Recombination landscape dimorphism contributes to sex chromosome evolution in the dioecious plant Rumex hastatulus

There is growing evidence across diverse taxa for sex differences in the genomic landscape of recombination, but the causes and consequences of these differences remain poorly understood. Strong recombination landscape dimorphism between the sexes could have important implications for the dynamics of sex chromosome evolution and turnover because low recombination in the heterogametic sex can help favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus, representing the first characterization of sex differences in recombination landscape in a dioecious plant. We provide evidence for strong sex differences in recombination, with pericentromeric regions of highly suppressed recombination in males that cover over half of the genome. These differences are found on autosomes as well as sex chromosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. Our results are consistent with the hypothesis that sex differences in the recombination landscape contributed to the formation of a large heteromorphic pair of sex chromosomes, and that pollen competition is an important determinant of recombination dimorphism.

Widespread Recombination Suppression Facilitates Plant Sex Chromosome Evolution

1SummaryClassical models suggest recombination rates on sex chromosomes evolve in a stepwise manner to localize the inheritance of sexually antagonistic variation in the sex where it is beneficial, thereby lowering rates of recombination between X and Y chromosomes. However, it is also possible that sex chromosome formation occurs in regions with pre-existing recombination suppression. To evaluate these possibilities, we constructed linkage maps and a chromosome-scale genome assembly for the dioecious plant Rumex hastatulus, a species with a young neo-sex chromosome found in part of its geographical range. We found that the ancestral sex-linked region is located in a large region characterized by low recombination. Furthermore, comparison between the recombination landscape of the neo-sex chromosome and its autosomal homologue indicates that low recombination rates preceded sex linkage. Our findings suggest that ancestrally low rates of recombination have facilitated the formation and evolution of heteromorphic sex chromosomes.

Chromosomal distribution of cyto-nuclear genes in a dioecious plant with sex chromosomes

The coordination between nuclear and organellar genes is essential to many aspects of eukaryotic life, including basic metabolism, energy production, and ultimately, organismal fitness. Whereas nuclear genes are bi-parentally inherited, mitochondrial and chloroplast genes are almost exclusively maternally inherited, and this asymmetry may lead to a bias in the chromosomal distribution of nuclear genes whose products act in the mitochondria or chloroplasts. In particular, because X-linked genes have a higher probability of co-transmission with organellar genes (2/3) compared to autosomal genes (1/2), selection for co-adaptation has been predicted to lead to an over-representation of nuclear-mitochondrial (N-mt) or nuclear-chloroplast (N-cp) genes on the X chromosome relative to autosomes. In contrast, the occurrence of sexually antagonistic organellar mutations might lead to selection for movement of cyto-nuclear genes from the X chromosome to autosomes to reduce male mutation load. Recent broad-scale comparative studies of N-mt distributions in animals have found evidence for these hypotheses in some species, but not others. Here, we use transcriptome sequences to conduct the first study of the chromosomal distribution of cyto-nuclear interacting genes in a plant species with sex chromosomes (Rumex hastatulus; Polygonaceae). We found no evidence of under- or over-representation of either N-mt or N-cp genes on the X chromosome, and thus no support for either the co-adaptation or the sexual-conflict hypothesis. We discuss how our results from a species with recently evolved sex chromosomes fit into an emerging picture of the evolutionary forces governing the chromosomal distribution of N-mt and N-cp genes.

Reversal of height dimorphism promotes pollen and seed dispersal in a wind-pollinated dioecious plant

Variation in the timing of reproductive functions in dioecious organisms may result in adaptive changes in the direction of sexual dimorphism during the breeding season. For plants in which both pollen and seeds are wind-dispersed, it may be advantageous for male plants to be taller when pollen is dispersed and female plants to be taller when seeds are dispersed. We examined the dynamics of height dimorphism in Rumex hastatulus , an annual, wind-pollinated, dioecious plant from the southern USA. A field survey of seven populations indicated that females were significantly taller than males at seed maturity. However, a glasshouse experiment revealed a more complex pattern of height growth during the life cycle. No dimorphism was evident prior to reproduction for six of seven populations, but at flowering, males were significantly taller than females in all populations. This pattern was reversed at reproductive maturity, consistent with field observations. Males flowered later than females and the degree of height dimorphism was greater in populations with a later onset of male flowering. We discuss the potential adaptive significance of temporal changes in height dimorphism for pollen and seed dispersal, and how this may be optimized for the contrasting reproductive functions of the sexes.

A satellite DNA evolutionary analysis in the North American endemic dioecious plant Rumex hastatulus (Polygonaceae)

We studied the evolution of RAE180 satellite DNA family in the North American endemic dioecious plant Rumex hastatulus . In this species, the Texas race is characterized by a single XX/XY sex chromosome system, whereas the North Carolina race has evolved a derived complex XX/XY1Y2 sex chromosome system. RAE180 repeats were autosomic and poorly represented (2 × 10–4% of the genome) with no differences between individuals of different genders or different races of R. hastatulus. In fact, the sex chromosomes of the North Carolina race are still euchromatic, and they have not accumulated satellite DNA sequences, which contrasts with that occurring in the rest of dioecious XX/XY1Y2 Rumex species. In R. hastatulus, we detected the existence of three RAE180 subfamilies. Notwithstanding, while in the Texas race the TX1/NC1 subfamily is the most frequent, the TX2/NC2 subfamily is the most abundant in the North Carolina race. Additionally, the third, less represented subfamily (TX3/NC3) appears currently as relict sequences in both genomes. A common feature of RAE180 satellite is the sudden replacement of one sequence variant by another in different species (or populations as in R. hastatulus races). Thus, the phylogenetic analysis of RAE180 repeats from six dioecious Rumex species supports the “library” hypothesis. According to this hypothesis, we assume that a set of divergent RAE180 variants were present in the ancestral genome of dioecious Rumex species, from which novel tandem arrays originated by the amplification of different variants in different lineages. Differential levels of RAE180 satellite DNA amplification in each lineage, at different evolutionary times, and in different chromosomal positions gave rise to differential patterns of sequence evolution.