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Single locus sex determination and female heterogamety in the basket willow (Salix viminalis L.).

ABSTRACT: Most eukaryotes reproduce sexually and a wealth of different sex determination mechanisms have evolved in this lineage. Dioecy or separate sexes are rare among flowering plants but have repeatedly evolved from hermaphroditic ancestors possibly involving male or female sterility mutations. Willows (Salix spp.) and poplars (Populus spp.) are predominantly dioecious and are members of the Salicaceae family. All studied poplars have sex determination loci on chromosome XIX, however, the position differs among species and both male and female heterogametic system exists. In contrast to the situation in poplars, knowledge of sex determination mechanisms in willows is sparse. In the present study, we have for the first time positioned the sex determination locus on chromosome XV in S. viminalis using quantitative trait locus mapping. All female offspring carried a maternally inherited haplotype, suggesting a system of female heterogamety or ZW. We used a comparative mapping approach and compared the positions of the markers between the S. viminalis linkage map and the physical maps of S. purpurea, S. suchowensis and P. trichocarpa. As we found no evidence for chromosomal rearrangements between chromosome XV and XIX between S. viminalis and P. trichocarpa, it shows that the sex determination loci in the willow and the poplar most likely do not share a common origin and has thus evolved separately. This demonstrates that sex determination mechanisms in the Salicaceae family have a high turnover rate and as such it is excellent for studies of evolutionary processes involved in sex chromosome turnover.

SUBMITTER: Pucholt P

PROVIDER: S-EPMC4434249 | biostudies-literature | 2015 Jun

REPOSITORIES: biostudies-literature

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Single locus sex determination and female heterogamety in the basket willow (Salix viminalis L.).

Pucholt P P Rönnberg-Wästljung A-C AC Berlin S S

Heredity 20150204 6

Most eukaryotes reproduce sexually and a wealth of different sex determination mechanisms have evolved in this lineage. Dioecy or separate sexes are rare among flowering plants but have repeatedly evolved from hermaphroditic ancestors possibly involving male or female sterility mutations. Willows (Salix spp.) and poplars (Populus spp.) are predominantly dioecious and are members of the Salicaceae family. All studied poplars have sex determination loci on chromosome XIX, however, the position dif ...[more]

PMID: 25649501

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Project description:BackgroundSex chromosomes have evolved independently multiple times in eukaryotes and are therefore considered a prime example of convergent genome evolution. Sex chromosomes are known to emerge after recombination is halted between a homologous pair of chromosomes, and this leads to a range of non-adaptive modifications causing gradual degeneration and gene loss on the sex-limited chromosome. However, the proximal causes of recombination suppression and the pace at which degeneration subsequently occurs remain unclear.ResultsHere, we use long- and short-read single-molecule sequencing approaches to assemble and annotate a draft genome of the basket willow, Salix viminalis, a species with a female heterogametic system at the earliest stages of sex chromosome emergence. Our single-molecule approach allowed us to phase the emerging Z and W haplotypes in a female, and we detected very low levels of Z/W single-nucleotide divergence in the non-recombining region. Linked-read sequencing of the same female and an additional male (ZZ) revealed the presence of two evolutionary strata supported by both divergence between the Z and W haplotypes and by haplotype phylogenetic trees. Gene order is still largely conserved between the Z and W homologs, although the W-linked region contains genes involved in cytokinin signaling regulation that are not syntenic with the Z homolog. Furthermore, we find no support across multiple lines of evidence for inversions, which have long been assumed to halt recombination between the sex chromosomes.ConclusionsOur data suggest that selection against recombination is a more gradual process at the earliest stages of sex chromosome formation than would be expected from an inversion and may result instead from the accumulation of transposable elements. Our results present a cohesive understanding of the earliest genomic consequences of recombination suppression as well as valuable insights into the initial stages of sex chromosome formation and regulation of sex differentiation.

Project description:The short rotation biomass crop willow (Salix genera) has been of interest for bioenergy but recently also for biofuel production. For a faster development of new varieties molecular markers could be used as selection tool in an early stage of the breeding cycle. To identify markers associated with growth traits, genome-wide association mapping was conducted using a population of 291 Salix viminalis accessions collected across Europe and Russia and a large set of genotyping-by-sequencing markers. The accessions were vegetatively propagated and planted in replicated field experiments, one in Southern Sweden and one in Central Sweden. Phenology data, including bud burst and leaf senescence, as well as different growth traits were collected and measured repeatedly between 2010 and 2017 at both field environments. A value of the plasticity for each accession was calculated for all traits that were measured the same year in both environments as the normalized accession value in one environment subtracted by the corresponding value in the other environment. Broad-sense accession heritabilities and narrow-sense chip heritabilities ranged from 0.68 to 0.95 and 0.45 to 0.99, respectively for phenology traits and from 0.56 to 0.85 and 0.24 to 0.97 for growth traits indicating a considerable genetic component for most traits. Population structure and kinship between accessions were taken into account in the association analyses. In total, 39 marker-trait associations were found where four were specifically connected to plasticity and interestingly one particular marker was associated to several different plasticity growth traits. Otherwise association consistency was poor, possibly due to accession by environment interactions which were demonstrated by the low structure adjusted accession correlations across environments (ranging from 0.40 to 0.58). However, one marker association with biomass fresh weight was repeatedly observed in the same environment over two harvest years. For some traits where several associations were found, the markers jointly explained over 20% of the accession variation. The result from this study using a population of unrelated accessions has given useful information about marker-trait associations especially highlighting marker-plasticity associations and genotype-by-environment interactions as important factors to take account of in future strategies of Salix breeding.

Project description:BackgroundSex chromosomes are in some species largely undifferentiated (homomorphic) with restricted sex determination regions. Homomorphic but different sex chromosomes are found in the closely related genera Populus and Salix indicating flexible sex determination systems, ideal for studies of processes involved in sex chromosome evolution. We have performed genome-wide association studies of sex and analysed sex chromosomes in a population of 265 wild collected Salix viminalis accessions and studied the sex determining locus.ResultsA total of 19,592 markers were used in association analyses using both Fisher's exact tests and a single-marker mixed linear model, which resulted in 48 and 41 sex-associated (SA) markers respectively. Across all 48 SA markers, females were much more often heterozygous than males, which is expected if females were the heterogametic sex. The majority of the SA markers were, based on positions in the S. purpurea genome, located on chromosome 15, previously demonstrated to be the sex chromosome. Interestingly, when mapping the genotyping-by-sequencing sequence tag harbouring the two SA markers with the highest significance to the S. viminalis genomic scaffolds, five regions of very high similarity were found: three on a scaffold that represents a part of chromosome 15, one on a scaffold that represents a part of chromosome 9 and one on a scaffold not anchored to the genome. Based on segregation differences of the alleles at the two marker positions and on differences in PCR amplification between females and males we conclude that females had multiple copies of this DNA fragment (chromosome 9 and 15), whereas males only had one (chromosome 9). We therefore postulate that the female specific sequences have been copied from chromosome 9 and inserted on chromosome 15, subsequently developing into a hemizygous W chromosome linked region.ConclusionsOur results support that sex determination in S. viminalis is controlled by one locus on chromosome 15. The segregation patterns observed at the SA markers furthermore confirm that S. viminalis females are the heterogametic sex. We also identified a translocation from chromosome 9 to the W chromosome.

Dataset Information

Single locus sex determination and female heterogamety in the basket willow (Salix viminalis L.).

Publications

Single locus sex determination and female heterogamety in the basket willow (Salix viminalis L.).

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