Advertisement

Chromosoma

, Volume 127, Issue 4, pp 505–513 | Cite as

Chromosome painting in meiosis reveals pairing of specific chromosomes in polyploid Solanum species

  • Li He
  • Guilherme T. Braz
  • Giovana A. Torres
  • Jiming JiangEmail author
Original Article

Abstract

Analysis of chromosome pairing has been an important tool to assess the genetic similarity of homologous and homoeologous chromosomes in polyploids. However, it is technically challenging to monitor the pairing of specific chromosomes in polyploid species, especially for plant species with a large number of small chromosomes. We developed oligonucleotide-based painting probes for four different potato chromosomes. We demonstrate that these probes are robust enough to monitor a single chromosome throughout the prophase I of meiosis in polyploid Solanum species. Cultivated potato (Solanum tuberosum, 2n = 4x = 48) is an autotetraploid. We demonstrate that the four copies of each potato chromosome pair as a quadrivalent in 66–78% of the meiotic cells at the pachytene stage. Solanum demissum (2n = 6x = 72) is a hexaploid and has been controversial regarding its nature as an autopolyploid or allopolyploid. Interestingly, no hexavalent pairing was observed in meiosis. Instead, we observed three independent bivalents in 83–98% of the meiotic cells at late diakinesis and early metaphase I for the four chromosomes. These results suggest that S. demissum has evolved into a cytologically stable state with predominantly bivalent pairing in meiosis.

Keywords

Polyploids Chromosome pairing Meiosis Chromosome painting 

Notes

Acknowledgements

We thank Drs. Bernd Friebe and Tomás Naranjo for valuable comments on the manuscript.

Author’s contributions

J.J. conceived the research, L.H. and G.T.B. and conducted FISH experiments. L.H., G.T.B., G.A.T., and J.J. analyzed data. J.J. wrote the article.

Funding information

This research was supported partially by National Science Foundation (NSF) grant ISO-1237969 and MSU startup funds to J.J.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

412_2018_682_MOESM1_ESM.pdf (1.4 mb)
Figure S1 (PDF 1387 kb)

References

  1. Armstrong KC (1971) Chromosome association at pachytene and metaphase in Medicago sativa. Can J Genet Cytol 13:697–702CrossRefGoogle Scholar
  2. Bomblies K, Jones G, Franklin C, Zickler D, Kleckner N (2016) The challenge of evolving stable polyploidy: could an increase in "crossover interference distance" play a central role? Chromosoma 125:287–300CrossRefGoogle Scholar
  3. 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 208:513–523CrossRefGoogle Scholar
  4. Calderon MD, Rey MD, Cabrera A, Prieto P (2014) The subtelomeric region is important for chromosome recognition and pairing during meiosis. Sci Rep-Uk 4:6488CrossRefGoogle Scholar
  5. Chang SB, de Jong H (2005) Production of alien chromosome additions and their utility in plant genetics. Cytogenet Genome Res 109:335–343CrossRefGoogle Scholar
  6. Curtis CA, Lukaszewski AJ, Chrzastek M (1991) Metaphase I pairing of deficient chromosomes and genetic mapping of deficiency breakpoints in common wheat. Genome 34:553–560CrossRefGoogle Scholar
  7. Darlington CD (1929) Meiosis in polyploids. II Aneuploid hyacinths. J Genet 21:17–56CrossRefGoogle Scholar
  8. Darlington CD (1931) Meiosis in diploid and tetraploid Primula sinensis. J Genet 24:65–96CrossRefGoogle Scholar
  9. Davies A, Jenkins G, Rees H (1990) Diploidisation of Lotusc corniculatus L. (Fabaceae) by elimination of multivalents. Chromosoma 99:289–295CrossRefGoogle Scholar
  10. Dong FG, Song JQ, Naess SK, Helgeson JP, Gebhardt C, Jiang JM (2000) Development and applications of a set of chromosome-specific cytogenetic DNA markers in potato. Theor Appl Genet 101:1001–1007CrossRefGoogle Scholar
  11. Doyle JJ, Sherman-Broyles S (2017) Double trouble: taxonomy and definitions of polyploidy. New Phytol 213:487–493CrossRefGoogle Scholar
  12. Filiault D, Ballerini E, Mandakova T, Akoz G, Derieg N, Schmutz J, Jenkins J, Grimwood J, Shu S, Hayes R, Hellsten U, Barry K, Yan J, Mihaltcheva S, Karafiatova K, Nizhynska V, Lysak M, Hodges S, Nordborg M (2018) The Aquilegia genome: adaptive radiation and an extraordinarily polymorphic chromosome with a unique history. bioRxiv:264101Google Scholar
  13. Fjellstrom RG, Beuselinck PR, Steiner JJ (2001) RFLP marker analysis supports tetrasonic inheritance in Lotus corniculatus L. Theor Appl Genet 102:718–725CrossRefGoogle Scholar
  14. Garriga-Caldere K, Huigen DJ, Jacobsen E, Ramanna MS (1999) Prospects for introgressing tomato chromosomes into the potato genome: an assessment through GISH analysis. Genome 42:282–288CrossRefGoogle Scholar
  15. Gillies CB (1989) Chromosome pairing and fertility in polyploids. In: Gillies CB (ed) Fertility and chromosome pairing: recent studies in plants and animals. CRC Press, Boca Raton, pp 137–176Google Scholar
  16. Gong ZY, Wu YF, Koblizkova A, Torres GA, Wang K, Iovene M, Neumann P, Zhang WL, Novak P, Buell CR, Macas J, Jiang JM (2012) Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24:3559–3574CrossRefGoogle Scholar
  17. Han YH, Zhang T, Thammapichai P, Weng YQ, Jiang JM (2015) Chromosome-specific painting in cucumis species using bulked oligonucleotides. Genetics 200:771–779CrossRefGoogle Scholar
  18. Hardigan MA, Crisovan E, Hamilton JP, Kim J, Laimbeer P, Leisner CP, Manrique-Carpintero NC, Newton L, Pham GM, Vaillancourt B, Yang XM, Zeng ZX, Douches DS, Jiang JM, Veilleux RE, Buell CR (2016) Genome reduction uncovers a large dispensable genome and adaptive role for copy number variation in asexually propagated Solanum tuberosum. Plant Cell 28:388–405CrossRefGoogle Scholar
  19. Hawkes JG (1958) Kartoffel: I. taxonomy, cytology and crossability. In: Kappert H, Rudorf W (eds) Handbuch der Pflanzenzüchtung, 2nd edn. vol 3, Berlin, Paul Parey Verlag, pp 1–43Google Scholar
  20. Hijmans R, Gavrilenko T, Stephenson S, Bamberg J, Salas A, Spooner DM (2007) Geographic and environmental range expansion through polyploidy in wild potatoes (Solanum section Petota). Glob Ecol Biogeogr 16:485–495CrossRefGoogle Scholar
  21. Hollister JD, Arnold BJ, Svedin E, Xue KS, Dilkes BP, Bomblies K (2012) Genetic adaptation associated with genome doubling in autotetraploid Arabidopsis arenosa. PLoS Genet 8:e1003093CrossRefGoogle Scholar
  22. Hou LL, Xu M, Zhang T, Xu ZH, Wang WY, Zhang JX, Yu MM, Ji W, Zhu CW, Gong ZY, Gu MH, Jiang JM, Yu HX (2018) Chromosome painting and its applications in cultivated and wild rice. BMC Plant Biol 18:110CrossRefGoogle Scholar
  23. Iovene M, Wielgus SM, Simon PW, Buell CR, Jiang JM (2008) Chromatin structure and physical mapping of chromosome 6 of potato and comparative analyses with tomato. Genetics 180:1307–1317CrossRefGoogle Scholar
  24. Irikura Y (1976) Cytogenetic studies on the haploid plants of tuberbearing Solanum species. II. Cytogenetic investigations on haploid plants and interspecific hybrids by utilizing haploidy. Res Bull Hokkaido Natl Agric Res Stn 115:1–80Google Scholar
  25. Jansky S (2000) Breeding for disease resisatnce in potato. Plant Breeding Reviews 19:69–156Google Scholar
  26. Ji Y, Chetelat RT (2007) GISH analysis of meiotic chromosome pairing in Solanum lycopersicoides introgression lines of cultivated tomato. Genome 50:825–833CrossRefGoogle Scholar
  27. Kamstra SA, Ramanna MS, De Jeu MJ, Kuipers AGJ, Jacobsen E (1999) Homoeologous chromosome pairing in the distant hybrid Alstroemeria aurea x A. inodora and the genome composition of its backcross derivatives determined by fluorescence in situ hybridization with species-specific probes. Heredity 82:69–78CrossRefGoogle Scholar
  28. Kato A, Lamb JC, Birchler JA (2004) Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc Natl Acad Sci U S A 101:13554–13559CrossRefGoogle Scholar
  29. Kishimoto T, Yamakawa M, Nakazawa D, Amano J, Kuwayama S, Nakano M (2014) Meiotic chromosome pairing in intergeneric hybrids of colchicaceous ornamentals revealed by genomic in situ hybridization (GISH). Euphytica 200:251–257CrossRefGoogle Scholar
  30. Krebs SL, Hancock JF (1989) Tetrasomic inheritance of isoenzyme markers in the highbush blueberry Vaccinium corymbosum L. Heredity 63:11–18CrossRefGoogle Scholar
  31. Law CN, Snape JW, Worland AJ (1987) Aneuploidy in wheat and its uses in genetic analysis In: Lupton FGH (ed) Wheat Breeding, pp 71–108CrossRefGoogle Scholar
  32. Loidl J (1986) Synaptonemal complex spreading in Allium. II. Tetraploid A. vineale. Can J Genet Cytol 28:754–761CrossRefGoogle Scholar
  33. Loidl J, Jones GH (1986) Synaptonemal complex spreading in Allium .1. Triploid A. sphaerocephalon. Chromosoma 93:420–428CrossRefGoogle Scholar
  34. Lysak MA, Fransz PF, Ali HBM, Schubert I (2001) Chromosome painting in Arabidopsis thaliana. Plant J 28:689–697CrossRefGoogle Scholar
  35. Maestra B, Naranjo T (1998) Homoeologous relationships of Aegilops speltoides chromosomes to bread wheat. Theor Appl Genet 97:181–186CrossRefGoogle Scholar
  36. Mandakova T, Kovarik A, Zozomova-Lihova J, Shimizu-Inatsugi R, Shimizu KK, Mummenhoff K, Marhold K, Lysak MA (2013) The more the merrier: recent hybridization and polyploidy in Cardamine. Plant Cell 25:3280–3295CrossRefGoogle Scholar
  37. Mandakova T, Marhold K, Lysak MA (2014) The widespread crucifer species Cardamine flexuosa is an allotetraploid with a conserved subgenomic structure. New Phytol 201:982–992CrossRefGoogle Scholar
  38. Mandakova T, Gloss AD, Whiteman NK, Lysak MA (2016) How diploidization turned a tetraploid into a pseudotriploid. Am J Bot 103:1187–1196CrossRefGoogle Scholar
  39. Marks GE (1955) Cytogenetic studies in tuberous Solanum species I. genomic differentiation in the group demissa. J Genet 53:262–269CrossRefGoogle Scholar
  40. Matsubayashi M (1991) Phylogenetic relationships in the potato and its related species. In: Tsuchiya T, Gupta P (eds) Chromosome engineering in plants: genetics, breeding, evolution. Elsevier, Amsterdam, pp 93–118Google Scholar
  41. Moens PB (1970) The fine structure of meiotic chromosome pairing in natural and artificial Lilium polyploids. J Cell Sci 7:55–63PubMedGoogle Scholar
  42. Naranjo T, Roca A, Goicoechea PG, Giraldez R (1987) Arm homoeology of wheat and rye chromosomes. Genome 29:873–882CrossRefGoogle Scholar
  43. Parisod C, Holderegger R, Brochmann C (2010) Evolutionary consequences of autopolyploidy. New Phytol 186:5–17CrossRefGoogle Scholar
  44. Pendinen G, Spooner DM, Jiang JM, Gavrilenko T (2012) Genomic in situ hybridization reveals both auto- and allopolyploid origins of different north and central American hexaploid potato (Solanum sect. Petota) species. Genome 55:407–415CrossRefGoogle Scholar
  45. Qu M, Li K, Han Y, Chen L, Li Z, Han Y (2017) Integrated karyotyping of woodland strawberry (Fragaria vesca) with oligopaint FISH probes. Cytogenet Genome Res 153:158–164CrossRefGoogle Scholar
  46. Quiros CF (1982) Tetrasomic segregation for multiple alleles in Alfalfa. Genetics 101:117–127PubMedPubMedCentralGoogle Scholar
  47. Reddi VR (1970) Pachytene pairing and nature of polyploidy in Sorghum arundinaceum. Caryologia 23:295–302CrossRefGoogle Scholar
  48. Rodriguez F, Spooner DM (2009) Nitrate reductase phylogeny of potato (Solanum sect. Petota) genomes with emphasis on the origins of the polyploid species. Syst Bot 34:207–219CrossRefGoogle Scholar
  49. Scholz M, Pendinen G (2016) The effect of homoeologous meiotic pairing in tetraploid Hordeum bulbosum L. x H. vulgare L. hybrids on alien introgressions in offspring. Cytogenet Genome Res 150:139–149CrossRefGoogle Scholar
  50. Schubert I, Fransz PF, Fuchs J, de Jong JH (2001) Chromosome painting in plants. Methods Cell Sci 23:57–69CrossRefGoogle Scholar
  51. Spooner DM, Rodriguez F, Polgar Z, Ballard LE, Jansky SH (2008) Genomic origins of potato polyploids: GBSSI gene sequencing data. Crop Sci 48:S27–S36CrossRefGoogle Scholar
  52. Stack S (1982) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. 1. The technique. Stain Technol 57:265–272CrossRefGoogle Scholar
  53. The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195CrossRefGoogle Scholar
  54. Wolf PG, Soltis PS, Soltis DE (1989) Tetrasomic inheritance and chromosome pairing behaviour in the naturally occurring autotetraploid Heuchera grossulariifolia (Saxifragaceae). Genome 32:655–659CrossRefGoogle Scholar
  55. Xin H, Zhang T, Han Y, Wu Y, Shi J, Xi M, Jiang J (2018) Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides. Chromosoma 127:313–321CrossRefGoogle Scholar
  56. Yant L, Hollister JD, Wright KM, Arnold BJ, Higgins JD, Franklin FCH, Bomblies K (2013) Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr Biol 23:2151–2156CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Horticulture InstituteSichuan Academy of Agricultural SciencesChengduChina
  2. 2.Department of HorticultureUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Department of Plant BiologyMichigan State UniversityEast LansingUSA
  4. 4.Department of HorticultureMichigan State UniversityEast LansingUSA
  5. 5.Departmento de BiologiaUniversidade Federal de LavrasLavrasBrazil

Personalised recommendations