Holocentric chromosome

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Holocentric chromosomes are

sister chromatids move apart in parallel and do not form the classical V-shaped figures typical of monocentric chromosomes.[4][5][6]

Holocentric chromosomes have evolved several times during both animal and plant evolution, and are currently reported in about eight hundred diverse species, including plants, insects, arachnids, and nematodes.

bivalents,[11] and may cause a restructuring of meiotic divisions resulting in an "inverted" meiosis.[12]

Evolution

Holocentric chromosomes were described for the first time by Franz Schrader in 1935, who identified

microtubules along their entire length rather than at a single primary constriction, as is typical of chromosomes with centromeres. In recent decades, several studies determined that this behaviour during mitosis can be observed in holocentric/holokinetic chromosomes but also in polykinetic chromosomes, which contain numerous (but discrete) microtubule-binding sites; even so, the term “holocentric/holokinetic” is still commonly used to refer to both processes.[1][5][7]

acentric chromosome
fragments cannot be attached to microtubules during metaphase (M) and they are subsequently lost during anaphase (A). On the contrary, chromosomal breakage of a holocentric chromosome results in chromosomal fragments that retain kinetic activity due to the chromosome-wide centromere extension and can be properly inherited.

Before molecular methods became available, the presence of holocentric chromosomes was evaluated mostly using

DNA damage resulting from desiccation and/or other chromosome-breaking factors.[14]

Despite these differences, holocentric chromosomes present intrinsic benefits since chromosomal mutations, such as fissions and fusions, are potentially neutral in holocentric chromosomes with respect to monocentric ones. However, the hypothesis of holocentrism as an anticlastogenic adaptation needs more systematic testing, including both controlled laboratory experiments and field studies across clastogenic gradients and large-scale phylogenetic analyses.[8] At the same time, Nagaki et al.[15] proposed that holocentrism can be easily acquired during plant and animal evolution by a slight difference in the kinetochore origin. In particular, they hypothesized that if the direction of kinetochore origin turns by 90° and occurs along the chromosome axes up to the telomeric regions, it is possible to “generate” holocentric chromosomes without any further step.

Structure

A detailed molecular analysis of the

spindle poles, in contrast to monocentric ones in which pulling forces are exerted on a single chromosomal point and chromosome arms trail behind. As a consequence, chromatids of holocentric chromosomes move apart in parallel and do not form the classical V-shaped figures typical of monocentric ones.[4] Moreover, if a holocentric chromosome is fragmented (for instance by X-ray irradiation
), each fragment retains centromere activity and can segregate properly to the poles.


In different organisms

Arthropods

Among

Segestridae),[7][14] millipedes[18] and centipedes.[18] Despite this widespread occurrence, most of the currently available data on holocentrism is related to aphid and lepidopteran species.[7][5] In aphids, holocentric chromosomes have been deeply studied and their ability to stabilize chromosomal fragments has been associated to their phytophagous life style. Indeed, several plants produce chemicals able to induce DNA damage to pest insects. Nicotine, for instance, is a naturally occurring alkaloid found primarily in members of the solanaceous plant family (including Nicotiana tabacum) that can cause replication fork stress resulting in various forms of DNA damage, including chromosomal fragmentations.[19][20] Similar effects have been also reported by other plant-produced molecules, such as caffeine and ethanol.[19][20] In view of their ability to favour the inheritance of chromosomal fragments, holocentrism has been associated to recurrent changes in the karyotypes of some aphid species and in particular in the peach potato aphid Myzus persicae, where both inter- and intra-individual rearranged karyotypes have been also observed.[21][22] Aphids also possess a constitutive expression of the telomerase coding gene so that they can initiate a de novo synthesis of telomere sequences at internal breakpoints, resulting in the stabilization of chromosomal fragments.[23][24] Among non-polyploid animals, Lepidoptera exhibit the highest variance in chromosome number between species within a genus and notable levels of interspecific and intraspecific karyotype variability.[12][25][26] Lepidoptera indeed tolerate chromosomal variations in view of their holokinetic chromosomes, which facilitate the successful inheritance of novel fission or fusion fragments. As a consequence, Lepidoptera can avoid the deleterious consequences of large-scale chromosomal fission and fusion.[12][25][26] Nevertheless, they can sometimes tolerate heterozygosity for multiple rearrangements in hybrids between population with differences in their karyotype, raising questions about additional mechanisms that rescue fertility in chromosomal hybrids. In Lepidoptera, therefore, chromosome evolution is believed to play a role in reinforcing speciation.[12] Comparing the genomes of lepidopteran species it has been also possible to analyse the effect of holocentrism in terms of rate of fixed chromosomal rearrangements. This approach evidenced in Lepidoptera two chromosome breaks per megabase of DNA per Million of years: a rate that is much higher than what observed in Drosophila and it is a direct consequence of the holocentric nature of the lepidopteran genomes.[27][28] At a structural level, insect holocentric chromosomes have not been studied in details, but it is interesting to underline the absence of homologues of CENP-C and CENP-A, previously considered essential for kinetochore functioning in eukaryotes.[29]

Nematodes

The best known group of holocentric species can be found in the

paralogous genes.[36][37]

Plants

In plants, holocentric chromosomes have been found in

epigenetic marks. Indeed, the cell cycle-dependent phosphorylation of serine 10 or serine 28 of H3 (that is typically enriched in pericentric regions of monocentric plant chromosomes) occurs uniformly along the Luzula chromosomes.[53] As previously described in aphids, L. elegans possesses a rapid and efficient de novo telomere formation based on a telomerase-mediated healing process that is active immediately after chromosomal damage by irradiation of chromosomes.[54] Newly formed telomere repeats were cytologially detectable 21 days after irradiation in about 50% of cases, with a complete healing of telomeres after three months favouring the fragment stabilization and karyotype fixation.[54]

Meiosis

In the late 19th century, van Beneden (1883) and Boveri (1890) described meiosis for the first time through a careful observation of germ cell formation in the nematode Ascaris. These observations, together with several further analyses, evidenced that canonical meiosis consists of a first division (called reductional division) that involves the segregation of chromosomal homologs resulting in the reduction of chromosome number, followed by a second division (called equational division) that involves the segregation of sister chromatids. A general rule for meiosis is therefore: first homologs, then sisters.

Schematic comparison of the chromosomal separation occurring during the first meiotic division in standard and inverted meiosis

However, the understanding of the reductional division in meiosis of Ascaris spp. has been obtained by studying the holocentric chromosomes which, in many other taxa, follow a reverse order of meiotic division.[12] Indeed, as reported in several nematodes, in insects belonging to the Hemiptera and Lepidoptera,[55][56] in mites,[57] and in some flowering plants,[8] species with holocentric chromosomes generally present an inverted meiotic sequence, in which segregation of homologs is postponed until the second meiotic division.

Furthermore, in most cases of inverted meiosis the absence of a canonical kinetochore structure has been observed, together with a restriction of the kinetic activity to the chromosomal ends.[12][55][56] These changes are related to the peculiar cohesion occurring in tetrads of the holocentric homologous chromosomes during meiosis that impose obstacles to the releases of chromosomes involved in multiple crossing over events.[55][56][57] In the holocentric chromosomes of C. elegans female meiosis,[58] this problem is circumvented by restricting crossing over to form only a single chiasma per bivalent and triggering the redistribution of kinetochore proteins along the bivalent axis, forming meiosis-specific cup-like structures that uniformly coat each half-bivalent but are excluded from the mid-bivalent region.[58] During anaphase I, C. elegans homologous chromosomes are segregated to the poles by microtubule-pushing from the mid-bivalent regions towards the poles.[58]

In contrast to C. elegans, other organisms with holocentric chromosomes, including both plants and insects,[12][55][56] circumvent this problem by segregating sister chromatids during meiosis I, leading to the term inverted meiosis, in which the order of reductional and equational division is inverted with respect to canonical meiosis. In this case therefore the separation of homologous chromosomes follows rather than precedes the segregation of sister chromatids. However, in order to have a successful inverted meiosis, it is necessary that a bipolar orientation of sister kinetochores occurs, together with their attachment to microtubules from opposite spindle poles in meiosis I. This allows the segregation of sister chromatids to opposite poles in anaphase I (equational division), but requires a mechanism to align and pair homologous chromosomes during the second meiotic division.[55][56][57] Interestingly, the presence of inverted meiosis can also facilitate proper chromosome segregation in hybrids from parental species with differences in their karyotypes or derived by populations with rearranged karyotypes, allowing rescue of the fertility and viability of hybrids and promoting a fast karyotype evolution and possibly chromosomal speciation, as reported in the Lepidoptera.[12]

References

This article was adapted from the following source under a CC BY 4.0 license (2020) (reviewer reports): Mauro Mandrioli; Gian Carlo Manicardi (2020). "Holocentric chromosomes".

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