Annals of Botany

What are holocentric chromosomes good for?

Possessing holocentric chromosomes may confer an advantage in clastogenic conditions and environments.

Holocentric chromosomes, unlike monocentric chromosomes, attach spindle microtubules along their entire length; they have long been considered as a peripheral peculiarity with an unclear function. Zedek and Bureš summarise evidence that the key to their evolutionary role is the tolerance to fragmentation whereby holocentric chromosomes confer an advantage in times of exposure to cosmic radiation, desiccation and other chromosome-breaking factors.

Fragmentation of holocentric and monocentric chromosomes and gamma radiation response in monocentrics and holocentrics.
Fragmentation of holocentric and monocentric chromosomes and gamma radiation response in monocentrics and holocentrics. Top: holocentric chromosomes and monocentric chromosomes are the two alternative chromosomal structures that have evolved in eukaryotes. The reason why holocentric chromosomes tolerate fragmentations is that they attach spindle microtubules along their entire length during cell divisions, and therefore all their fragments are normally inherited by daughter cells that receive a proper set of genetic material. Monocentric chromosomes, by contrast, attach spindle microtubules to the kinetochore (shown in red), which is formed in a small centromeric region, and their fragments without a centromere are distributed randomly to daughter cells and eventually lost, which is often lethal. Bottom: gamma irradiation causes chromosomal fragmentations that need to be repaired, and for that purpose, the cell cycle is arrested in G2 phase in plants. Therefore, the number of G2 cells in gamma-irradiated plants should increase, resulting in a higher G2/G1 ratio. If the G2/G1 ratio of an irradiated plant is divided by the G2/G1 ratio of a non-irradiated control, the resulting value shows the overall response in cell cycle arrest to gamma irradiation (y-axis). These values for 13 monocentric and ten holocentric species are shown in the two box-plots. Relative to monocentrics, there is basically no increase in the G2/G1 ratio in holocentrics after irradiation, suggesting that holocentrics cope with chromosomal fragmentation more effectively. Monocentric species are represented by Asplenium bulbiferumBegonia boweraeCymbalaria muralisEuonymus japonicusKalanchoë delagoensisLavandula angustifoliaLysimachia nemorumPeperomia glabellaPisum sativumPlectranthus amboinicusSedum spuriumSenecio articulatus and Silene nocturna. Holocentric species are represented by Carex grayiC. humilisC. piluliferaDrosera capensisD. scorpioidesEleocharis palustrisIsolepis proliferaLuzula sylvaticaPrionium serratum and Scirpus cernuus. See Zedek et al. (2016) for further details.

They conclude that holocentric chromosomes may have played a major role in the evolutionary trajectory half a billion years ago; the first land colonisers had to cope with intense radiation and desiccation, and phylogenetic evidence suggests that holocentricity may underlie the resilient genetic makeup of the ancestors of land plants and animals.

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