Abstract
Due to reciprocal chromosomal translocations, many species of Oenothera (evening primrose) form permanent multichromosomal meiotic rings. However, regular bivalent pairing is also observed. Chiasmata are restricted to chromosomal ends, which makes homologous recombination virtually undetectable. Genetic diversity is achieved by changing linkage relations of chromosomes in rings and bivalents via hybridization and reciprocal translocations. Although the structural prerequisite for this system is enigmatic, whole-arm translocations are widely assumed to be the mechanistic driving force. We demonstrate that this prerequisite is genome compartmentation into two epigenetically defined chromatin fractions. The first one facultatively condenses in cycling cells into chromocenters negative both for histone H3 dimethylated at lysine 4 and for C-banding, and forms huge condensed middle chromosome regions on prophase chromosomes. Remarkably, it decondenses in differentiating cells. The second fraction is euchromatin confined to distal chromosome segments, positive for histone H3 lysine 4 dimethylation and for histone H3 lysine 27 trimethylation. The end-segments are deprived of canonical telomeres but capped with constitutive heterochromatin. This genomic organization promotes translocation breakpoints between the two chromatin fractions, thus facilitating exchanges of end-segments. We challenge the whole-arm translocation hypothesis by demonstrating why reciprocal translocations of chromosomal end-segments should strongly promote meiotic rings and evolution toward permanent translocation heterozygosity. Reshuffled end-segments, each possessing a major crossover hot spot, can furthermore explain meiotic compatibility between genomes with different translocation histories.
Highlights
The plant genus Oenothera is an adaptable and highly successful taxon
Nuclei stained with DAPI or chromomycin A3 (CMA3) with facultative chromocenters and minute blocks of terminal heterochromatin. (O) Oe. biennis strain suaveolens Grado
Nucleus with facultative chromocenters (DAPI staining, top) that are negative for H3K4me2. (P) Oe. elata ssp hookeri strain johansen Standard
Summary
The plant genus Oenothera (evening primrose, Onagraceae, 2n = 2x = 14) is an adaptable and highly successful taxon. Due to reciprocal chromosomal translocations, it extensively forms multichromosomal rings at meiosis (Cleland, 1972; Golczyk et al, 2008; see Supplemental Figure 1 for details). Meiotic configurations can range from a single ring, where all chromosomes are involved in catenation, through intermediate forms with rings and bivalents, to solely bivalents (Supplemental Figure 1). A drastic restriction of homologous recombination to chromosomal ends is observed throughout the genus: In Oenothera, chromosomal endsegments are the only sites throughout the genome where chiasmata are formed. The terminal chiasmata are obligatory for proper and regular meiosis I segregation (Cleland, 1972). Techniques of classical and molecular genetics show unusually low levels of crossovers, allowing Oenothera genomes to be regarded as essentially nonrecombining (Rauwolf et al, 2008, 2011)
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