Asynapsis and unreduced gamete formation in a Trifolium interspecific hybrid

Abstract

Background Unreduced gametes, a driving force in the widespread polyploidization and speciation of flowering plants, occur relatively frequently in interspecific or intergeneric hybrids. Studies of the mechanisms leading to 2n gamete formation, mainly in the wheat tribe Triticeae have shown that unreductional meiosis is often associated with chromosome asynapsis during the first meiotic division. The present study explored the mechanisms of meiotic nonreduction leading to functional unreduced gametes in an interspecific Trifolium (clover) hybrid with three sub-genomes from T. ambiguum and one sub-genome from T. occidentale. Results Unreductional meiosis leading to 2n gametes occurred when there was a high frequency of asynapsis during the first meiotic division. In this hybrid, approximately 39% of chromosomes were unpaired at metaphase I. Within the same cell at anaphase I, sister chromatids of univalents underwent precocious separation and formed laggard chromatids whereas paired chromosomes segregated without separation of sister chromatids as in normal meiosis. This asynchrony was frequently accompanied by incomplete or no movement of chromosomes toward the poles and restitution leading to unreduced chromosome constitutions. Reductional meiosis was restored in progeny where asynapsis frequencies were low. Two progeny plants with approximately 5 and 7% of unpaired chromosomes at metaphase I showed full restoration of reductional meiosis. Conclusions The study revealed that formation of 2n gametes occurred when asynapsis (univalent) frequency at meiosis I was high, and that normal gamete production was restored in the next generation when asynapsis frequencies were low. Asynapsis-dependent 2n gamete formation, previously supported by evidence largely from wheat and its relatives and grasshopper, is also applicable to hybrids from the dicotyledonous plant genus Trifolium. The present results align well with those from these widely divergent organisms and strongly suggest common molecular mechanisms involved in unreduced gamete formation.

Introgression of Trifolium ambiguum Into Allotetraploid White Clover (Trifolium repens) Using the Ancestral Parent Trifolium occidentale as a Bridging Species

“…All three BC 2 plants had 32 or 33 chromosomes and moderate to high fertilities (Table 3), suggesting that any sub-genomic imbalances did not drastically reduce fertility. A high frequency of asynapsis (i.e., univalents) at meiosis can be associated with the generation of 2n gametes in interspecific hybrids (Ansari et al, 2022). However, in the materials analyzed, no products of 2n gametes were observed.…”

Polyploidy in Orchid Breeding, Advances and Perspectives

“…In eukaryotes, meiotic cell division halves the chromosome number in gametes via a single DNA replication followed by two events of chromosome segregation 26 . During meiosis I, homologous chromosomes should pair and synapse and exchange genetic information via recombination.…”

“…However, in the Arabidopsis mutants parallel-spindle 1 or Jason, disturbed orientation of the spindle leads to a similar effect 31 . These features are often referred to as examples of FDR 31 and are somewhat common in amphihaploid-and polyhaploid-wide F1 hybrids in which homology is very low and meiotic pairing does not occur 26 . Thus, some researchers consider that this type of meiotic non-reduction is better described as asynaptic-or univalent-dependent 26 .…”

Advances and Perspectives for Polyploidy Breeding in Orchids

“…In eukaryotes, meiotic cell division halves the chromosome number in gametes via a single DNA replication followed by two events of chromosome segregation [ 39 ]. During meiosis I, homologous chromosomes should pair and synapse and exchange genetic information via recombination.…”

“…However, in the Arabidopsis mutants parallel-spindle 1 or Jason , disturbed orientation of the spindle leads to a similar effect [ 43 ]. These features are often referred to as examples of FDR [ 43 ] and are somewhat common in amphihaploid- (see Table 1 ) and polyhaploid-wide (see Table 1 ) F 1 hybrids in which homology is very low and meiotic pairing does not occur [ 39 ]. Thus, some researchers consider that this type of meiotic non-reduction is better described as asynaptic- or univalent-dependent [ 39 ].…”