Cytomixis-like chromosomes/chromatin elimination from pollen mother cells (PMCs) in wheat-rye allopolyploids

Abstract

Polyploidy is an important event and major force in plant speciation. Amongst the polyploids, allopolyploids have attracted special attention to investigate genetic and epigenetic mechanisms. Also, they are the means for the development of new genotypes and genomic combinations to facilitate genetic enhancement and agricultural productivity. Whereas natural allopolyploids are genetically stable and well adapted, the newly synthesized ones are highly unstable. This instability is manifested into alterations at genomic and/or phenotypic level. Here we present the phenomenon of direct chromosome/chromatin elimination from pollen mother cells (PMCs) in wheat-rye hybrids as one aspect of instability leading to irregular meiosis and disturbances in meiotic process. One of the prominent irregularities noticed is peripherally separated uncondensed or pycnotic masses of chromatin in all meiotic stages. We have observed that this chromatin undergoes elimination by budding-like way, whereby a "mini-cell" is created. It was also found that nucleoli are the first to be eliminated along with a small mass of chromatin. By means of GISH we have shown that both rye and wheat chromatin might be eliminated. In the separated groups of chromosomes/ chromatin neither DNaseI nor DNase II activity was detected. Immunolocalization of tubulin allowed for differentiation between chromatin elimination from microspores and elimination from earlier stages of meiosis. It was noticeable, that in microspores special cytoskeleton structure pushing micronuclei out from the cells was created. Elimination occurred before and after meiosis as well as in each stage of meiotic division, but its intensity varied, depending on the PMC. The basis of the elimination mechanism might be the same as in cytomixis, because both phenomena share common symptoms, although cytomixis per se was rare in the analyzed hybrids.

Chromosome Elimination in Intergeneric Hybrid of <i>Oryza sativa</i> × <i>Luziola peruviana</i>

“…It is possible that some factors may trigger the deletion for stabilization of the newly formed genome, however, the base of the cellular mechanisms involved in the process of chromosome elimination are poorly understood [13]. Genomic conflict occurs in meiosis, possibly by asynchronism and cell cycle length of the genomes involved, time differences in replication between parental species that leads to strand breaks and genomic rearrangements and that may be of unknown signals of protein synthesis or post-translational changes in existing proteins [12]. The complexity of the events involved in the cell cycle difficult to distinguish between different hypotheses.…”

“…Processes of chromosome elimination by problem in pairing and segregation associated with chromatin degradation or fragmentation of chromosomes, may be the reason for the changes in the chromosome number [12], including uniparental non-disjunction of univalent chromosomes in metaphase; if the force to one of the poles is more stronger than other, the chromosomes move toward to pole without separation of sister chromatids, causing nondisjunction [15] [17]. Lagging chromosomes due to spindle fibers fail to join the centromere, the chromatids were immobilized on the periphery of the cell and did not enter the polar regions where new nuclei were formed The immobilization of chromosomes in the cell periphery may be related to malfunction of the sister kinetochores that leading to anchorage failures of spindle [14], if the force in both poles is equal, the chromosomes do not move from the equatorial plate and are excluded from the nuclei of the daughter cells [15].…”

“…Chromosome elimination is established as a dynamic process of genome stabilization that occurs during hybridization and has been well explored and investigated in wheat with different kinds of Poaceae, among other intergeneric hybrid [12] [13]. Partial or total elimination chromosomes and exchange between parental chromosomes frequently occur during early development of the progeny [14], and present a barrier to the transfer of desirable traits from wild species to cultivated, but may act in favor of crop improvement programs [15] [16].…”

“…During meiosis the univalent chromosomes lagging at anaphase I and II, and micronuclei formation during telophase I and II cause meiotic disorders due to failure to enter in the newly nucleus and finally are eliminated [12] [14]. The chromosome elimination by micronuclei formation in intergeneric hybrids is given by the nonsegregation of chromosomes or fragments during karyokinesis and the extrusion of chromatin during interphase [15].…”

New insights into cytomixis: specific cellular features and prevalence in higher plants

“…Diploid gametes can be produced in several ways, and cytomixis might well be one of them (Falistocco et al 1995;Ghaffari 2006;Lattoo et al 2006). On the other hand, cytomixis may be involved in elimination of the "surplus" DNA by discharging part of the chromatin from the nucleus to the cytoplasm of another cell, thereby providing for either stabilization of a polyploid genome or return from a polyploid to a diploid state (Cheng et al 1987;Baptista-Giacomelli and Pagliarini 2000;Zhou 2003;Kalinka et al 2010). …”