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Flowers of the female and male trees in Salicaceae species. On willow and poplar, the male or female flowers are separately arranged in morphologically different catkins on the male or female trees. Photos taken by Tongming Yin and Jing Hou.

Flowers of the female and male trees in Salicaceae species. On willow and poplar, the male or female flowers are separately arranged in morphologically different catkins on the male or female trees. Photos taken by Tongming Yin and Jing Hou.

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Willows (Salix) and poplars (Populus) are dioecious plants in Salicaceae family. Sex chromosome in poplar genome was consistently reported to be associated with chromosome XIX. In contrast to poplar, this study revealed that chromosome XV was sex chromosome in willow. Previous studies revealed that both ZZ/ZW and XX/XY sex-determining systems could...

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... is a family of dioecious woody plants, and the male or female flowers are arranged in morphologically different catkins (Figure 1) on the male or female trees 10 . Salix and Populus are the sister genera in Salicaceae (Figure 2). ...
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... 1,137 151 segregating markers were generated by 90 primer combinations with the 374 mapping progeny. Among these markers, 494 testcross markers from the maternal parent were mapped into 266 bins distributed on 19 linkage groups, covering a genetic distance of 1924.5 cM (Supplementary Figure 1); Alternatively, 549 testcross loci from the male were assigned into 263 bins on 19 linkage groups, spanning a genetic distance of 2223.8 cM (Supplementary Figure 2). The coverage of the female and male maps was estimated to be 99.99% and 99.97% at 20 cM of a marker, respectively. ...
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... results showed that gender locus could only be mapped on the maternal map, but was unmappable on the paternal map, indicating that the female was the heterogametic gender in willow, which was in agreement with the findings in P. deltoides 22 and P. alba 26 that revealed sex determination occurred through a ZW system, in which females are heterogametic 22 . It was also noteworthy that marker density in the vicinity of the gender locus (Supplementary Figure 1) was significantly higher than that expected by chance alone (P # 0.0001 with a Poisson calculator), which indicated severe recombination suppression around the gender locus. Recombination suppression has been recognized as a critical mechanism that triggered the divergence of the alternate sex chromosomes 2,22,30,31 . ...
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... 1,137 151 segregating markers were generated by 90 primer combinations with the 374 mapping progeny. Among these markers, 494 testcross markers from the maternal parent were mapped into 266 bins distributed on 19 linkage groups, covering a genetic distance of 1924.5 cM (Supplementary Figure 1); Alternatively, 549 testcross loci from the male were assigned into 263 bins on 19 linkage groups, spanning a genetic distance of 2223.8 cM (Supplementary Figure 2). The coverage of the female and male maps was estimated to be 99.99% and 99.97% at 20 cM of a marker, respectively. ...
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... results showed that gender locus could only be mapped on the maternal map, but was unmappable on the paternal map, indicating that the female was the heterogametic gender in willow, which was in agreement with the findings in P. deltoides 22 and P. alba 26 that revealed sex determination occurred through a ZW system, in which females are heterogametic 22 . It was also noteworthy that marker density in the vicinity of the gender locus (Supplementary Figure 1) was significantly higher than that expected by chance alone (P # 0.0001 with a Poisson calculator), which indicated severe recombination suppression around the gender locus. Recombination suppression has been recognized as a criti- cal mechanism that triggered the divergence of the alternate sex chromosomes 2,22,30,31 . ...

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... In recent years, several approaches to identify X chromosomal sequences have been introduced that rely on high-throughput sequencing methods. These methods were reviewed by Palmer et al. (2019) and vary in their costs, in required sample sizes and on the availability of a reference genome (Al-Dous et al., 2011;Gautier, 2014;Picq et al., 2014;Hou et al., 2015;Muyle et al., 2016). In species with a chromosome-level genome assembly, comparison of the sequencing coverage depth across chromosomes between individuals of each sex is a reliable method for identifying sex chromosomes. ...
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Differences between sexes in growth, ecology and behaviour strongly shape species biology. In some animal groups, such as spiders, it is difficult or impossible to identify the sex of juveniles based on external morphology. This information would be useful for field surveys, behavioural experiments and ecological studies, such as those on sex ratios and dispersal. In species with sex chromosomes, sex can be determined based on the specific sex chromosome complement. Additionally, information on the sequence of sex chromosomes provides the basis for studying sex chromosome evolution. We combined cytogenetic and genomic data to identify the sex chromosomes in the sexually dimorphic spider Argiope bruennichi and designed quantitative real-time polymerase chain reaction sex markers. We found that the genome size and GC content of this spider fall into the ranges reported for the majority of araneids. The male karyotype is formed by 24 acrocentric chromosomes with an X1X20 sex chromosome system, with little similarity between X chromosomes, suggesting an origin of these chromosomes by X chromosome fission or early duplication of an X chromosome and subsequent independent differentiation of the copies. Our data suggest X chromosomes of similar sizes in A. bruennichi. They are smaller chromosomes of the complement. Our findings open the door to new directions in spider evolutionary and ecological research.
... Conversely, the SDR of S. purpurea has been mapped to a large, pericentromeric region on Salix chr15, but has been found to maintain a few orthologous regions present within the P. trichocarpa chr19 SDR (Zhou et al. 2018). However, it is unclear whether dioecy evolved before or after their divergence (Hou et al. 2015). The sex systems of Salix also lack a consensus model. ...
... The sex systems of Salix also lack a consensus model. For instance, similar to S. purpurea, both S. suchowensis (Hou et al. 2015;Chen et al. 2016) and S. viminalis (Pucholt et al. 2015;Pucholt et al. 2017b;Hallingbä ck et al. 2021) have female heterogametic (ZW) systems with SDRs located on Salix chr15, yet tree-form S. nigra has an XY system SDR on chr07 (Sanderson et al. 2021). Considering the variability in sex determination systems and SDR locations already discovered within Salix, elucidating the mechanisms of sex determination in more species could help to build a more cohesive understanding of SDR evolution. ...
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Within the genus Salix, there are approximately 350 species native primarily to the northern hemisphere and adapted to a wide range of habitats. This diversity can be exploited to mine novel alleles conferring variation important for production as a bioenergy crop, but also to identify evolutionarily important genes, such as those involved in sex determination. To leverage this diversity, we created a mapping population by crossing six Salix species (S. viminalis, S. suchowensis, S. integra, S. koriyanagi, S. udensis, and S. alberti) to common male and female S. purpurea parents. Each family was genotyped via genotyping-by-sequencing and assessed for kinship and population structure as well as the construction of 16 backcross linkage maps to be used as a genetic resource for breeding and selection. Analyses of population structure resolved both the parents and F1 progeny to their respective phylogenetic section and indicated that the S. alberti parent was misidentified and was most likely S. suchowensis. Sex determining regions were identified on Salix chromosome 15 in the female-informative maps for seven of the eight families indicating that these species share a common female heterogametic ZW sex system. The eighth family, S. integra × S. purpurea, was entirely female and had a truncated chromosome 15. Beyond sex determination, the Salix F1 hybrid common parent population (Salix F1 HCP) introduced here will be useful in characterizing genetic factors underlying complex traits, aid in marker-assisted selection, and support genome assemblies for this promising bioenergy crop.
... For the majority of investigated poplar species, chromosome 19 is the sex chromosome [25][26][27][28][29][30][31][32][33][34][35] but in P. euphratica chromosome 14 is the sex chromosome [24]. In willows chromosome 15 is the sex chromosome in many of the investigated species [36][37][38][39][40][41][42][43], although chromosome 7 and 14 also have been identified as the sex chromosomes for S. dunii and S. nigra respectively [44,45]. Furthermore, most poplars are male heterogametic while the majority of the studied willows are female heterogametic but Z-W heterogamy exist in poplars [24] and X-Y heterogamy have been identified in willows [45]. ...
... As both a chromosome 9 and chromosome 15 copies also is present in the female S. suchowensis draft genome assembly and the female S. purpurea v5.1 assembly, this indicates that the translocation happened prior to the divergence of S. viminalis, S. purpurea and S. suchowensis. Furthermore, previous studies have shown that these closely related species have their SD locus in approximately the same location on chromosome 15 [37,39] suggesting that these species share the same ZW sex chromosome system. This sex chromosome system likely evolved when a dominant feminizing SD gene invaded a population [18] of a common willow ancestor. ...
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Background Sex 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. Results A 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. Conclusions Our 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.
... The genome duplication in poplar and willow is very recent, occurring around 8-13 Mya, defined as the "Pt-α" events and "Sp-α" events, respectively (Sterck et al., 2005;Berlin et al., 2010). The Ks value reflects the generation time of the homologous gene to some extent and is often used as the basis for assessing the gene duplication events (Cui et al., 2006;Hou et al., 2015). ...
... After genome duplication, antagonism eliminates most of the duplicate genes, so there are some genes produced by dispersed duplication. Different replication events appear to have led to the complexity of the R2R3 MYB genes in the willow genome (Dai et al., 2014;Hou et al., 2015). It also provides a theoretical basis suggesting that the willow has undergone more environmental adaptation than the poplar and has evolved more varieties. ...
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The MYB transcription factor (TF) family is one of the largest plant transcription factor gene family playing vital roles in plant growth and development, including defense, cell differentiation, secondary metabolism, and responses to biotic and abiotic stresses. As a model tree species of woody plants, in recent years, the identification and functional prediction of certain MYB family members in the poplar genome have been reported. However, to date, the characterization of the gene family in the genome of the poplar’s sister species willow has not been done, nor are the differences and similarities between the poplar and willow genomes understood. In this study, we conducted the first genome-wide investigation of the R2R3 MYB subfamily in the willow, identifying 216 R2R3 MYB gene members, and combined with the poplar R2R3 MYB genes, performed the first comparative analysis of R2R3 MYB genes between the poplar and willow. We identified 81 and 86 pairs of R2R3 MYB paralogs in the poplar and willow, respectively. There were 17 pairs of tandem repeat genes in the willow, indicating active duplication of willow R2R3 MYB genes. A further 166 pairs of poplar and willow orthologs were identified by collinear and synonymous analysis. The findings support the duplication of R2R3 MYB genes in the ancestral species, with most of the R2R3 MYB genes being retained during the evolutionary process. The phylogenetic trees of the R2R3 MYB genes of 10 different species were drawn. The functions of the poplar and willow R2R3 MYB genes were predicted using reported functional groupings and clustering by OrthoFinder. Identified 5 subgroups in general expanded in woody species, three subgroups were predicted to be related to lignin synthesis, and we further speculate that the other two subgroups also play a role in wood formation. We analyzed the expression patterns of the GAMYB gene of subgroup 18 (S18) related to pollen development in the male flower buds of poplar and willow at different developmental stages by qRT-PCR. The results showed that the GAMYB gene was specifically expressed in the male flower bud from pollen formation to maturity, and that the expression first increased and then decreased. Both the specificity of tissue expression specificity and conservation indicated that GAMYB played an important role in pollen development in both poplar and willow and was an ideal candidate gene for the analysis of male flower development-related functions of the two species.
... In shrub willow species examined thus far, which include S. viminalis, S. suchowensis, and S. purpurea, females are the heterogametic sex (Semerikov et al., 2003;Hou et al., 2015;Pucholt et al., 2015;Chen et al., 2016;Zhou et al., 2018), where the SDR maps to chromosome 15 (Hou et al., 2015;Zhou et al., 2018). However, the SDR maps to chromosome 7 in S. nigra where the males are Fred E. Gouker and Craig H. Carlson contributed equally to this study. ...
... In shrub willow species examined thus far, which include S. viminalis, S. suchowensis, and S. purpurea, females are the heterogametic sex (Semerikov et al., 2003;Hou et al., 2015;Pucholt et al., 2015;Chen et al., 2016;Zhou et al., 2018), where the SDR maps to chromosome 15 (Hou et al., 2015;Zhou et al., 2018). However, the SDR maps to chromosome 7 in S. nigra where the males are Fred E. Gouker and Craig H. Carlson contributed equally to this study. ...
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Premise: The evolution of sex chromosomes is driven by sexual dimorphism, yet it can be challenging to document sexually dimorphic traits in dioecious plant species. At the genetic level, sexual dimorphism can be identified through sequence variation between females and males associated with sexually antagonistic traits and different fitness optima. This study aims to examine sexual dimorphism for 26 traits in three populations of Salix purpurea (a diversity panel and F1 and F2 populations) and determine the effect of the traits on biomass yield, a key trait in Salix bioenergy crops across multiple years, locations, and under manipulated growth conditions. Methods: Sexual dimorphism was evaluated for morphological, phenological, physiological, and wood composition traits in a diversity panel of unrelated S. purpurea accessions and in full-sib F1 and F2 families produced through controlled cross pollinations and grown in replicated field trials. Results: We observed sexual dimorphism in the timing of development for several traits that were highly predictive of biomass yield across three populations of S. purpurea. Across all populations and years surveyed, males had significantly shallower branching angle. Male plants highly predictive of biomass yield across three populations of S. purpurea also accumulated more nitrogen under fertilizer amendment as measured by SPAD in the diversity panel and had greater susceptibility to the rust fungus Melampsora americana in the F2 family. Allometric modelling of biomass yield showed an effect of sex and of location on the interaction between yield and stem height. Conclusions: These results provide evidence of sexual dimorphism for certain traits in S. purpurea that may be involved in sex chromosome evolution.
... ep). Populus is also an important model genus for studying the evolution of dioecy in plants as two different genetic systems of sexual determination have been identified 34,35 (XY and ZW systems). Over 30 species are currently recognized in the genus Populus with many of the species growing across massive geographic ranges 36,37 . ...
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The chloroplast is one of two organelles containing a separate genome that codes for essential and distinct cellular functions such as photosynthesis. Given the importance of chloroplasts in plant metabolism, the genomic architecture and gene content have been strongly conserved through long periods of time and as such are useful molecular tools for evolutionary inferences. At present, complete chloroplast genomes from over 4000 species have been deposited into publicly accessible databases. Despite the large number of complete chloroplast genomes, comprehensive analyses regarding genome architecture and gene content have not been conducted for many lineages with complete species sampling. In this study, we employed the genus Populus to assess how more comprehensively sampled chloroplast genome analyses can be used in understanding chloroplast evolution in a broadly studied lineage of angiosperms. We conducted comparative analyses across Populus in order to elucidate variation in key genome features such as genome size, gene number, gene content, repeat type and number, SSR (Simple Sequence Repeat) abundance, and boundary positioning between the four main units of the genome. We found that some genome annotations were variable across the genus owing in part from errors in assembly or data checking and from this provided corrected annotations. We also employed complete chloroplast genomes for phylogenetic analyses including the dating of divergence times throughout the genus. Lastly, we utilized re-sequencing data to describe the variations of pan-chloroplast genomes at the population level for P . euphratica . The analyses used in this paper provide a blueprint for the types of analyses that can be conducted with publicly available chloroplast genomes as well as methods for building upon existing datasets to improve evolutionary inference.
... In willow (Salix spp.), the SDR was identified on chromosome 15 with female heterogamety (ZW) in Salix viminalis (Pucholt et al., 2015), Salix suchowensis (Hou et al., 2015;Chen et al., 2016), Salix purpurea (Zhou et al., 2018), and Salix triandra (Li et al., 2020). A recent study revealed large palindromic structures on the W chromosome of S. purpurea and an ortholog of ARR17 (Salix purpurea RESPONSE REGULATOR 9, SpRR9) was suggested as a strong candidate gene for sex determination (Zhou et al., 2020a). ...
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The diversity of inflorescences among flowering plants is captivating. Such charm is not only due to the variety of sizes, shapes, colors, and flowers displayed, but also to the range of reproductive systems. For instance, hermaphrodites occur abundantly throughout the plant kingdom with both stamens and carpels within the same flower. Nevertheless, 10% of flowering plants have separate unisexual flowers, either in different locations of the same individual (monoecy) or on different individuals (dioecy). Despite their rarity, dioecious plants provide an excellent opportunity to investigate the mechanisms involved in sex expression and the evolution of sex-determining regions (SDRs) and sex chromosomes. The SDRs and the evolution of dioecy have been studied in many species ranging from Ginkgo to important fruit crops. Some of these studies, for example in asparagus or kiwifruit, identified two sex-determining genes within the non-recombining SDR and may thus be consistent with the classical model for the evolution of dioecy from hermaphroditism via gynodioecy, that predicts two successive mutations, the first one affecting male and the second one female function, becoming linked in a region of suppressed recombination. On the other hand, aided by genome sequencing and gene editing, single factor sex determination has emerged in other species, such as persimmon or poplar. Despite the diversity of sex-determining mechanisms, a tentative comparative analysis of the known sex-determining genes and candidates in different species suggests that similar genes and pathways may be employed repeatedly for the evolution of dioecy. The cytokinin signaling pathway appears important for sex determination in several species regardless of the underlying genetic system. Additionally, tapetum-related genes often seem to act as male-promoting factors when sex is determined via two genes. We present a unified model that synthesizes the genetic networks of sex determination in monoecious and dioecious plants and will support the generation of hypothesis regarding candidate sex determinants in future studies.
... Compared with poplar genomes, willow genomes are generally smaller and contain fewer protein-coding genes. Using k-mer analysis, it was estimated that the genome size of S. suchowensis was~425 Mb 8 , while that of S. purpurea was~450 Mb 7 , both of which are slightly smaller than the estimated 485 Mb P. trichocarpa genome 1 24 . Using PacBio sequencing long reads, the size of our improved genome assembly for S. suchowensis was 356.5 Mb, and 36,937 putative proteinencoding genes were predicted in the whole genome. ...
Article
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Salix suchowensis is an early-flowering shrub willow that provides a desirable system for studies on the basic biology of woody plants. The current reference genome of S. suchowensis was assembled with 454 sequencing reads. Here, we report a chromosome-scale assembly of S. suchowensis generated by combining PacBio sequencing with Hi-C technologies. The obtained genome assemblies covered a total length of 356 Mb. The contig N50 of these assemblies was 263,908 bp, which was ~65-fold higher than that reported previously. The contiguity and completeness of the genome were significantly improved. By applying Hi-C data, 339.67 Mb (95.29%) of the assembled sequences were allocated to the 19 chromosomes of haploid willow. With the chromosome-scale assembly, we revealed a series of major chromosomal fissions and fusions that explain the genome divergence between the sister genera of Salix and Populus. The more complete and accurate willow reference genome obtained in this study provides a fundamental resource for studying many genetic and genomic characteristics of woody plants.
... This family includes two sister genera, Populus and Salix, which are comprised exclusively of dioecious species (Peto 1938;Zhang et al. 2018;Li et al. 2020). Previous studies in multiple Salix species have consistently mapped the SDRs to chromosome 15, and proposed a ZW system in which females are the heterogametic sex (Hou et al. 2015;Pucholt et al. 2015;Chen et al. 2016;Pucholt et al. 2017;Zhou et al. 2018;Zhou, Macaya-Sanz, Carlson, et al. 2020). However, an XY system was recently identified on chromosome 7 in S. nigra (Sanderson et al., unpublished data). ...
... Moreover, our results simultaneously showed that the Salicaceae exhibit an extremely fast rate of sex-chromosome turnover. In previous studies, SDRs have been reported only on chromosome 15 with female heterogamety (ZW) in willow except S. nigra (Hou et al. 2015;Pucholt et al. 2015;Chen et al. 2016;Pucholt et al. 2017;Zhou et al. 2018;Zhou, Macaya-Sanz, Carlson, et al. 2020;Sanderson et al., unpublished data), and on chromosome 19 of poplar with most species showing male heterogamety (XY) (Gaudet et al. 2007;Yin et al. 2008;Geraldes et al. 2015). However, our study identified an XY system with the SDR on chromosome 14 of P. euphratica for the first time, and confirmed a ZW system with SDR on chromosome 19 of P. alba. ...
Article
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Dioecy, the presence of separate sexes on distinct individuals, has evolved repeatedly in multiple plant lineages. However, the specific mechanisms by which sex systems evolve and their commonalities among plant species remain poorly understood. With both XY and ZW sex systems, the family Salicaceae provides a system to uncover the evolutionary forces driving sex chromosome turnovers. In this study, we performed a genome-wide association study to characterize sex determination in two Populus species, P. euphratica and P. alba. Our results reveal an XY system of sex determination on chromosome 14 of P. euphratica, and a ZW system on chromosome 19 of P. alba. We further assembled the corresponding sex determination regions, and found that their sex chromosome turnovers may be driven by the repeated translocations of a Helitron-like transposon. During the translocation, this factor may have captured partial or intact sequences that are orthologous to a type-A cytokinin response regulator gene. Based on results from this and other recently published studies, we hypothesize that this gene may act as a master regulator of sex determination for the entire family. We propose a general model to explain how the XY and ZW sex systems in this family can be determined by the same RR gene. Our study provides new insights into the diversification of incipient sex chromosomes in flowering plants by showing how transposition and rearrangement of a single gene can control sex in both XY and ZW systems.
... Almost all species in the Salicaceae are dioecious, including those in Salix and Populus [12]. However, both female and male heterogamety are found in this family [13][14][15][16]. Chromosome 19 (Chr19) has been shown to be male heterogametic in several Populus studies [13,[17][18][19]. ...
... Although sex determination has been consistently mapped to Chr19 in Populus, other chromosomes also show sex association peaks [13]. In contrast, sex determination consistently maps to a single major locus in Salix, where single association peaks have been identified on Chr15 [14,15,20] and Chr7 [21]. Multiple locations of sex-specific markers in Populus were proposed to be associated with the erroneous assembly of portions of the SDR in the reference genome [13]. ...
Article
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The ages and sizes of a sex-determination region (SDR) are difficult to determine in non-model species. Due to the lack of recombination and enrichment of repetitive elements in SDRs, the quality of assembly with short sequencing reads is universally low. Unique features present in the SDRs help provide clues about how SDRs are established and how they evolve in the absence of recombination. Several Populus species have been reported with a male heterogametic configuration of sex (XX/XY system) mapped on chromosome 19, but the exact location of the SDR has been inconsistent among species, and thus far, none of these SDRs has been fully assembled in a genomic context. Here we identify the Y-SDR from a Y-linked contig directly from a long-read PacBio assembly of a Populus trichocarpa male individual. We also identified homologous gene sequences in the SDR of P. trichocarpa and the SDR of the W chromosome in Salix purpurea. We show that inverted repeats (IRs) found in the Y-SDR and the W-SDR are lineage-specific. We hypothesize that, although the two IRs are derived from the same orthologous gene within each species, they likely have independent evolutionary histories. Furthermore, the truncated inverted repeats in P. trichocarpa may code for small RNAs that target the homologous gene for RNA-directed DNA methylation. These findings support the hypothesis that diverse sex-determining systems may be achieved through similar evolutionary pathways, thereby providing a possible mechanism to explain the lability of sex-determination systems in plants in general.