Sexual polyploidization in plants--cytological mechanisms and molecular regulation

Abstract

In the plant kingdom, events of whole genome duplication or polyploidization are generally believed to occur via alterations of the sexual reproduction process. Thereby, diploid pollen and eggs are formed that contain the somatic number of chromosomes rather than the gametophytic number. By participating in fertilization, these so-called 2n gametes generate polyploid offspring and therefore constitute the basis for the establishment of polyploidy in plants. In addition, diplogamete formation, through meiotic restitution, is an essential component of apomixis and also serves as an important mechanism for the restoration of F1 hybrid fertility. Characterization of the cytological mechanisms and molecular factors underlying 2n gamete formation is therefore not only relevant for basic plant biology and evolution, but may also provide valuable cues for agricultural and biotechnological applications (e.g. reverse breeding, clonal seeds). Recent data have provided novel insights into the process of 2n pollen and egg formation and have revealed multiple means to the same end. Here, we summarize the cytological mechanisms and molecular regulatory networks underlying 2n gamete formation, and outline important mitotic and meiotic processes involved in the ectopic induction of sexual polyploidization.

Fig. 1

Types of 2n gamete-forming mechanism based on the genotypic outcome. Classification of 2n gamete-forming cytological mechanisms based on the genetic make-up of the generated diplogametes and graphical representation of the equivalent meiotic restitution, as observed in simultaneous-type meiotic cell division. For simplicity, the meiotic cell is diploid and only contains two chromosomes that are fully heterozygous (e.g. blue and red chromosomes obtained from genetically different parents). FDR, first division restitution; IMR, indeterminate meiotic restitution; MI, meiosis I; MII, meiosis II; SDR, second division restitution.

Fig. 2

Cytological mechanism of tripolar, parallel and fused spindles, and the associated formation of first division restitution (FDR)-type 2n gametes. Graphical representation of the process of meiotic nonreduction through aberrations in meiosis II (MII) spindle orientation, and the presumed link with alterations in meiosis I (MI)-to-MII interzonal microtubule array formation. The segregation of a heterozygous centromeric marker (Rr) is represented by the black (r) and red (R) lines. Microtubular structures are represented by green fluorescent figure arrays. Additional tetrad figures in the Arabidopsis parallel spindle (ps) mutant jas, harboring a heterozygous centromere-linked pollen fluorescence marker (e.g. FTL 1323; dsRed2; Francis et al., 2007), indicate that ps-generated diploid spores in restituted dyads and triads maintain parental heterozygosity in genomic regions close to the centromere. Bar, 20 μm.

Fig. 3

Overview of the molecular factors involved in diploid and polyploid gamete formation in plants. Graphical representation of all proteins and molecular networks controlling pre- and post-meiotic ploidy stability, meiotic genome reduction and haploid spore formation in plants. Proteins that are known to generate diploid and/or polyploid gametes on mutation are indicated by asterisks. Please see main text for definitions of abbreviations.