Holocentric plant meiosis: first sisters, then homologues

Abstract

Meiosis is a crucial process of sexual reproduction by forming haploid gametes from diploid precursor cells. It involves 2 subsequent divisions (meiosis I and meiosis II) after one initial round of DNA replication. Homologous monocentric chromosomes are separated during the first and sister chromatids during the second meiotic division. The faithful segregation of monocentric chromosomes is realized by mono-orientation of fused sister kinetochores at metaphase I and by bi-orientation of sister kinetochores at metaphase II. Conventionally this depends on a 2-step loss of cohesion, along chromosome arms during meiosis I and at sister centromeres during meiosis II.

However, meiosis in organisms with holocentric chromosomes illustrates that our views of meiotic chromosome arrangement and control of meiosis based on observations of monocentric chromosomes may not apply to all organisms. Two recent publications in Nature Communications from the Schlögelhofer¹ and Houben² laboratories show independently that the plants Luzula elegans (Juncaceae), Rhynchospora pubera and R. tenuis (Cyperaceae) invert the order of meiotic chromatid segregation events. In these species sister chromatids separate already during meiosis I. This behavior is caused by the holokinetic centromeres forming a longitudinal centromere-like groove along each sister chromatid.

Likely, due to their alternative chromosome organization, species with holocentric chromosomes cannot make use of the 2-step cohesion loss during meiosis typical for monocentric chromosomes that requires the distinction between chromosome arms and sister centromeres. As adaptation, species with holocentric chromosomes have evolved different solutions to handle them during meiosis, such as chromosome remodeling (for review³) or functional monocentric chromosomes (for review⁴). The existence of another proposed phenomenon termed inverted or post-reductional meiosis has been proposed, but ultimate proof was missing so far. The strongest support for its existence came from a study⁵ of a diploid mealybug individual with a heteromorphic chromosome pair.

The above-mentioned plant species display a holocentric chromosome architecture and behavior throughout meiosis. Initial prophase I events proceed cytologically similar as those known from monocentric chromosomes, e.g. telomere bouquet, axis and synaptonemal complex formation occur. In addition, meiotic double strand breaks are induced and processed likely even in the achiasmatic chromosomes of R. tenuis. Astonishing, in contrast to a monopolar sister centromere orientation, the holokinetic sister centromeres are not fused and interact individually bi-orientated with the meiotic spindle (Fig. 1). This results in the separation of sister chromatids already during meiosis I. To ensure faithful haploidization the homologous non-sister chromatids remain usually terminally linked after metaphase I by chromatin threads until metaphase II. Then they separate at anaphase II. Thus, an inverted sequence of meiotic sister chromatid segregation occurs. This meiotic mode is accurate for chiasmatic holocentric chromosomes, whereas ∼30% of the achiasmatic chromosomes of R. pubera show meiotic mis-segregation. This alternative meiotic progression is most likely one of the possible adaptations to deal with a holocentric chromosome structure and behavior during meiosis.

Figure 1.

Model illustrating the structure of meiotic chromosomes and the sequence of meiotic segregation events in L. elegans. Holocentric U-shaped rod-like bivalents align at metaphase I in such a manner that sister chromatids and not homologues separate. Homologous non-sister chromatids are terminally linked by chromatin threads until metaphase II. Then, during meiosis II, the associated homologous non-sister chromatids become holokinetically separated.

In L. elegans chromatin threads are heterochromatic and enriched by satellite DNAs. Similarly, meiotic chromatin stretches are also found in both Rhynchospora species. Their occurrence in achiasmatic R. pubera chromosomes suggests that these chromatin threads are formed in a chiasma-independent manner. Interestingly, they are not described for holocentric chromosomes using a different meiotic mode like nematodes. Thus, chromatin threads are likely conducive for holocentric chromosomes undergoing an inverted meiotic chromatid segregation process. Noteworthy, monocentric meiotic chromosomes can also be associated via chromatin stretches (e.g., in Drosophila⁶ or crane flies⁷).

In future the following questions need to be addressed for a better understanding of this peculiar type of meiosis: i) How is the meiotic recombination process regulated in holocentric chromosomes undergoing alternative meiotic chromatid segregation? ii) What keeps the homologues together until anaphase I and what keeps the homologous non-sister chromatids together at their ends after metaphase I until metaphase II – are terminal (satellite DNA-enriched) chromatin threads a prerequisite for an inverted meiosis, are cohesins involved, or other mechanisms? iii) Do species with holocentric chromosome possess specific meiotic proteins? To address some of these questions genes involved in meiotic kinetochore formation, recombination and cohesion will be analyzed based on deep sequencing of the meiotic transcriptome and on cytological studies.

As holocentricity has arisen multiple times during evolution since it is present in independent eukaryotic lineages including green algae, protozoans, invertebrates and higher plants even more meiotic adaptations than the 3 so far described basic variants are likely. Further studies of species with holocentric chromosomes will broaden our mainly monocentric chromosome-biased knowledge on meiotic chromosome segregation and may lead to further interesting findings.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.