Holocentric chromosomes

Abstract

Holocentric chromosomes possess multiple kinetochores along their length rather than the single centromere typical of other chromosomes [1]. They have been described for the first time in cytogenetic experiments dating from 1935 and, since this first observation, the term holocentric chromosome has referred to chromosomes that: i. lack the primary constriction corresponding to centromere observed in monocentric chromosomes [2]; ii. possess multiple kinetochores dispersed along the chromosomal axis so that microtubules bind to chromosomes along their entire length and move broadside to the pole from the metaphase plate [3]. These chromosomes are also termed holokinetic, because, during cell division, chromatids move apart in parallel and do not form the classical V-shaped figures typical of monocentric chromosomes [4-6]. Holocentric chromosomes 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 [7,8]. As a consequence of their diffuse kinetochores, holocentric chromosomes may stabilize chromosomal fragments favouring karyotype rearrangements [9,10]. However, holocentric chromosome may also present limitations to crossing over causing a restriction of the number of chiasma in bivalents [11] and may cause a restructuring of meiotic divisions resulting in an inverted meiosis [12]. Evolution and structure of holocentric chromosomes Evolution of holocentric chromosomes Holocentric chromosomes were described for the first time in 1935 to identify chromosomes with a diffuse kinetochore (or with a diffuse kinetochore activity) making these chromosomes able to bind to microtubules along their entire length. In the last decades, several studies assessed that the same behaviour during mitosis can be observed not only for holocentric/ holokinetic chromosomes, but also for polykinetic chromosomes that contain numerous (but discrete) microtubule-binding sites, but the term "holocentric/holokinetic" is still used for both [1,5,7]. Before molecular methods became available, the presence of holocentric chromosomes was evaluated mostly using cytology and, considering that many species are difficult to study cytologically, it can be surmised that the true presence of holocentrism may be underestimated. In addition, there are several taxa, whose chromosomes are still uncharacterized, but their

Chromosome Fusion Affects Genetic Diversity and Evolutionary Turnover of Functional Loci but Consistently Depends on Chromosome Size

“…Comparing the ten smallest Heliconiini chromosomes with their homologues in Melitaea cinxia , it seems clear that chromosome lengths have been highly stable over this long evolutionary time period. Our data therefore seem to contradict the notion that holocentric chromosomes have uniform distributions of GC, repeats and gene content across chromosomes ( Grbić et al 2011 ; Mandrioli and Manicardi 2020 ), and contrasts with monocentric chromosomes where these features are compartmentalized to GC-rich and GC-poor regions ( Bernardi et al 1985 ). Whether the uneven distributions we observe are favored due to meiotic pairing or some other selective driver remains to be tested.…”

“…In Heliconius butterflies, 10 pairs of the 31 ancestral chromosomes are thought to have fused, resulting in 21 chromosomes, whereas the ancestral chromosome number is retained in their sister genus Eueides and most other outgroup genera within Heliconiini ( Davey et al 2016 ). The impact of these chromosome fusions on the recombination landscape may be especially pronounced in Heliconius due to their holocentric chromosomes where multiple kinetochores, rather than a single centromere, may favor the escape of some of the deleterious effects of chromosome fusions ( Mandrioli and Manicardi 2020 ). There also appears to be a strict rule of one crossover per chromosome per meiosis in this clade ( Davey et al 2016 ).…”

Chromosome fusion affects genetic diversity and evolutionary turnover of functional loci, but consistently depends on chromosome size

“…Comparing the ten smallest Heliconiini chromosomes with their homologues in Melitaea cinxia, it seems clear that chromosome lengths have been highly stable over this long evolutionary time period. Our finding seems to contradict the notion that holocentric chromosomes have uniform distributions of GC, repeats and gene content across chromosomes (22,29), contrasting with monocentric chromosomes with localized centromeres, in which they are compartmentalized to GC-rich and GC-poor regions (30). Whether the uneven distributions we observe are favoured due to meiotic pairing or some other selective driver remains to be tested.…”

“…In Heliconius butterflies, 20 of the 31 ancestral chromosomes are thought to have fused, resulting in 21 chromosomes, with the ancestral chromsome number still present in their sister genus Eueides (21). The impact of chromosome fusions on the recombination landscape may be especially pronounced in Heliconius, as holocentric species may escape some of the deleterious effects of chromosome fusions (22) and there appears to be a strict rule of one crossover per chromosome per meiosis (21). Fused chromosomes should therefore have a reduced recombination rate per base pair (bp) compared to their ancestral, unfused progenitors.…”

Karyotype asymmetry in Cuscuta L. subgenus Pachystigma reflects its repeat DNA composition

“…Three species of subgenus Cuscuta (holocentric), C. epithymum (2 n = 14), C. europaea L. (2 n = 14), and C. epilinum Weihe (2 n = 6 x = 42), had a reduction in the chromosome number. In the case of this subgenus, there may have been chromosomal fusion events, since holocentric chromosomes have diffuse kinetochores, and consequently these chromosomes can stabilize fragments or fused chromosomes favouring rearrangements (Mandrioli and Manicardi, 2020).…”