Tinkering with meiosis

Abstract

Meiosis is at the heart of Mendelian heredity. Recently, much progress has been made in the understanding of this process, in various organisms. In the last 15 years, the functional characterization of numerous genes involved in meiosis has dramatically deepened our knowledge of key events, including recombination, the cell cycle, and chromosome distribution. Through a constantly advancing tool set and knowledge base, a number of advances have been made that will allow manipulation of meiosis from a plant breeding perspective. This review focuses on the aspects of meiosis that can be tinkered with to create and propagate new varieties. We would like to dedicate this review to the memory of Simon W. Chan (1974-2012) (http://www.plb.ucdavis.edu/labs/srchan/).

Figure 1

Chromosome behavior at meiosis. Meiosis consists of two rounds of chromosome segregation following a single replication. At the onset of replication, the sister chromatids are held together by cohesion (purple rings). Homologous chromosomes pair during prophase I and engage in recombination: at least one crossover per pair of homologues is always observed. Crossovers and sister chromatid cohesion ensure that recombined chromosomes are physically linked to form a bivalent at metaphase I. At anaphase I, this cohesion is released except at the centromeres: homologous chromosomes segregate to opposite poles while sister chromatids remain together. At metaphase II, destruction of the centromeric cohesion allows the segregation of sister chromatids to opposite poles starting at anaphase II.

Figure 2. Mutants producing dipoid gametes in Arabidopsis thaliana

(A) Schematic representation of chromosome behavior at mitosis and at meiosis in wild type and in mutants producing diploid gametes. For simplification only two pairs of chromosomes are represented. (B) Genetic content of the resulting diploid cells or gametes: The frequency of heterozygosity in the gametes (i.e. from an A/a parent, % of diploid gametes being A/a, and not A/A or a/a), is represented according to the position of genetic marker along the chromosome. During mitosis in diploid cells, chromosomes replicate and sister chromatids segregate to opposite poles and produce two diploid daughter cells. The resulting cells are identical to the mother cell, retaining 100% heterozygosity from the mother cell all along the genome. During meiosis, replicated homologous chromosomes pair and engage in recombination, then segregate to two opposite poles. Sister chromatids are separated at meiosis II and four recombined haploid spores are formed. During meiosis in Atps1 or jas mutants, recombined chromosomes are segregated normally during the first division but are pooled back together on a single metaphase II plate because of parallel or fused spindles. Sister chromatids are then segregated during anaphase II. This mechanism mimics the absence of first division, as only the segregation of sister chromatids is effective, but recombination occurred. Consequently, heterozygosity is conserved close to centromere (all the gametes are A/a at centromeric loci) but is decreased towards telomeres (2/3 Aa and 1/3 A/A or aa). In contrast, in osd1 or tam mutants, the first division occurs normally, the homologous chromosomes are separated, but the omission of the second meiotic division enables sister chromatids to remain together in the same daughter cell. Thus the heterozygosity of the parent is lost at the centromeres (all the gametes are either A/A or a/a, never A/a at centromeric loci).However, crossovers shuffle the chromatids and the frequency of heterozygote gametes (A/a) tends towards 2/3 at loci away from centromeres. Finally, in a dyad or a MiMe mutant, meiosis is replaced by a mitosis-like division (with a higher efficiency in MiMe). The genetic information (notably heterozygosity at all loci) from the mother cell is conserved all along the chromosomes since neither recombination nor the second meiotic division occurred.