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Pinterest Email Send Text Message Print. b SLR-X and SLR-Y haplotypes reconstructed from genome sequences of our sequenced male see main text. The yellow bars at the left indicate the X and Y telomeres, and physical distances kb from the telomere end are shown under each bar.

The dashed lines represent deleted sequences, whereas the loops on SLR-Y represent the two Y-specific hemizygous sequence YHS described in the text. The gray portion on SLR-X indicates a region described in the text, where divergence between SLR-X and SLR-Y is higher than elsewhere in the SLR. c The Y-specific region rebuilt from 13 PCR amplified fragments fragment names are shown above the arrows.

Red asterisks indicate the fragments are further amplified with natural stands of P. Similar results were obtained in two independent experiments. M molecular marker, B blank control.

Source data underlying d are provided as a Source Data file. Because the sequenced male inherited his X chromosome from his sequenced female parent, we could use single-nucleotide polymorphisms SNPs to infer the complete SLR-X and SLR-Y haplotypes in the sex-linked region Fig. Annotation predicted 41 genes in the SLR-X haplotype and 26 in SLR-Y.

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At least 16 genes with assigned functions were found in both the SLR-X and -Y, including a cluster of 5 tandem genes encoding leucine-rich repeats LRR receptor-like protein kinases Supplementary Table 3. Supplementary Figure 3 shows the alignment of homologous genes between SLR-X and -Y.

Divergence between genic sequences on the SLR-X and -Y is highest for genes neighboring the telomeric repeat regions, and some are unalignable Fig. To identify the P. deltoides sex determining factors, we performed a genome-wide association study GWAS based on SNPs, using 49 female and 46 male trees Supplementary Table 4.

Genome resequencing generated a total of 1. We refer to such SNPs as SEMSs SNPs exactly matching with sexes. In total, are elsewhere, of which 78 are in a chromosome XIX PAR gene Fig. thaliana type-A RR genes. We named this gene FERR female-specifically expressed RESPONSE REGULATORbased on evidence for its function described below.

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Phenotypes previously reported for mutations in two members of this A. thaliana gene family, arr16 and arr17include effects on plant photomorphogenesis, cell division activity and root hydrotropism, but not changes in floral organs 3132 However, a recent study demonstrated involvement of such a gene in female functions and sex determination in P. tremula 29and named the FERR ortholog ARR17 29 although, as discussed below, it is not the ortholog of the A. thaliana ARR17 gene.

The y -axis shows the negative logarithm of P values from Wald Chi-Squared Test implemented in GEMMA. The Roman numerals under the x -axis indicate the chromosome identity.

b shows results of coverage GWAS using the female genome as the reference.

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c shows results of SNPs GWAS using SLR-Y as reference. d shows results of coverage GWAS using SLR-Y as reference. R1, R2, YHS1-YHS3 at the bottom of c and d indicate regions contain GWAS signals completely associated with sexes. Note that the FERR-R and MSL genes are not shown as significant in cbecause the SNP analysis is not relevant to these genes, since they are absent from the X haplotype.

The other 42 SEM variants are in genes on three other chromosomes and one unplaced contig, Contig Fig. Previous studies in P. balsamifera 26 and P. trichocarpa 28using the assembled genome sequence of a P. trichocarpa female as the reference 34also found SNPs associated with sex on multiple chromosomes.

However, using a female genome as the reference will produce false positive SEMSs, because reads from Y-linked regions that are missing from the female genome will erroneously map to homologous sequences elsewhere in the genome.

Examination of our P. deltoides non-SLR SEMSs indeed revealed sequence similarity with the SLR-Y Supplementary Table 6.

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Use of the SLR-Y as our reference for GWAS analysis eliminated all the non-SLR SEMSs Fig. As mentioned above, some segments of the X and Y haplotypes are unalignable Supplementary Fig. To examine this possibility, we performed coverage-based GWAS in our 95 P. deltoides samples see Methods section. With the SLR-Y as the reference, we detected three Y-specific hemizygous sequences YHSstwo large ones, YHS1 in Fig. These sequences are present in all male trees and absent in all females Fig.

No female-specific sequences were detected using the SLR-X as reference Fig. The YHS1 sequence was validated by amplifying and Sanger sequencing 13 overlapping fragments in the sequenced male Fig.

This yielded a 41,bp sequence identical to the SLR-Y sequence, which is therefore complete, and includes no gaps. We tested 20 trees of each sex from the GWAS samples for the presence of YHS1 using PCR primers designed to amplify eight separate fragments Fig. Three gene models were predicted in YHS1, and one in YHS2 Fig. Sequence analysis indicated that three gene models are transposable elements, but one gene EVM in YHS1 is the duplication of FERR described above.

We named the FERR duplicate FERR-Rstanding for its inferred FERR repressor function, as deduced from experiments described below. A duplication of FERR was also recently found in the P. tremula sex-determining region which is located in a different chromosome XIX region from that of P. deltoidesand was named ARR17 inverted repeat EVM also within YHS1 was found to produce long non-coding transcripts see details belowand was named MSLfor male-specific lncRNA.

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Before describing our evidence about these functions, we first describe data about expression during flower development that eliminates the protein-coding genes in the fully sex-linked region as candidate sex determining genes. Poplars have small florets, without petals or sepals, and many florets are attached to the rachis of morphologically different male or female catkins Supplementary Fig. A single male floret consists of a group of stamens inserted on a disk, while a female floret has a single-celled ovary seated in a cup-shaped disk Supplementary Fig.

Poplars bloom in early spring before the flush of leaves, but female and male flower primordia start differentiating in June of the previous year Fig. Four stages of sex organ development related to occurrence of doiecy are recognized 35T1 before the initiation of stamen or carpel primordiaT2 early stamen or carpel developmentpre-meiosis stage T3and post-meiosis stage T4 ; the Methods section defines the stages.

Longitudinal sections of flower buds Fig. deltoides male and female flower primordia are distinguishable starting from early June T1 and early July T3respectively. The sex-determining genes must therefore act at these early stages.

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a Morphology of the male and female flower buds at developmental stages T1-T4 defined in the text. b Longitudinal sections of male and female inflorescences at T1 and T3. The red arrows point to the floret primordia, and the yellow arrow denotes the anther primordium. Three independent samples were observed with similar results. c Gene expression profiles in the 8 flower development stages described in the text. The data for c are provided as a Source Data file.

Our RNA-seq experiments detected no expression of two of the Y-specific transposable elements, eliminating them from consideration as candidate sex determining genes. In contrast, TCPCLCMET1, FERR-Rand MSL were expressed in all four early flower development stages.

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qRT-PCR bioassays showed that none of these genes has expression limited to flower tissue, and none shows a consistent sex difference in expression Fig. The three protein-coding genes, TCPCLCand MET1are present in both the SLR-X and -Y, making them unlikely candidates for the sex determining genes, given their lack of consistent sex differences in expression.

However, the two SLR-Y hemizygous genes, FERR-R and MSLare present only in male P. Despite being expressed in all four early flower development stages, and not exclusively in flower tissue, these two non-protein-coding genes are considered as candidate sex determining genes in P. We next describe expression and function data that support this view. The SLR-Y hemizygous gene FERR-R shows homology with FERR a PAR gene and with the autosomal HEMA1 gene Fig. a Sequence homology analysis for FERR - R.

e1-e5 represent the five exons of FERR in black or HEMA1 in red.

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S1-S8 indicate the duplicated segments described in the text. b Abundance of FERR -R transcripts and the FERR - R generated siRNAs, and the differential methylation of FERR in the two sexes.

The gray shadow shows the region methylated only in males, and the red vertical bars indicate the methylation levels in this region. c Transient expression experiment in poplar protoplasts. siFERR is siRNA generated by FERR - R. Three independent experiments were performed with similar observation.

Expression data from strand-specific lncRNA-Seq and small RNA-Seq revealed that the male-specific FERR-R copy is transcribed into long transcripts that generate small interfering RNAs siRNAs; Fig.

In other organisms, siRNAs have been found to guide the methylation of homologous DNA through RNA-directed DNA methylation We found that, in P. Bisulfite sequencing showed that methylation of the corresponding regions in FERR occurred specifically in males Fig. balsamiferamale-specific DNA methylation was also detected in the promoter and first intron of the homologous gene, PbRR9 Besides inducing siRNA-directed DNA methylation, siRNAs produced by FERR-R were also found to target FERR exons 1 to 3, suggesting that FERR-R might also trigger siRNA-guided cleavage of FERR transcripts.

Transient expression experiment in poplar mesophyll protoplasts confirmed that cleavage indeed occurred, and involved interaction between FERR-R and FERR.

Supplementary Figure 6 shows a model of the interaction between FERR - R and FERRbased on the observations just described. qRT-PCR revealed that FERR is expressed only during the initiation of female flower primordia and the early development of female flowers in P.

In the early stages of flower development, the scales form a large proportion of bud tissue, and the flowers are too small to separate into different tissues before stage T5. FERR is expressed in whole flower buds including scales of stages T1 to early stage T5.

In stage T5 female flower buds, removal of the scales increased FERR expression more than fold, indicating that high FERR levels in earlier stages were obscured by the presence of scale tissue. After stage T5, FERR expression decreased to a low level by stage T8 Fig. The effects of the FERR-R duplication described above act by affecting expression of FERRand must therefore be specific to early carpel development, even though, as described above, expression of FERR-R is not specific to early bud stages.

FERR -like genes resembling A. thaliana ARR17 were among candidate sex determining genes in several previous studies of poplar and willow species PbRR9 in P. balsamifera 2637PtRR9 or PtRR11 in P. trichocarpa 38ARR17 in P.

tremula 29RR in Salix purpurea Phylogenetic analysis of type-A RR genes Supplementary Fig. deltoides FERR EVM trichocarpa FERR Potri.

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thaliana ARR17 gene the closest sequence is another gene in this family, EVM thaliana overexpressing P. deltoides FERR. These had normal androecium development, but often showed stigma exaggeration, in extreme cases producing flowers with two pistils or carpel-like sepals Fig.

We, therefore, propose that FERR is a female-specifically expressed P. deltoides response regulator RR that promotes female functions during the initiation of female flower primordia and early carpel development.

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Such a function is consistent with our evidence above that the Y-linked FERR-R gene suppresses FERR functions in P. deltoides males, and corresponds to the hypothesized female suppressor, or Su Finvolved in the evolution of dioecy 7. In our model, the pre-duplication FERR gene of the ancestor promoted female functions, and suppressing these created males in the dioecious descendant species.

Type-A RR genes have a very complex regulatory network, not currently well characterized, and, although transcriptomic data from our transgenic A. Each line number represents an independent transgenic line.

a The first and second row show the stigma hypertrophy and exsertion commonly observed in FERR -overexpressing plants; the third row shows extreme floral phenotypes observed in two FERR -overexpressing lines. A flower with two bent pistils left and one with carpel-like sepals right, red arrow were found in lineand line middle produced a flower with one bent pistil and an unfused carpel.

Due to the abnormal floral structures, it is difficult to stage the flowers in the third row from the top.

However, by relying on the developmental stage of petals, stamens, and sepals, we classified these flowers as late stages b Dissected flowers of wild type WT and MSL -overexpressing plants. WT flowers have four long and two short stamens tetradynamous stamenwhereas the flowers from MSL -overexpressing plants had six long stamens line 2extra stamens lines 51 and 13or reduplicated Y-shaped stamens lines 7 and Raw reads matching the MSL sequence in our male genome sequence were extracted and assembled to confirm the male-specificity in our GWAS samples Supplementary Fig.

Based on a de novo repeat library constructed from P. deltoides chromosomes Supplementary Data 2MSL homology regions in Populus and Salix species. However, the only complete copy was the one in YHS1. MSL sequences are completely absent from the A. thaliana and Oryza sativa genomes. Although most other poplar and willow species have only partial sequences Supplementary Data 2a complete MSL is present in the genome of a male P.

simonii in a different subgenus from P. deltoidessee Supplementary Data 2. This sequence is also in a YHS at the peritelomeric end of chromosome XIX, as in P. deltoidesand is absent from females of this species, and could be involved in sex determination in these two species.

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A function for a transposable element is not implausible, as such elements generate lncRNAs in many species 39404142 qRT-PCR revealed continuous expression of MSL in male P. deltoides Fig. Transcripts are detected in lncRNA-seq, but not general RNA-Seq Supplementary Fig. To test for a phenotypic effect of MSLwe over-expressed it in A.

Overexpression of PdeMSL in A. thaliana to levels 5- to fold higher than levels in P. deltoides did not affect the pistils, and seed set was unaffected, but did affect the androecium, commonly resulting in flowers with six long stamens, or seven or occasionally 8 stamens, stamens bearing two anthers, or branched stamens Fig. thaliana flowers. These androecium-specific effects suggest that the MSL gene may promote maleness in P. Supporting this, GO analysis revealed that genes with significantly increased expression in our transgenic lines Supplementary Data 3gene expression data from A.

thaliana overexpressing MSLSupplementary Table 7show significant enrichment for pollen development functions Supplementary Fig. deltoides belongs to subgenus Aigeiros in the genus Populus.

To test whether the hemizygous YHS1 region is present in other poplars, we sequenced the genome of a male P. davidianain the same subgenus, Leuceas P. tremula and P. tremuloides in an earlier-branching section of Populus than Aigeiros 44 ; sex-determining regions of all three subgenus Leuce species map to the pericentromeric region of chromosome XIX 17 PdaFERR-R shares twelve duplicated segments with its putative progenitor, PdaFERRbut, unlike the P.

deltoides duplication, only exon 1 of FERR is duplicated, and no HEMA1 exons are present Supplementary Fig. Aligning the sequences flanking P. trichocarpa genomes revealed that this YHS is in the pericentromeric region of chromosome XIX. The different locations in species in the two subgenera support the hypothesis that their dioecy evolved independently 29yet involved a similar mechanism. Neither P.

davidiananor P. tremula has a complete MSL sequence, and therefore probably have no active PdeMSL orthologs. Partial MSL sequences were found in contigs in many genome regions, but no lncRNA transcripts were detected from the P. davidiana chromosome XIX peritelomeric and pericentromeric regions copies Supplementary Fig.

The development of female and male flowers in plants usually involves genes with spatially highly specific expression within the plant body or the flower primordia, and specific developmental timing.

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Most sex-limited and sex-biased genes in plants are not carried on the sex chromosomes, and their expression levels are probably controlled by an upstream sex-determining gene or genes 31 Many genes probably function in the development of sexual dimorphisms of poplars, but we propose that FERR-R is the upstream female-suppressor gene. deltoides XX females, FERR function is active due to the absence of the FERR-R gene, which is male-specific being present only as a Y-linked copy in the YHS1 of the Y haplotype, and absent from the X-linked region.

Although FERR-R expression is not confined to the flower development stage when sex determination occurs, temporal specificity is provided by FERRwhich is expressed only during the initiation of carpel primordia and early female flower development, and our transformation experiments in A. thaliana demonstrate that it is a female promotor. FERR belongs to the type-A RR gene family of transcription repressors in cytokinin signaling 30and altering cytokinin signaling has been reported to affect flower development RR genes have been suggested as sex determiners in other plants, including kiwifruit 8S.

purpurea 22 and Ginkgo Finally, a recent study showed that, in P. tremula in subgenus Leucelike P. davidianaknockout of the ortholog of the P.

deltoides FERR gene ARR17 in P. tremulain female trees converted them into males, indicating that P. tremula has a single-gene sex determination system However, the hypothesis that FERR-R suppresses femaleness, creating males, does not account for the evolution of females from the cosexual ancestor from which dioecious poplars evolved.

This ancestor must have had a functional female-promoting FERR gene, or a similar ARR17 homolog. Its loss of activity through partial duplication could have created male, which would produce a population with cosexuals and males termed androdioecy. Androdioecy is, however, extremely rare, and requires very unusual conditions to evolve 7. Even if such an evolutionary change did occur, another change is still necessary to generate females.

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This would require a mutation causing loss of male functions, to convert the cosexuals into females. A mutation within the same gene as the femaleness suppressor is formally possible, resulting in a single-gene sex determination system. thaliana over-expression affects only the pistils. A second gene therefore seems to be required to explain the evolution of dioecy in poplars.

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Two possibilities exist for this second gene. A second possibility is that the MSL sequence is a domesticated transposable element that produces lncRNAs that promote male functions. If the cosexual ancestor possessed this gene, its loss would create females, but the gene would remain present in the male-determining region as observed in the fully Y-linked region of P.

Our findingthat MSL over-expression affects the A. thaliana androecium, but not the gynoecium, and alters expression of genes with male functions, is consistent with this possibility. To test this possibility further, we asked whether MSL sequences are shared between different poplar species. Presence of a TE sequence at the same location in multiple species is unlikely, because TE insertions are rarely fixed in all individuals of a species.

Our finding of a complete MSL sequence in P. simonii in a different subgenus, Tacamahacafrom the one, Aigeiro s, that includes P. deltoidessee Supplementary Data 2therefore suggests that that this sequence may have a function in these species. The retention of a complete sequence of such an insertion for a long evolutionary time, corresponding to the divergence of two subgenera, is unexpected, and could signify that it has a plant function, such as increasing male functions.

Alternatively a mutation that increased male functions could have arisen on chromosome XIX after the chromosome acquired its male-determining locus. If it arose on a Y haplotype that happened to carry the MSL insertion, the resulting selective sweep would have led to this haplotype replacing the ancestral version though the maintenance of its complete sequence remains surprising.

However, function of MSL is evident in heterologously expressed A. thaliana in this study.

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Without a test of its function in poplar, such as a knockout, we cannot currently determine its role in androecia development in poplar. Moreover, findings in this study show that MSL cannot be essential for male functions in all Salicaceae species, given that other poplar and willow species have only partial sequences, and that the knockout of a single gene in P.

tremulaARR17converted female trees into males davidianain the same subgenus as P. tremula subgenus Leuceonly partial MSL homologous sequences are present, and the FERR-R duplication is in the pericentromeric region of chromosome XIX Supplementary Data 2.

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These two differences from the findings in subgenera Aigeiro s P. deltoides and Tacamahaca P. simonii suggest that dioecy evolved independently in these taxa, and in subgenus Leuce. It is unknown how females of P. davidianaor P.

tremula evolved. If a gene like MSL was involved, it might no longer be essential after FERR-R appeared, and have been lost.

It will be important in the future to locate the sex determining loci in more poplar species, to determine whether a peritelomeric location generally correlates with the presence of a complete MSL gene in the region, and a pericentromeric location with its absence. Nevertheless, the single-gene and possible two-gene systems in different sections of Populus make this genus particularly interesting for studying the evolution of sex determination in plants.

Many sex chromosomes, including the mammalian, bird, and Drosophila Ys, have evolved suppressed crossing over, sometimes followed by loss of large numbers of genes present on the X and on the Y ancestorcausing hemizygosity in males, a process known as genetic degeneration 48 The P. deltoides sex-determining genes also appear to be in a non-recombining region, but it is physically much smaller than in these animals, and even than the regions in plants such as papaya 5051kiwifruit 52and asparagus 5.

Our analysis revealed that FERR-R originated by segmental duplication of the FERR gene perhaps following a male-sterility mutation involving deletion of the MSL gene from the genome region into which the duplicate copy inserted, or perhaps followed by insertion of an MSL sequence into the region.

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