Meiosis Progression and Recombination in Holocentric Plants: What Is Known?

Abstract

Differently from the common monocentric organization of eukaryotic chromosomes, the so-called holocentric chromosomes present many centromeric regions along their length. This chromosomal organization can be found in animal and plant lineages, whose distribution suggests that it has evolved independently several times. Holocentric chromosomes present an advantage: even broken chromosome parts can be correctly segregated upon cell division. However, the evolution of holocentricity brought about consequences to nuclear processes and several adaptations are necessary to cope with this new organization. Centromeres of monocentric chromosomes are involved in a two-step cohesion release during meiosis. To deal with that holocentric lineages developed different adaptations, like the chromosome remodeling strategy in Caenorhabditis elegans or the inverted meiosis in plants. Furthermore, the frequency of recombination at or around centromeres is normally very low and the presence of centromeric regions throughout the entire length of the chromosomes could potentially pose a problem for recombination in holocentric organisms. However, meiotic recombination happens, with exceptions, in those lineages in spite of their holocentric organization suggesting that the role of centromere as recombination suppressor might be altered in these lineages. Most of the available information about adaptations to meiosis in holocentric organisms is derived from the animal model C. elegans. As holocentricity evolved independently in different lineages, adaptations observed in C. elegans probably do not apply to other lineages and very limited research is available for holocentric plants. Currently, we still lack a holocentric model for plants, but good candidates may be found among Cyperaceae, a large angiosperm family. Besides holocentricity, chiasmatic and achiasmatic inverted meiosis are found in the family. Here, we introduce the main concepts of meiotic constraints and adaptations with special focus in meiosis progression and recombination in holocentric plants. Finally, we present the main challenges and perspectives for future research in the field of chromosome biology and meiosis in holocentric plants.

Keywords: centromere; cohesion; holocentric chromosome; inverted meiosis; meiotic recombination.

Figure 1

General model for canonical meiosis in monocentric organisms vs. inverted meiosis (both chiasmatic and achiamatic) in holocentric plants. (A) Canonical meiosis: During meiosis I reciprocal genetic exchange between homologs (crossovers) occurs, sisters-chromatids mono-orient via fused sister-centromeres and segregate to the same poles. During meiosis II, sisters-chromatids bi-orient and segregate to the opposite poles, resulting in four haploid gametes at the end. (B) Schematic representation of chiasmatic inverted meiosis observed in R. pubera (from metaphase I only one bivalent is illustrated for better understanding). During meiosis I, COs take place but the difference is that, centromeres from sisters are not fused, sister chromatids bi-orient and segregate to the opposite poles already at anaphase I. During meiosis II homologous non-sisters align, bi-orient and segregate to the opposite poles, resulting in four haploid gametes similar to canonical meiosis. (C) Schematic representation of achiasmatic inverted meiosis observed in R. tenuis. The sequence of events during inverted meiosis observed in R. tenuis is similar to that of R. pubera, but meiosis in R. tenuis is reported to be achiasmatic i.e., crossover formation doesn't occur during prophase I. As a result, four univalents are observed during diakinesis instead of two bivalents.

Figure 2

Chromatin threads and cohesion in Luzula chromosomes. (A) Model highlighting the structural adaptations during inverted meiosis of Luzula elegans (see Heckmann et al., 2014) for further details). A rod bivalent with single crossover is illustrated in the model. CENH3 (centromeric protein) appears as a single linear line and centromeres of sisters are not fused. The sister chromatids bi-orient and attach to microtubules from opposite poles. Homologous non-sister chromatids associate with each other by end-to-end connections reported to be established by satellite elements, which maintain non-sister chromatids together up to meiosis II. (B,C) CENH3 and Le α-kleisin distribution during mitotic metaphase of Luzula elegans (B) and Hordeum vulgare (C) (see Ma et al., 2016) for further details). In the holocentric plant Luzula, CENH3(centromeric protein) appear as linear signals during mitotic metaphase. Le α-kleisin appears in the CENH3 regions and not between sister centromeric units. Whereas, in case of the monocentric plant Hordeum vulgare, the same Le α-kleisin is reported to present in the centromeric regions as well as establishing a connection between the sister centromeres.

Figure 3

Meiotic recombination in holocentric plants. (A) Scheme of what is known about distribution of hotspots for meiotic recombination with respect to centromere organization on monocentric and holocentric plant chromosomes. (B) Types of CO and bivalent formation and corresponding models with regard to centromeric units distribution in R. pubera. Bivalent microscopic images were made by M. Castellani.