex chromosome structure of the 2 species, along with small differences in their autosomal complexes. It suggests that differentiation of these 2 closely related species was not accompanied by major structural changes within their sex chromosomes. Molecular tests, however, revealed differences in the composition of male-specific repetitive sequence RAYSII, occurring in the Y1 chromosome. Amplification of this sequence showed the presence of a single product (∼700 bp) in R. acetosa and of 2 products (∼600 bp and ∼700 bp) in R. thyrsiflorus. The longer product (∼700 bp) was also revealed in R. arifolius, another species closely related to R. acetosa. The shorter DNA fragment, characteristic of R. thyrsiflorus, differed from the common product by of a large indel with a length of 110 bp. This fragment may serve as a species-specific molecular marker useful in taxonomical and population studies as well as in further research on the sex chromosome differentiation in R. thyrsiflorus.
... Previous research determining the number and location of 5S and 35S ribosomal DNA loci distribution in Polygonaceae does not show a clear tendency of 5S or 35S loci to be in higher or lower abundance than the other; in Fagopyrum and Persicaria most species present more 35S than 5S loci (Choi et al. 2008;Kikuchi et al. 2008;Sheng et al. 2013), while in Rumex it is the other way round (Koo et al. 2004;Kim et al. 2006). Nevertheless, the number of rDNA sites detected for Calligonum is consistent with the most commonly found numbers in angiosperms. ...
... Two authors have determined the number and location of the 35S and 5S rRNA loci in Polygonaceae, also finding a variation in the number of the rDNA sites in Fagopyrum esculentum: Kikuchi et al. (2008) reported the presence of six signals of both 35S and 5S rDNA, but Sheng et al. (2013) detected eight 35S rDNA and four 5S rDNA sites. A considerable variation in rDNA loci number was also identified in the species Rumex acetosa: according to Kim et al. (2006), it presented four 35S and 5S rDNA sites, while Koo et al. (2004) showed two 5S rDNA sites and three to four 35S rDNA sites. Many other examples outsides family Polygonaceae can be found showing that intraspecific variation in the number of rDNA loci is a common finding (Garcia et al. 2012). ...
Most Calligonum species are desert plants, characteristic of the Saharan bioclimatic region. All species karyologically analyzed until present have the basic chromosome number x = 9 and comprise diploids, triploids and tetraploids. The Tunisian flora comprises diploid Calligonum arich and C. azel, of restricted distribution, and the tetraploid C. comosum with wider distribution. Analyses of their karyotypes and polyploidisation-linked rDNA changes by orcein staining, fluorochrome banding with chromomycin A3 and fluorescent in situ hybridisation with 5S and 26S ribosomal DNA probes have been performed. We report the chromosome number for Calligonum arich (2n = 18) as well as the diploid level for C. comosum for the first time. Chromosome counts have also verified the earlier described tetraploid cytotype (2n = 36) of C. comosum. A general pattern of six GC-rich bands as well as two 35S sites and four 5S sites is described for Calligonum species at the diploid level although there is intraspecific variation regarding the site number in a second type of C. comosum, with one pair of 35S rDNA sites and two pairs of 5S rDNA sites. The tetraploid cytotype of C. comosum has undergone locus loss and genome downsizing. Genome size assessments confirmed previous data. Nonetheless, statistically significant differences were found depending on the type of tissue used for estimation. Measurements from seeds had always larger values than from leaves. The presence of cytosolic compounds in leaves, interfering with DNA staining, is discussed as a possible cause of the differences.
... During the compilation of the data, it was often observed that acrocentric chromosomes had rDNA sites on the short arm, as for example in species of Ipheion [35], Nothoscordum [34,46], Rumex [47] , and Alstroe- meria [48] . To assess whether the short arm of acrocentric chromosomes is a especially preferred region for rDNA cluster location, 266 species with single site or multiple sites having at least one acrocentric chromosome per karyotype were analyzed. ...
Background
45S rDNA sites are the most widely documented chromosomal regions in eukaryotes. The analysis of the distribution of these sites along the chromosome in several genera has suggested some bias in their distribution. In order to evaluate if these loci are in fact non-randomly distributed and what is the influence of some chromosomal and karyotypic features on the distribution of these sites, a database was built with the position and number of 45S rDNA sites obtained by FISH together with other karyotypic data from 846 plant species.
Results
In angiosperms the most frequent numbers of sites per diploid karyotype were two and four, suggesting that in spite of the wide dispersion capacity of these sequences the number of rDNA sites tends to be restricted. The sites showed a preferential distribution on the short arms, mainly in the terminal regions. Curiously, these sites were frequently found on the short arms of acrocentric chromosomes where they usually occupy the whole arm. The trend to occupy the terminal region is especially evident in holokinetic chromosomes, where all of them were terminally located. In polyploids there is a trend towards reduction in the number of sites per monoploid complement. In gymnosperms, however, the distribution of rDNA sites varied strongly among the sampled families.
Conclusions
The location of 45S rDNA sites do not vary randomly, occurring preferentially on the short arm and in the terminal region of chromosomes in angiosperms. The meaning of this preferential location is not known, but some hypotheses are considered and the observed trends are discussed.
... This fusion must have occurred between the centromeres of two acrocentric chromosomes and resulted in the loss of their short arms, since no 45S rDNA signal were observed in the extra metacentric chromosomes. Fusion of acrocentric chromosomes bearing nucleolar organizer regions on their short arms, with the loss of ribosomal sites, has been reported in several other genera such as Lillium (Muratović et al., 2005) and Rumex (Koo et al., 2004). In Nothoscordum, Robertsonian translocations seems to be a common phenomenon and may also have occurred between acrocentric and metacentric chromosomes, as in N. arenarium (Souza et al., 2009) and in four individuals of N. gracile from Santa Maria (Brazil) which have a metacentric chromosome with a proximal CMA band on one of its arms. ...
Nothoscordum gracile is an apomitic tetraploid widely distributed throughout the Americas and naturalized in many temperate regions of other continents. It has been suggested to form a species complex with sexual and apomictic N. nudicaule and N. macrostemon. Tetraploids of these species also share a structurally heterozygous chromosome complement 2n = 19 (13M + 6A). In this work, the origin of N. gracile and its relationships with its related species was investigated based on cytological and molecular data.
Cytogenetic analyses were based on meiotic behaviour, CMA bands, localization of 5S and 45S rDNA sites, and genomic in situ hybridization (GISH). Nuclear ITS and plastidial trnL-trnF sequences were also obtained for most individuals.
Proximal CMA bands were observed in the long arms of all acrocentrics of 2x and 4x N. macrostemon but not in diploid and some tetraploid cytotypes of N. nudicaule. Samples of N. gracile showed a variable number of CMA bands in the long arms of acrocentrics. Analysis of ITS sequences, dot-blot, GISH, and 5S and 45S rDNA sites, revealed no differentiation among the three species. The trnL-trnF cpDNA fragment showed variation with a trend to geographical structuring irrespective of morphospecies and fully congruent with karyotype variation.
The 2n = 19 karyotype was probably formed by a centric fusion event occurring in N. nudicaule and later transmitted to tetraploid cytotypes of N. macrostemon. Diploids of N. nudicaule and N. macrostemon appeared as consistent recently diverged species, whereas tetraploid apomicts seem to constitute an assemblage of polyploid hybrids originating from multiple independent hybridization events between them, part of which are morphologically recognizable as N. gracile.
... The tetraploid R. acetosella had four 45S rDNA loci and two 5S rDNA loci in different chromosomes (Figure 2A). In R. acetosa, the 45S ribosomal unit was present in two autosomal loci (Figure 2C), while there is one 5S rDNA locus (Koo et al. 2004). Both Southern-blot hybridization and PCR amplification techniques demonstrated the presence of RAE180 satellite-DNA sequences in the three species analysed (seeFigure 5). ...
The structural features and evolutionary state of the sex chromosomes of the XX/XY species of Rumex are unknown. Here, we report a study of the meiotic behaviour of the XY bivalent in Rumex acetosella and R. suffruticosus, a new species which we describe cytogenetically for the first time in this paper, and also that of the XY(1)Y(2) trivalent of R. acetosa by both conventional cytogenetic techniques and analysis of synaptonemal complex formation. Fluorescent in situ hybridization with satellite DNA and rDNA sequences as probes was used to analyse the degree of cytogenetic differentiation between the X and Y chromosomes in order to depict their evolutionary stage in the three species. Contrasting with the advanced state of genetic differentiation between the X and the Y chromosomes in R. acetosa, we have found that R. acetosella and R. suffruticosus represent an early stage of genetic differentiation between sex chromosomes. Our findings further demonstrate the usefulness of the genus Rumex as a model for analysing the evolution of sex chromosomes in plants, since within this genus it is now possible to study the different levels of genetic differentiation between the sex chromosomes and to analyse their evolutionary history from their origin.
Using meiosis and mitosis chromosomes, we have karyotyped and physically mapped of Humulus japonicus. The somatic metaphase chromosome numbers were 2n = 2× = 14 + XX in female, 2n = 2× = 14 + XY1Y2 in male and 2n = 3× = 21 + XXX in triploid. The 5S and 45S rDNA genes were physically mapped on the metaphase chromosomes using fluorescence in situ hybridization (FISH). One pair of 5S rDNA gene was detected on the short arm of chromosome 4 and two pairs of 45S rDNA gene were observed on the terminal regions of the short arms of chromosome 5 and 7 in both female and male plants. In addition, three pairs of two rDNAs were detected on the chromosome 4, 5 and 7 of triploid. At meiosis, a trivalent chromosome figure was clearly seen, of which Y1 and Y2 could be distinguished from X by their premature condensation and three chromosomes, Y1-X-Y2, the forms associated by terminal chiasmata.
In order to elucidate the interspecific relationships of the genus Pulsatilla, a molecular cytogenetic study was carried out on the five species (P. cernua, P. davurica, P. koreana, P. tongkangensis, and P. chinensis) of the genus Pulsatilla distributed throught the Korean Peninsula. The Somatic methaphase chromosome numbers of all five species were 2n = 2x = 16. The 5S and 45S rDNA genes were physically mapped on the metaphase chromosomes using fluorescence in situ hybridization (FISH). The 5S rDNA genes were detected on the long arm of chromosome 4 and on the long arm of chromosome 7, In addition, the 45S rDNA genes were localized on the short arms of chromosomes 7 and 8 in P. cernua, P. davurica and P. chinensis. An additional locus of the 5S rDNA gene was detected on the chromosome 6 in P. koreana. One of the 5S rDNA loci was not found on the homologue of chromosome 4 in P. tongkangenesis. A polymorphism of the signal intensity was also detected on the chromosomes 7 and 8 in P. tongkangenesis. Sequence analysis showed that the 5S rDNA sequences varied between species, ranging from 495 to 535 bp. The sequence data indicated that P. koreana was distantly related to the other four species of Pulsatilla.
Rumex acetosa L. is a dioecious flowering plant with a well developed sex chromosome system: 2n = 12 + XX in the female plants and 2n = 12 + XY1Y2 in the male plants. To isolate and characterize sex-linked DNA, we used the RAPD (randomly amplified polymorphic DNA) method, Southern blot analysis, and FISH (fluorescence in situ hybridization). As a result of the RAPD analysis, one male-specific DNA segment was identified and was designated as RAY-1.5 (R. acetosa Y chromosome enriched 1.5 k bp sequence). RAY-1.5 consists of two tandemly repeated sequences in the 5′-region and has an identical sequence to the Y chromosome specific and male enriched sequences. Southern blot analysis and FISH supported the assumption that RAY-1.5 is a male-specific, Y chromosome enriched repetitive DNA. Although RAY-1.5 has similarities to known male specific or enriched sequences, it was discovered to be a new sex-related DNA in R. acetosa.
Using both molecular and cytogenetic methods, we have examined and characterized eight Rumex species distributed throughout the Korean Peninsula. The somatic metaphase chromosomes in the Lapathum group were 2n=6x=60 in three of the species (R. crispus, R. japonicus and R. longifolius), 2n=5x=50 in one species (R. nipponicus), and 2n=4x=40 in two of the species (R. obtusifolius and R. maritinus). In the two dioecious groups, the chromosome numbers were 2n=6x=42 (female) and 43 (male) in R. acetocella, and 2n=2x=14 (female) and 15 (male) in R. acetosa. Using the FISH method, we physically mapped the 5S and 45S rDNA genes on the chromosomes of all the studied species. All of the species, except R. japonicus, possessed four 45S rDNA sites, whereas the 5S rDNA gene sites were variable, ranging between 2 and 8. Polymorphic 5S rDNA sites at the same ploidy level were found among species in the subgenus Lapathum group. Nucleotide sequence analysis revealed that the 5S rDNA spacer also varied between the species, ranging between 308 and 315 bp, except for each 120 bp coding region. FISH and 5S rDNA spacer sequencing were successfully applied to the identification and characterization of the eight Rumex species examined in this study.
Dioecy is relatively rare in plants and sex determination systems vary among such species. A good example of a plant with heteromorphic sex chromosomes is hop (Humulus lupulus). The genotypes carrying XX or XY chromosomes correspond to female and male plants, respectively. Until now no clear cytogenetic markers for the sex chromosomes of hop have been established. Here, for the first time the sex chromosomes of hop are clearly identified and characterized. The high copy sequence of hop (HSR1) has been cloned and localized on chromosomes by fluorescence in situ hybridization. The HSR1 repeat has shown subtelomeric location on autosomes with the same intensity of the signal. The signal has been present in the subtelomeric region of the long arm and in the near-centromeric region but absent in the telomeric region of the short arm of the X chromosome. At the same time the signal has been found in the telomeric region only of the long arm of the Y chromosome. This finding indicates that the sex chromosomes of hop have evolved from a pair of autosomes via ancient translocation or inversion. The observation of the meiotic configuration of the sex bivalents shows the location of a pseudoautosomal region on the long arms of X and Y chromosomes.
The complete nucleotide sequence of a rice nuclear 17S rRNA gene (rDNA) has been determined. The rice rDNA is 1812 bp long
and its G+C content is 5l.3% This nucleotide sequence shows 79% 80% and 80%, homology to those of yeast, Xenopus laevis and rat 18S rDNAs, respectively. Divergency of nucleotide sequences is largely attributed to five blocks of highly variable
regions, where eukaryotic specific sequences can be observed.
The chromosome characteristics of five closely-related species in Rumex subgenus Acetosa are considered. All are dioecious diploids with 2n=12+XX in females and 2n = 12+XY1Y2 in males. The autosomes of all species are very similar, all highly acrocentric and displaying apparent homoeology, and only two chromosome changes have occurred in the evolution of the group – shift of an NOR and deletion of part of the long arm of chromosome 6. The heterochromatic Y-chromosomes are more variable and only two species cannot be identified by examination of the Ys alone. Hypervariability in centromere location is characteristic of Ys in the whole subgenus although there is no quantitative variation in heterochromatin. On the autosomes, parallel polymorphisms for heterochromatic supernumerary segments on the short arms of pairs 1, 5 and 6 are found in 4 of the 5 species, and euchromatic B-chromosomes are common in three species. These recurrent patterns of chromosome variation emphasise the close relationships within the species group
The dioecious flowering plant Rumex acetosa is polymorphic for heterochromatic supernumerary segments carried on the short arms of chromosomes 1 and 6 in British populations. SS1 is found in the majority of populations but at a very low frequency, averaging only 4 per cent of chromosome 1. There is no obvious pattern to this distribution. SS6 was found in half the populations examined, all from the warmer southern and western parts of Britain. Overall it accounts for 6 per cent of chromosome 6 and averages 12 per cent in polymorphic populations. In heterozygotes SS1 is transmitted through the egg at a frequency of 063, a highly significant deviation from expectation. Pollen transmission shows a slight but nonsignificant deficit of SS1 chromosomes. Mendelian expectations were fulfilled for seven crosses involving SS6. One cross, however, showed a highly significant excess transmission through the pollen. It is argued that meiotic drive plays a role in the maintenance of the ubiquitous SS1 low-frequency polymorphism but not the SS6 polymorphism which shows clear environmental correlations.
The molecular cytogenetic organization of 17S ribosomal RNA genes (17S rDNA), a part of the 45S rDNA repeat, was investigated on the chromosomes of the liverwort Marchantia polymorpha using fluorescence in-situ hybridization (FISH). The numbers of 17S rDNA loci visualized in female and male chromosomes were ten and nine, respectively. This heterogeneous localization was due to the presence of an additional 17S rDNA locus on the X chromosome and its absence on the Y chromosome. The signal on the X chromosome covered almost the entire region of its long arm. The other nine signals were observed on the same loci of respective autosomes in both sexes. Southern hybridization analysis revealed an additional band including 17S rDNA exclusively on EcoRI digested female genomic DNA supporting the existence of an additional 17S rDNA locus on the X chromosome.
Dosage sex-chromosome systems have been detected in two genera of flowering plants. Rumex and Humulus. In Rumex subgenus Acetosa dioecious species have a multiple sex chromosome system with two X chromosomes in females and an X and two Y chromosomes in males. The Y chromosomes are facultatively heterochromatic appearing as chromocentres in somatic interphase nuclei, but undergo RNA transcription, show DNase-I sensitivity, and are genomically-similar to the rest of the complement. Sex determination is dependent on X/autosome balance, and androecium development is not dependent on the presence of Y chromosomes. Intermediate X/autosome ratios between 0.5 and 1.00 give hermaphrodite individuals. The autosomes also affect sex expression, with some enhancing male and others female development. Disomy for one quarter of an X-chromosome is sufficient for functional female development. Y-chromosomes act sporophytically and are required for meiotic success, although a complete Y-complement is not a haploid requirement for pollen maturation or fertilisation. The American annual species R. hastatulus is polytypic for sex-chromosomes and has features both of X/autosome balance and active-Y systems. Humulus lupulus (hop) is highly polytypic with at least six sex-chromosome types. The dosage system is similar to that of Rumex although Y-chromosomes are required for successful pollen maturation. In Humulus dioecy is less strict than in Rumex and a simple synthetic hormone treatment is able to induce male flowers on a female cultivar.
Because of their structural and catalytic functions during protein synthesis, the 18S, 5.8S, and 28S ribosomal RNAs (rRNAs) are essential for the support of differentiation, development, and growth. The genes encoding these RNAs are present in high copy number in all eukaryotes. Although there is evidence for the existence of variation for rRNA gene copy number within higher vertebrate species, there is little knowledge concerning the effects of such variation, especially reductions, on development and viability of homeothermic vertebrates. The main objective of this study was to determine the developmental potential of chick embryos containing defined deficiencies for rRNA gene copy number in order to assess the contribution of rDNA cluster size variation to embryonic mortality in homeothermic vertebrates. This was achieved by studying a strain of chickens containing nucleolar size polymorphisms that reflect rDNA cluster size polymorphisms. Embryos exhibiting a nucleolar phenotype of one large and one very small nucleolus (Pp) are heterozygous for a reduced rDNA cluster (+/p1) and were shown in the present study to contain about 66% of the complement of rRNA genes in normal individuals (+/+) that show two large equal-sized nucleoli (PP). The +/p1 embryos were found to develop and grow normally. Embryos exhibiting a nucleolar phenotype of two very small nucleoli (pp) are homozygous for the rDNA-deficient cluster (p1/p1) and contained about 45% of the normal rDNA complement of genes. These p1/p1 embryos were arrested in their development during early gastrulation. They exhibited a characteristic morphology consisting of a dorsal invagination that was strikingly different from the primitive streak formed in +/+ and +/p1 individuals.(ABSTRACT TRUNCATED AT 250 WORDS)
X and Y sex chromosomes from the dioecious plant Silene latifolia (white campion) were isolated from mitotic metaphase chromosome preparations on polyester membranes. Autosomes were ablated using an argon ion laser microbeam and isolated sex chromosomes were then recovered on excised fragments of polyester membrane. Sex chromosome associated DNA sequences were amplified using the degenerate oligonucleotide primed polymerase chain reaction (DOP-PCR) and pools of DOP-PCR products were used to investigate the genomic organization of the S. latifolia sex chromosomes. The chromosomal locations of cloned sex chromosome repeat sequences were analysed by fluorescence in situ hybridization and data complementary to laser ablation studies were obtained by genomic in situ hybridization. In combination, these studies demonstrate that the X and Y sex chromosomes of S. latifolia are of very similar DNA composition and also that they share a significant repetitive DNA content with the autosomes. The evolution of sex chromosomes in Silene is discussed and compared with that in another dioecious species, Rumex acetosa.
The dioecious plant Rumex acetosa has a multiple sex chromosome system: XX in female and XY(1)Y(2) in male. Both types of Y chromosome were isolated from chromosome spreads of males by manual microdissection, and their chromosomal DNA was amplified using degenerate oligonucleotide primed-polymerase chain reaction (DOP-PCR). When the biotin-labeled DOP-PCR product was hybridized with competitor DNA in situ, the fluorescent signal painted the Y chromosomes. A library of Y chromosome DNA was constructed from the DOP-PCR product and screened for DNA sequences specific to the Y chromosome. One Y chromosome-specific DNA sequence was identified and designated RAYSI (R. acetosa Y chromosome-specific sequence I). RAYSI is a tandemly arranged repetitive DNA sequence that maps to the 4',6-diamidino-2-phenylindole bands of both Y chromosomes.
The dioecious plant Rumex acetosa has a multiple sex chromosome system: females are 2n = XX + 12, males are 2n = XY1Y2 + 12, and the two Y chromosomes are heterochromatic. A DNA sequence abounded in the mare genome was isolated and analyzed. The sequence (RAE180) was a 180-bp-long tandemly arranged repetitive sequence, distributed in chromosomes Y1 and Y2, and two pairs of autosomes. Both Y chromosomes contained large amounts of RAE180 and the sequence formed many DAPI bands, while, on the two pairs of autosomes, RAE180 did not form DAPI bands. The internal structure and morphological changes of the Y chromosomes were analyzed by FISH, using RAE180 and the Y-chromosome-specific sequence RAYSI as probes. The pattern of the FISH signals caused by the accumulation of RAE180 and RAYSI suggested the structural change in the Y chromosomes during the process of sex chromosome evolution, and the morphological change in the Y chromosomes was explained by reciprocal translocation and inversion.