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Molecular Genetics and Genomics

, Volume 293, Issue 6, pp 1437–1452 | Cite as

Characterization of a large sex determination region in Salix purpurea L. (Salicaceae)

  • Ran Zhou
  • David Macaya-Sanz
  • Eli Rodgers-Melnick
  • Craig H. Carlson
  • Fred E. Gouker
  • Luke M. Evans
  • Jeremy Schmutz
  • Jerry W. Jenkins
  • Juying Yan
  • Gerald A. Tuskan
  • Lawrence B. Smart
  • Stephen P. DiFazio
Original Article

Abstract

Dioecy has evolved numerous times in plants, but heteromorphic sex chromosomes are apparently rare. Sex determination has been studied in multiple Salix and Populus (Salicaceae) species, and P. trichocarpa has an XY sex determination system on chromosome 19, while S. suchowensis and S. viminalis have a ZW system on chromosome 15. Here we use whole genome sequencing coupled with quantitative trait locus mapping and a genome-wide association study to characterize the genomic composition of the non-recombining portion of the sex determination region. We demonstrate that Salix purpurea also has a ZW system on chromosome 15. The sex determination region has reduced recombination, high structural polymorphism, an abundance of transposable elements, and contains genes that are involved in sex expression in other plants. We also show that chromosome 19 contains sex-associated markers in this S. purpurea assembly, along with other autosomes. This raises the intriguing possibility of a translocation of the sex determination region within the Salicaceae lineage, suggesting a common evolutionary origin of the Populus and Salix sex determination loci.

Keywords

Sex Salix Genome Suppressed recombination Dioecy 

Notes

Acknowledgements

We are grateful to Matt Olson for helpful comments on the manuscript.

Funding

This work was supported by grants from the USDA-NIFA CAP program (4705-WVU-USDA-9703), the DOE JGI Community Sequencing Program, and the NSF Dimensions of Biodiversity Program (DEB-1542509). Sequencing was conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, was supported by the Office of Science of the U.S. Department of Energy under Contract no. DE-AC02-05CH11231.

Compliance with ethical standards

Conflict of interest

All the authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Data availability

All raw sequencing data are available from the NCBI Sequence Read Archive (accessions SRP003908, SRP086434, and SRP086435) and the genome assembly and annotation are available from Phytozome (https://phytozome.jgi.doe.gov).

Supplementary material

438_2018_1473_MOESM1_ESM.xlsx (149 kb)
Table S1 Significant markers (LOD>3.5) from QTL mapping of sex. The table includes linkage group (LG), map positions (in centimorgans), map type (female backcross, F, male backcross, M, and intercross, IC), the physical scaffold from the genome assembly, the physical position of the marker in the genome assembly, and the frequency of different genotype configurations in the progeny. Table S2 Number of unfiltered GBS markers produced by the Tassel pipeline for the F2 family 317. Markers/100kb is the average number of markers per 100 kb interval. F:M Backcross is the ratio of markers in a Female Backcross configuration (heterozygous in the female parent, homozygous in the male parent) to markers in the Male Backcross configuration (homozygous in female parent, heterozygous in male parent). Table S3 Results of GWAS for sex. The table includes all significant markers (p<1x10-7). Table S4 Best matches for secondary S. purpurea SDRs to the S. purpurea and P. trichocarpa genomes. “Secondary Blast Hit” is the best blastn hit to the S. purpurea genome, after excluding self hits. Table S5 Markers showing a female-specific genotype configuration (one allele observed in females, none in males). These are presumably derived from W segments included in the genome assembly. Table S6 Scaffolds with >30% female-specific sequence. “Proportion W” is a calculation based on the proportion of the scaffold, after excluding gaps, that is present in the female sequence but absent in the male sequence (Female-Specific). Table S7 Repeat composition of the S. purpurea chromosomes. Table S8 Predicted genes found within the SDR of S. purpurea. “W Overlap” and “W proportion” represent the intersection of the location of the gene with female-specific genome segments. Omega values are the ratio of nonsynonymous (dN) to synonymous (dS) substitutions between the S. purpurea and P. trichocarpa orthologs. Multiple values are provided in cases with multiple Populus orthologs, presumably due to lineage-specific expansion (XLSX 148 KB)
438_2018_1473_MOESM2_ESM.pdf (4.5 mb)
Fig. S1 Pairwise Scaled Identity by State (IBS) for the (a) complete association population (N=112), (b) the complete F2 full sib Family (N=497), and (c) the association population with clones removed (N=75). The IBS cutoff used for identifying clonal pairs was 0.9. Fig. S2 Frequency of mapped markers with and without segregation distortion in family 317 for males and females. A. Markers in female-backcross configuration. B. Markers in male-backcross configuration. Notice the lack of undistorted (normal) markers on chr 19 in female backcross configuration. Fig. S3 Quantile–Quantile (Q–Q) plots of observed and expected P-values for the GWAS for sex. Red line indicates X = Y. Fig. S4 Box plots of average observed heterozygosity for males and females for sex-associated loci in the S. purpurea association population. Fig. S5 Distribution of differences in null allele frequency between females and males in the association population. Extreme values are shaded in red. Fig. S6 Proportion of reference sequence gaps (“assembly Ns”) in regions that showed no coverage in the female (a) or male (b) reference-based alignments. The male had 0 coverage primarily in regions with minimal reference gaps, suggesting that these are regions that are present in the female sequence and absent in the male. Fig. S7 Box plot showing that the proportion of repeat elements is elevated in the SDR. Fig. S8 Delineation of putative centromeres relative to the SDRs, for chromosomes not shown in the main text. Bar plots represent, from the top, gene density, repeat density, density of centromeric repeats, and physical:genetic distance ratio (Mb/cM) in 100 kb windows. Blue shading shows positions of putative centromeres, as defined by empirical thresholds represented by horizontal red lines. The position of the SDRs are indicated by vertical red shading. Fig. S9 Box plots comparing the composition of putative centromeric intervals to the rest of the genome, including (from top to bottom) gene content, total repeat content, presence of putative centromere-associated repeat elements, and physical:genetic distance ratio (Mb/cM). Fig. S10 Dot plot derived from aligning the S. suchowensis SDR (primarily located on scaffold64) to S. purpurea chr 15 using lastz. Fig. S11 Alignment of Kinesin genes from the SDR of S. purpurea and their closest ortholog in P. trichocarpa. SapurV1A.1267s0010 is artificially truncated due to an assembly gap overlapping with the gene. Conserved domains are highlighted and labeled. Tandem duplicate pairs are 1.) SapurV1A.0719s0080 and SapurV1A.0719s0090; and 2.) SapurV1A.1267s0010 and SapurV1A.1267s0020 (PDF 4560 KB)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ran Zhou
    • 1
  • David Macaya-Sanz
    • 1
  • Eli Rodgers-Melnick
    • 1
  • Craig H. Carlson
    • 2
  • Fred E. Gouker
    • 2
  • Luke M. Evans
    • 1
  • Jeremy Schmutz
    • 3
    • 4
  • Jerry W. Jenkins
    • 3
  • Juying Yan
    • 4
  • Gerald A. Tuskan
    • 4
    • 5
  • Lawrence B. Smart
    • 2
  • Stephen P. DiFazio
    • 1
  1. 1.Department of BiologyWest Virginia UniversityMorgantownUSA
  2. 2.Horticulture Section, School of Integrative Plant ScienceCornell University, New York State Agricultural Experiment StationGenevaUSA
  3. 3.HudsonAlpha Institute of BiotechnologyHuntsvilleUSA
  4. 4.Department of Energy Joint Genome InstituteWalnut CreekUSA
  5. 5.Biosciences DivisionOak Ridge National LabOak RidgeUSA

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