Does polyploidy inhibit sex chromosome evolution in angiosperms?

Abstract

Dioecy is rare in flowering plants (5–6% of species), but is often controlled genetically by sex-linked regions (SLRs). It has so far been unclear whether, polyploidy affects sex chromosome evolution, as it does in animals, though polyploidy is quite common in angiosperms, including in dioecious species. Plants could be different, as, unlike many animal systems, degenerated sex chromosomes, are uncommon in plants. Here we consider sex determination in plants and plant-specific factors, and propose that constraints created at the origin of polyploids limit successful polyploidization of species with SLRs. We consider the most likely case of a polyploid of a dioecious diploid with an established SLR, and discuss the outcome in autopolyploids and allopolyploids. The most stable system possibly has an SLR on just one chromosome, with a strongly dominant genetic factor in the heterogametic sex (e.g., xxxY male in a tetraploid). If recombination occurs with its homolog, this will prevent Y chromosome degeneration. Polyploidy may also allow for reversibility of multiplied Z or X chromosomes into autosomes. Otherwise, low dosage of Y-linked SLRs compared to their multiple homologous x copies may cause loss of reliable sex-determination at higher ploidy levels. We discuss some questions that can be studied using genome sequencing, chromosome level-assemblies, gene expression studies and analysis of loci under selection.

Evolutionary origin and establishment of a dioecious diploid‐tetraploid complex

“…This implies that the autotetraploids have a stable dioecious sexual system. The S. polyclona autotetraploids probably have a ZZZW/ZZZZ system and a dominant W‐linked female‐determining factor, so that the allele dosage in polyploids does not disturb sex determination, as in other similar plant systems (Akagi et al, 2016; Gerchen et al, 2022; He & Hörandl, 2022; Krasovec et al, 2018; Toups et al, 2022; Warmke & Blakeslee, 1939; Westergaard, 1958). Hence, we speculated that the W2 inherited female‐heterogametic system from its diploid progenitor, this system was maintained during polyploidization and helped W2 to keep the dioecious sexual system rather than reversion to another sexual system.…”

“…Strongly degenerated sex chromosomes pose a barrier to polyploidization (Stöck et al, 2021; reviewed by He & Hörandl, 2022). The sex‐linked region of diploid S. polyclona occupied 35.2% of chromosome 15's physical size (Figure 1) but may not be degenerated enough to prevent polyploidization.…”

“…Polyploidization is an important mechanism of speciation and the evolution of flowering plants (Comai, 2005; Grant, 1981; Van de Peer et al, 2017). Approximately 35% of extant flowering plant species are of recent polyploid origin, including dioecious (i.e., bearing different sexes on separate individuals) polyploids (Wood et al, 2009; reviewed by He & Hörandl, 2022). Polyploids are classified into autopolyploids and allopolyploids based on the origin of the duplicated genomes, either through genome duplication of a single species or via hybridization and the doubling of two differentiated genomes, respectively (Tayalé & Parisod, 2013).…”

“…This partly explains why research on allopolyploids is far broader and deeper than that on autopolyploids (Rieseberg & Willis, 2007; Spoelhof et al, 2017). Studies on dioecious autopolyploid plants are extremely rare (reviewed by He & Hörandl, 2022), and thus the factors that contribute to the establishment and persistence of dioecious polyploids remain poorly understood.…”

“…However, selfing is not possible in dioecious plants, and apomixis is a complex and rare trait that is not easy to establish in dioecious plants (e.g., Hojsgaard et al, 2014; Hojsgaard & Hörandl, 2019; but see e.g., Lindera , Nakamura et al, 2021). Hence, because male and female polyploid individuals of the same ploidy level are needed to establish a population, newly formed polyploids are more severely constrained by minority cytotype exclusion in dioecious than cosexual plants (He & Hörandl, 2022).…”