Evolution of holocentric chromosomes: Drivers, diversity, and deterrents

Senaratne, Aruni P.; Cortes-Silva, Nuria; Drinnenberg, Ines A.

doi:10.1016/j.semcdb.2022.01.003

Cited by 25 publications

(23 citation statements)

References 126 publications

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“…We also delineate the linear organization of B. mori chromosome into large center and arm regions. The similarity to the linear chromosomal organization of C. elegans might reflect convergent evolution along the two holocentric lineages that evolved independently from different monocentric ancestors 34,35 .…”

Section: Bombyx Mori Linear Genome Organizationmentioning

confidence: 99%

Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth

Gil,

Navarrete,

Rosin

et al. 2023

Preprint

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The hallmarks of chromosome organization in multicellular eukaryotes are chromosome territories (CT), chromatin compartments, and different types of domains, including topologically associated domains (TADs). Yet, most of these concepts derive from analyses of organisms with monocentric chromosomes. Here we describe the 3D genome architecture of an organism with holocentric chromosomes, the silkwormBombyx mori. At the genome-wide scale,B. morichromosomes form highly separated territories and lack substantial trans contacts. As described in other eukaryotes,B. morichromosomes segregate into an active A and an inactive B compartment. Remarkably, we also identify a third compartment, Secluded »S», with a unique contact pattern. Compartment S shows strong enrichment of short-range contacts and depletion of long-range contacts. It hosts a unique combination of genetic and epigenetic features, localizes at the periphery of CTs and shows developmental plasticity. Biophysical modeling shows that formation of such secluded domains requires a new mechanism – a high density of extruded loops within them along with low level of extrusion and compartmentalization of A and B. Together with other evidence of loop extrusion in interphase, this suggests SMC-mediated loop extrusion in this insect. Overall, our analyses highlight the evolutionary plasticity of 3D genome organization driven by a new combination of known processes.

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Section: Bombyx Mori Linear Genome Organizationmentioning

confidence: 99%

Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth

Gil,

Navarrete,

Rosin

et al. 2023

Preprint

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“…Such fusions may be advantageous if autosomes harbor sexually antagonistic polymorphisms (Blackmon et al 2017) and may appear particularly feasible in the Lepidoptera exhibiting holocentric chromosomes. That is, lepidopteran chromosomes have centromere activity along their entire length (as opposed to a single point centromere), making segregation during meiosis relatively robust to chromosome fusions and fissions (Luktanov et al 2018; Senaratne et al 2022). An alternative hypothesis holds that the lepidopteran W derives from a supernumerary (non-essential) B chromosome recruited for female-specific performance and that started to segregate with the Z chromosome (Lukhtanov 2000; Dalikova et al 2017; Fraïsse et al 2017; Lewis et al 2021).…”

Section: Introductionmentioning

confidence: 99%

Chromosome-level assemblies of thePieris manniibutterfly genome suggest Z-origin and rapid evolution of the W chromosome

Blattner

Ruffener

Berner

2023

Preprint

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The insect order Lepidoptera (butterflies and moth) represents the largest group of organisms with ZW/ZZ sex determination. While the origin of the Z chromosome predates the evolution of the Lepidoptera, the W chromosome is considered younger, but its origin is debated. To shed light on the origin of the lepidopteran W, we here produce chromosome-level genome assemblies for the butterfly Pieris mannii, and compare the sex chromosomes within and between P. mannii and its sister species P. rapae. Our analyses clearly indicate a common origin of the W chromosomes of the two Pieris species, and reveal similarity between the Z and W in chromosome sequence and structure. This supports the view that the W originates from Z-autosome fusion rather than from a redundant B chromosome. We further demonstrate the extremely rapid evolution of the W relative to the other chromosomes and argue that this may preclude reliable conclusions about the origin of the W based on comparisons among distantly related Lepidoptera. Finally, we find that sequence similarity between the Z and W chromosomes is greatest toward the chromosome ends, perhaps reflecting selection for the maintenance of recognition sites essential to chromosome segregation. Our study highlights the utility of long-read sequencing technology for illuminating chromosome evolution.

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“…Holocentromeres have arisen several times independently among animals and plants, such as in the Cyperaceae (sedges) family (Melters et al, 2012;Escudero et al, 2016;Senaratne et al, 2022). The genus Rhynchospora Vahl (beaksedges) is the third largest clade of Cyperaceae (Araújo et al, 2012), with about 400 species distributed worldwide (POWO, 2023).…”

Section: Introductionmentioning

confidence: 99%

Oligo-barcodes illuminate holocentric karyotype evolution inRhynchospora(Cyperaceae)

Mata-Sucre,

Parteka,

Ritz

et al. 2023

Preprint

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Holocentric karyotypes are assumed to rapidly evolve through chromosome fusions and fissions due to the diffuse nature of their centromeres. Here, we took advantage of the recent availability of a chromosome-scale reference genome forRhynchospora breviuscula, a model species of this holocentric genus, and developed the first set of oligo-based barcode probes for a holocentric plant. These probes were applied to 13 additional species of the genus, aiming to investigate the evolutionary dynamics driving the karyotype evolution inRhynchospora. The two sets of probes were composed of 27,392 (green) and 23,968 (magenta) oligonucleotides, and generated 15 distinct FISH signals as a unique barcode pattern for the identification of all five chromosome pairs of theR. breviusculakaryotype. Oligo-FISH comparative analyzes revealed different types of rearrangements, such as fusions, fissions, putative inversions and translocations, as well as genomic duplications among the analyzed species. Two rounds of whole genome duplication (WGD) were demonstrated inR. pubera, but both analyzed accessions differed in the complex chain of events that gave rise to its large, structurally diploidized karyotypes with 2n= 10 or 12. Considering the phylogenetic relationships and divergence time of the species, the specificity and synteny of the probes were maintained up to species with a divergence time of ∼25 My. However, karyotype divergence in more distant species hindered chromosome mapping and the inference of specific events. This barcoding system is a powerful tool to study chromosomal variations and genomic evolution in holocentric chromosomes ofRhynchosporaspecies.

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Evolution of holocentric chromosomes: Drivers, diversity, and deterrents

Cited by 25 publications

References 126 publications

Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth

Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth

Chromosome-level assemblies of thePieris manniibutterfly genome suggest Z-origin and rapid evolution of the W chromosome

Oligo-barcodes illuminate holocentric karyotype evolution inRhynchospora(Cyperaceae)

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