Alteration of basic chromosome number by fusion–fission cycles

Schubert, Ingo; Rieger, R.; Fuchs, Jörg

doi:10.1139/g95-170

Cited by 25 publications

(19 citation statements)

References 12 publications

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“…In contrast, fission has received relatively little attention as a mechanism of chromosome number change in plants. Fission-fusion cycles have been observed in the common bean (Schubert et al, 1995) and there is no obvious mutational reason why fissions should not contribute to karyotypic evolution in plants as well as in mammals. Non-centric fission (that is, breakage of a chromosome into two pieces, only one of which includes a centromere) can carry obvious deleterious effects, but centric fissions should be less intrinsically deleterious, and no more so in plants than in mammals.…”

Section: Discussionmentioning

confidence: 99%

Comparative linkage maps suggest that fission, not polyploidy, underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae)

Fishman

et al. 2014

Heredity

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Changes in chromosome number and structure are important contributors to adaptation, speciation and macroevolution. In flowering plants, polyploidy and subsequent reductions in chromosome number by fusion are major sources of chromosomal evolution, but chromosome number increase by fission has been relatively unexplored. Here, we use comparative linkage mapping with gene-based markers to reconstruct chromosomal synteny within the model flowering plant genus Mimulus (monkeyflowers). Two sections of the genus with haploid numbers X14 have been inferred to be relatively recent polyploids because they are phylogenetically nested within numerous taxa with low base numbers (n ¼ 8-10). We combined multiple data sets to build integrated genetic maps of the M. guttatus species complex (section Simiolus, n ¼ 14) and the M. lewisii group (section Erythranthe; n ¼ 8), and then aligned the two integrated maps using 4100 shared markers. We observed strong segmental synteny between M. lewisii and M. guttatus maps, with essentially 1-to-1 correspondence across each of 16 chromosomal blocks. Assuming that the M. lewisii (and widespread) base number of 8 is ancestral, reconstruction of 14 M. guttatus chromosomes requires at least eight fission events (likely shared by Simiolus and sister section Paradanthus (n ¼ 16)), plus two fusion events. This apparent burst of fission in the yellow monkeyflower lineages raises new questions about mechanisms and consequences of chromosomal fission in plants. Our comparative maps also provide insight into the origins of a chromosome exhibiting centromere-associated female meiotic drive and create a framework for transferring M. guttatus genome resources across the entire genus.

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Section: Discussionmentioning

confidence: 99%

Comparative linkage maps suggest that fission, not polyploidy, underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae)

Fishman

et al. 2014

Heredity

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“…Such translocations are very common among plants (Jones 1978), animals (White 1973) and humans (Hamerton 1975), and are believed to have played a significant role in karyotype evolution (Jones 1978). Robertsonian translocations can arise from the fusion of two telocentrics forming a metacentric chromosome (Holmquist and Dancis 1979;Schubert et al 1995). Alternatively, recombination in the short arms of two acrocentric chromosomes followed by the loss of the acentric fragment may lead to a metacentric chromosome that also results in a change of the basic chromosome number of an organism.…”

Section: Introductionmentioning

confidence: 99%

The centromere structure in Robertsonian wheat-rye translocation chromosomes indicates that centric breakage-fusion can occur at different positions within the primary constriction

et al. 2001

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Univalent chromosomes at meiotic metaphase I have a tendency to misdivide at the centromeres. Fusion of the misdivision products may produce Robertsonian translocations. The fine structure of the centromeres in Robertsonian wheat-rye translocation chromosomes was analyzed by fluorescence in situ hybridization (FISH) using two centromere-specific DNA clones: pRCS1, derived from rice, and pAWRC1, derived from rye. Clone pRCS1 hybridizes to the centromeres of all grasses including wheat and rye, whereas clone pAWRC1 is rye specific and hybridizes only to the centromeres of rye. Four of the six wheat-rye translocations derived from a single centric misdivision event (1st generation translocations) had hybrid centromeres, with approximately half of the centromere derived from rye and half from wheat. In the two other 1st generation translocations, the entire centromere was derived from rye. Among eight reconstructed wheat and rye chromosomes that originated from two consecutive centric misdivision-fusion events (2nd generation translocations), T1BS.1BL (derived from T1BS.1RL and T1RS.1BL) and one of three T2BS.2BL (derived from T2RS.2BL and T2BS.2RL) had hybrid centromeres. T1RS.1RL (derived from T1BS.1RL and T1RS.1BL), two of three T2BS.2BL, and all three T2RS.2RL (derived from T2RS.2BL and T2BS.2RL) had rye centromeres. All three 3rd generation translocations had hybrid centromeres with approximately half of the centromere derived from rye. There were no indications that the composite structure of the centromere in these chromosomes affected their behavior in mitosis or meiosis. These observations support the notion of a compound structure of the centromere in higher organisms, and indicate that during the centric breakage-fusion event, centromere breakage may occur in different positions along the segment of the chromosome that interacts with the spindle fibers. Normal behavior of the 1st, 2nd, and 3rd generation centric translocations in mitosis and meiosis indicates that, at least in wheat and rye, centromeres are not chromosome specific.

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“…The resulting metacentric chromosomes are actually dicentric and usually one of the centromeres is inactivated to ensure mitotic stability. Complete fission-fusion cycles have been reported for faba beans (Vicia faba L.) (Schubert et al, 1995) and for wheat-rye translocations (Lukaszewski, 1993(Lukaszewski, , 1994(Lukaszewski, , 1997. Although several steps are required to produce Robertsonian translocations (Badaeva et al, 1995), they are widespread in plants (Jones, 1978), animals (White, 1973), and humans (Page et al, 1996;Sullivan et al, 1996) and have played a significant role in karyotype evolution.…”

mentioning

confidence: 98%

Robertsonian translocations in wheat arise by centric misdivision of univalents at anaphase I and rejoining of broken centromeres during interkinesis of meiosis II

Friebe¹,

Zhang²,

Linc³

et al. 2005

Cytogenet Genome Res

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The mechanism of origin of Robertsonian translocations was investigated in plants monosomic for chromosome 1A of wheat and 1H^t of Elymus trachycaulus by GISH. Chromosomes 1A and 1H^t stayed univalent in all metaphase I cells analyzed, suggesting that Robertsonian translocations do not originate from meiotic recombination in centromeric regions with shared DNA sequence homology. At ana-/telophase I, the 1H^t and 1A univalents underwent either chromosome or chromatid segregation and misdivided in 6–7% of the pollen mother cells. None of the ana-/telophases I analyzed had Robertsonian translocations, which were only observed in 2% of the “half tetrads” at ana-/telophase II. The frequency of Robertsonian translocations observed at ana-/telophase II corresponds well with the number of Robertsonian translocations (1–4%) detected in progenies derived from plants monosomic for group-1 chromosomes of wheat (1A, 1B, and 1D) and 1H^t of E. trachycaulus. Our data suggest that Robertsonian translocations arise from centric misdivision of univalents at ana-/telophase I, followed by segregation of the derived telocentric chromosomes to the same nucleus, and fusion of the broken ends during the ensuing interkinesis.

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Alteration of basic chromosome number by fusion–fission cycles

Cited by 25 publications

References 12 publications

Comparative linkage maps suggest that fission, not polyploidy, underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae)

Comparative linkage maps suggest that fission, not polyploidy, underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae)

The centromere structure in Robertsonian wheat-rye translocation chromosomes indicates that centric breakage-fusion can occur at different positions within the primary constriction

Robertsonian translocations in wheat arise by centric misdivision of univalents at anaphase I and rejoining of broken centromeres during interkinesis of meiosis II

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