Chromosoma

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Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides

  • Haoyang Xin
  • Tao Zhang
  • Yonghua Han
  • Yufeng Wu
  • Jisen Shi
  • Mengli Xi
  • Jiming Jiang
Original Article

Abstract

Dioecious species accounted for 6% of all plant species, including a number of crops and economically important species, such as poplar. However, sex determination and sex chromosome evolution have been studied only in few dioecious species. In poplar, the sex-determining locus was mapped to chromosome 19. Interestingly, this locus was mapped to either a peritelomeric or a centromeric region among different poplar species. We developed an oligonucleotide (oligo)-based chromosome painting probe based on the sequence of chromosome 19 from Populus trichocarpa. We performed chromosome painting in P. tomentosa and P. deltoides. Surprisingly, the distal end on the short arm of chromosome 19, which corresponds to the location of the sex-determining locus reported in several species, was not painted in both species. Thus, the DNA sequences associated with this region have not been anchored to the current chromosome 19 pseudomolecule, which was confirmed by painting of somatic metaphase chromosome 19 of P. trichocarpa. Interestingly, the unpainted distal ends of the two chromosome 19 did not pair at the pachytene stage in 22–24% of the meiotic cells in the two species, suggest that these regions from the sex chromosomes have structurally diverged from each other, resulting in the reduced pairing frequency. These results shed light on divergence of a pair of young sex chromosomes in poplar.

Keywords

Chromosome painting Sex chromosome Chromosome pairing Oligo-FISH Poplar 

Notes

Acknowledgements

The authors thank Dr. Qiang Cheng (Nanjing Forestry University, China) and Dr. Wenli Zhang (Nanjing Agriculture University, China) for their valuable discussion and advice for this research.

Funding information

The research was supported by grant 31670603 from the National Natural Science Foundation of China, grant 16KJA220001 from the Jiangsu Provincial Key Basic Research Foundation for Universities, the Doctorate Fellowship Foundation of Nanjing Forestry University, and funds from the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Supplementary material

412_2018_664_Fig5_ESM.gif (80 kb)
Fig. S1

Somatic metaphase painting of chromosome 19 in P. trichocarpa. The painting probe is detected by red color. The two arrows indicate the non-painted distal end of the chromosomes. Bars = 10 μm. (GIF 79 kb)

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High Resolution Image (TIFF 10133 kb)
412_2018_664_Fig6_ESM.gif (90 kb)
Fig. S2

Oligo-based painting of chromosome 19 in Populus simonii. The painting probe is detected by red color. The telomeres of all chromosomes are detected by green color. (a) Painting of chromosome 19 of P. simonii. (b) The pachytene chromosome 19 in (a) was digitally straightened and aligned with the sequence map. The peritelomeric gap is marked by two yellow lines. The three FISH signal gaps are marked by green lines. (c) Locations of 26,929 (red) oligos along the sequence map of poplar chromosome 19. Note: the three FISH signal gaps are aligned with three large gaps in c that lack oligos. The middle gap is the putative position of the centromere of chromosome 19. Bars = 10 μm. (GIF 89 kb)

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High Resolution Image (TIFF 9833 kb)
412_2018_664_Fig7_ESM.gif (66 kb)
Fig. S3

FISH mapping of five LRR genes (green signals) combined with the poplar chromosome 19 painting probe (red signals) in two Populus species. a FISH on a complete pachytene cell in P. tomentosa. b FISH on a complete pachytene cell in P. deltoides. Note: the five LRR genes (L1-L5) on chromosome 19 were indicated by the green arrows. The additional FISH signals, indicated by white arrows, were most likely derived from the cross-hybridization of the five probes to other LRR genes in the poplar genome. Bars = 10 μm. (GIF 66 kb)

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High Resolution Image (TIFF 6247 kb)
412_2018_664_Fig8_ESM.gif (56 kb)
Fig. S4

FISH mapping of probe L4 (green signals), a telomeric DNA probe (TEL, green signals), and the chromosome 19 painting probe (red signals) in P. tomentosa. Note: L4 generated two separate FISH signals (green arrows) on the chromosome. Bar = 10 μm (GIF 56 kb)

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High Resolution Image (TIFF 11428 kb)

References

  1. Blackburn K, Harrison J (1924) A preliminary account of the chromosomes and chromosome behaviour in the Salicaceae. Ann Bot 38:361–378CrossRefGoogle Scholar
  2. Braz GT, He L, Zhao HN, Zhang T, Semrau K, Rouillard J-M, Torres GA, Jiang JM (2018) Comparative oligo-FISH mapping: an efficient and powerful methodology to reveal karyotypic and chromosomal evolution. Genetics 208:513–523CrossRefPubMedGoogle Scholar
  3. Charlesworth B (1991) The evolution of sex chromosomes. Science 251:1030–1033CrossRefPubMedGoogle Scholar
  4. Charlesworth D (2002) Plant sex determination and sex chromosomes. Heredity 88:94–101CrossRefPubMedGoogle Scholar
  5. Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128CrossRefPubMedGoogle Scholar
  6. Cheng ZK, Buell CR, Wing RA, Gu M, Jiang JM (2001) Toward a cytological characterization of the rice genome. Genome Res 11:2133–2141CrossRefPubMedPubMedCentralGoogle Scholar
  7. Eckenwalder JE (1996) Systematics and evolution of Populus. In: Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research Press, Ottawa, pp 7–32Google Scholar
  8. Erlanson EW, Hermann FJ (1927) The morphology and cytology of perfect flowers in Populus tremuloides Michx. Mich Acad Sci Arts Lett 8:97–110Google Scholar
  9. Fransz P, Armstrong S, Alonso-Blanco C, Fischer TC, Torres-Ruiz RA , Jones G (1998) Cytogenetics for the model system Arabidopsis thaliana. Plant J 13:867–876Google Scholar
  10. Gaudet M, Jorge V, Paolucci I, Beritognolo I, Mugnozza GS, Sabtti M (2008) Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait. Tree Genet Genomes 4:25–36Google Scholar
  11. Geraldes A, Hefer CA, Capron A, Kolosova N, Martinez-Nunez F, Soolanayakanahally RY, Stanton B, Guy RD, Mansfield SD, Douglas CJ, Cronk QCB (2015) Recent Y chromosome divergence despite ancient origin of dioecy in poplars (Populus). Mol Ecol 24:3243–3256Google Scholar
  12. Han YH, Zhang T, Thammapichai P, Weng YQ, Jiang JM (2015) Chromosome-specific painting in Cucumis species using bulked oligonucleotides. Genetics 200:771–779CrossRefPubMedPubMedCentralGoogle Scholar
  13. Iovene M, Yu QY, Ming R, Jiang JM (2015) Evidence for emergence of sex-determining gene(s) in a centromeric region in Vasconcellea parviflora. Genetics 199:413–421CrossRefPubMedGoogle Scholar
  14. Islam-Faridi MN, Nelson CD, DiFazio SP, Gunter LE, Tuskan GA (2009) Cytogenetic analysis of Populus trichocarpa—ribosomal DNA, telomere repeat sequence, and marker-selected BACs. Cytogenet Genome Res 125:74–80CrossRefPubMedGoogle Scholar
  15. Jiang JM, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068CrossRefPubMedGoogle Scholar
  16. Jiang JM, Gill BS, Wang GL, Ronald PC, Ward DC (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci 92:4487–4491CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kersten B, Pakull B, Groppe K, Lueneburg J, Fladung M (2014) The sex-linked region in Populus tremuloides Turesson 141 corresponds to a pericentromeric region of about two million base pairs on P. trichocarpa chromosome 19. Plant Biol 16:411–418CrossRefPubMedGoogle Scholar
  18. Kersten B, Pakull B, Fladung M (2017) Genomics of sex determination in dioecious trees and woody plants. Trees-Struct Funct 31:1113–1125CrossRefGoogle Scholar
  19. Kocsis E, Trus BL, Steer CJ, Bisher ME, Steven AC (1991) Image averaging of flexible fibrous macromolecules: the clathrin triskelion has an elastic proximal segment. J Struct Biol 107:6–14CrossRefPubMedGoogle Scholar
  20. Lou QF, Zhang YX, He YH, Li J, Jia L, Cheng CY, Guan W, Yang SQ, Chen JF (2014) Single-copy gene-based chromosome painting in cucumber and its application for chromosome rearrangement analysis in Cucumis. Plant J 78:169–179CrossRefPubMedGoogle Scholar
  21. Ming R, Wang JP, Moore PH, Paterson AH (2007) Sex chromosomes in flowering plants. Am J Bot 94:141–150CrossRefPubMedGoogle Scholar
  22. Mousavi M, Tong CF, Liu FX, Tao ST, Wu JY, Li HG, Shi JS (2016) De novo SNP discovery and genetic linkage mapping in poplar using restriction site associated DNA and whole-genome sequencing technologies. BMC Genomics 17:656CrossRefPubMedPubMedCentralGoogle Scholar
  23. Pakull B, Groppe K, Meyer M, Markussen T, Fladung M (2009) Genetic linkage mapping in aspen (Populus tremula L. and Populus tremuloides Michx.) Tree Genet Genomes 5:505–515CrossRefGoogle Scholar
  24. Pakull B, Groppe K, Mecucci F, Gaudet M, Sabatti M, Fladung M (2011) Genetic mapping of linkage group XIX and identification of sex-linked SSR markers in a Populus tremula x Populus tremuloides cross. Can J For Res 41:245–253CrossRefGoogle Scholar
  25. Paolucci I, Gaudet M, Jorge V, Beritognolo I, Terzoli S, Kuzminsky E, Muleo R, Scarascia Mugnozza G, Sabatti M (2010) Genetic linkage maps of Populus alba L. and comparative mapping analysis of sex determination across Populus species. Tree Genet Genomes 6:863–875CrossRefGoogle Scholar
  26. Peto F (1938) Cytology of poplar species and natural hybrids. Can J For Res 16:445–455CrossRefGoogle Scholar
  27. Strauss SH, Martin FM (2004) Poplar genomics comes of age. New Phytol 164:1–4CrossRefGoogle Scholar
  28. Taylor G (2002) Populus: Arabidopsis for forestry. Do we need a model tree? Ann Bot 90:681–689CrossRefPubMedPubMedCentralGoogle Scholar
  29. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604CrossRefPubMedGoogle Scholar
  30. Tuskan GA, DiFazio S, Faivre-Rampant P, Gaudet M, Harfouche A, Jorge V, Labbé JL, Ranjan P, Sabatti M, Slavov G, Street N, Tschaplinski TJ, Yin TM (2012) The obscure events contributing to the evolution of an incipient sex chromosome in Populus: a retrospective working hypothesis. Tree Genet Genomes 8:559–571CrossRefGoogle Scholar
  31. Van Buijtenen J, Einspahr D (1959) Note on the presence of sex chromosomes in Populus tremuloides. Bot Gazette 121:60–61CrossRefGoogle Scholar
  32. Wang YX, Zhang B, Sun XY, Tan BY, Xu LA, Huang MR, Wang MX (2011) Comparative genome mapping among Populus adenopoda, P. alba, P. deltoides, P. euramericana and P. trichocarpa. Genes Genet Syst 86:257–268CrossRefPubMedGoogle Scholar
  33. Wang JP, Na JK, Yu QY, Gschwend AR, Han J, Zeng FC, Aryal R, VanBuren R, Murray JE, Zhang WL, Navajas-Perez R, Feltus FA, Lemke C, Tong EJ, Chen CX, Man Wai C, Singh R, Wang ML, Min XJ, Alam M, Charlesworth D, Moore PH, Jiang JM, Paterson AH, Ming R (2012) Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc Natl Acad Sci 109:13710–13715CrossRefPubMedPubMedCentralGoogle Scholar
  34. Xin HY, Lan Y, Shi JS, Ma Y, Xi ML (2016) Pachytene chromosome preparation in Populus deltoides Marsh. Curr Protoc Plant Bio 1:566–573CrossRefGoogle Scholar
  35. Yin TM, DiFazio SP, Gunter LE, Zhang XY, Sewell MM, Woolbright SA, Allan GJ, Kelleher CT, Douglas CJ, Wang MX, Tuskan GA (2008) Genome structure and emerging evidence of an incipient sex chromosome in Populus. Genome Res 18:422–430Google Scholar
  36. Yu QY, Hou SB, Feltus FA, Jones MR, Murray JE, Veatch O, Lemke C, Saw JH, Moore RC, Thimmapuram J, Liu L, Moore PH, Alam M, Jiang JM, Paterson AH, Ming R (2008) Low X/Y divergence in four pairs of papaya sex-linked genes. Plant J 53:124–132CrossRefPubMedGoogle Scholar
  37. Zhang WL, Wang XU, Yu QY, Ming R, Jiang JM (2008) DNA methylation and heterochromatinization in the male-specific region of the primitive Y chromosome of papaya. Genome Res 18:1938–1943CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Haoyang Xin
    • 1
  • Tao Zhang
    • 2
  • Yonghua Han
    • 3
  • Yufeng Wu
    • 4
  • Jisen Shi
    • 1
  • Mengli Xi
    • 1
  • Jiming Jiang
    • 5
  1. 1.Co-Innovation Center for Sustainable Forestry in Southern China/Key Laboratory of Forest Genetics and Biotechnology of Ministry of EducationNanjing Forestry UniversityNanjingChina
  2. 2.Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Centre for Modern Production Technology of Grain Crops/Key Laboratory of Plant Functional Genomics of the Ministry of EducationYangzhou UniversityYangzhouChina
  3. 3.The Key Laboratory of Biotechnology for Medicinal Plants of Jiangsu ProvinceJiangsu Normal UniversityXuzhouChina
  4. 4.The State Key Laboratory of Crop Genetics and Germplasm Enhancement, Bioinformatics CenterNanjing Agricultural UniversityNanjingChina
  5. 5.Department of Plant Biology, Department of HorticultureMichigan State UniversityEast LansingUSA

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