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Nicotiana suaveolens accessions with different ploidy levels exhibit different reproductive isolation mechanisms in interspecific crosses with Nicotiana tabacum

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Abstract

Reproductive isolation, including prezygotic and postzygotic barriers, is a mechanism that separates species. Many species in the Nicotiana section Suaveolentes exhibit reproductive isolation in crosses with Nicotiana tabacum. In this study, we investigated whether the chromosome numbers and ploidy levels of eight Nicotiana suaveolens accessions are related to the reproductive isolation after crosses with N. tabacum by flow cytometry and chromosome analyses. Additionally, the internal transcribed spacer (ITS) regions of the eight N. suaveolens accessions were sequenced and compared with the previously reported sequences of 22 Suaveolentes species to elucidate the phylogenetic relationships in the section Suaveolentes. We revealed that four N. suaveolens accessions comprised 64 chromosomes, while the other four accessions carried 32 chromosomes. Depending on the ploidy levels of N. suaveolens, several types of reproductive isolation were observed after crosses with N. tabacum, including decreases in the number of capsules and the germination rates of hybrid seeds, as well as hybrid lethality and abscission of enlarged ovaries at 12–17 days after pollination. A phylogenetic analysis involving ITS sequences divided the eight N. suaveolens accessions into three distinct clades. Based on the results, we confirmed that N. suaveolens accessions vary regarding ploidy levels and reproductive isolation mechanisms in crosses with N. tabacum. These accessions will be very useful for revealing and characterizing the reproductive isolation mechanisms in interspecific crosses and their relationships with ploidy levels.

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References

  • Baldwin BG (1993) Molecular phylogenetics of Calycadenia (Compositae) based on ITS sequences of nuclear ribosomal DNA: chromosomal and morphological evolution reexamined. Am J Bot 80:222–238

    Article  CAS  Google Scholar 

  • Bushell C, Spielman M, Scott RJ (2003) The basis of natural and artificial postzygotic hybridization barriers in Arabidopsis species. Plant Cell 15:1430–1442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chase MW, Knapp S, Cox AV et al (2003) Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Ann Bot 92:107–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarkson JJ, Knapp S, Garcia VF, Olmstead RG, Leitch AR, Chase MW (2004) Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions. Mol Phylogenet Evol 33:75–90

    Article  CAS  PubMed  Google Scholar 

  • Clarkson JJ, Kelly LJ, Leitch AR, Knapp S, Chase MW (2010) Nuclear glutamine synthetase evolution in Nicotiana: phylogenetics and the origins of allotetraploid and homoploid (diploid) hybrids. Mol Phylogenet Evol 55:99–112

    Article  CAS  PubMed  Google Scholar 

  • Dickinson GR, Lee DJ, Wallace HM (2012) The influence of pre- and post-zygotic barriers on interspecific Corymbia hybridization. Ann Bot 109:1215–1226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doležel J, Bartos J (2005) Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot 95:99–110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Goodspeed TH (1954) The genus Nicotiana. Chronica Botanica Company, Waltham

    Google Scholar 

  • Guo J, Xu X, Li W et al (2016) Overcoming inter-subspecific hybrid sterility in rice by developing indica-compatible japonica lines. Sci Rep 6:26878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichitani K, Namigoshi K, Sato M et al (2007) Fine mapping and allelic dosage effect of Hwc1, a complementary hybrid weakness gene in rice. Theor Appl Genet 114:1407–1415

    Article  CAS  PubMed  Google Scholar 

  • Inoue E, Marubashi W, Niwa M (1994) Simple method for overcoming the lethality observed in the hybrid between Nicotiana suaveolens and N. tabacum. Breed Sci 44:333–336

    Google Scholar 

  • Ishikawa R, Ohnishi T, Kinoshita Y, Eiguchi M, Kurata N, Kinoshita T (2011) Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. Plant J 65:798–806

    Article  CAS  PubMed  Google Scholar 

  • Japan Tobacco Inc (1994) The genus Nicotiana illustrated. Japan Tobacco Inc, Tokyo

    Google Scholar 

  • Kradolfer D, Wolff P, Jiang H, Siretskiy A, Köhler C (2013) An imprinted gene underlies postzygotic reproductive isolation in Arabidopsis thaliana. Dev Cell 26:525–535

    Article  CAS  PubMed  Google Scholar 

  • Kuboyama T, Saito T, Matsumoto T et al (2009) Fine mapping of HWC2, a complementary hybrid weakness gene, and haplotype analysis around the locus in rice. Rice 2:93–103

    Article  Google Scholar 

  • Ladiges PY, Marks CE, Nelson G (2011) Biogeography of Nicotiana section Suaveolentes (Solanaceae) reveals geographical tracks in arid Australia. J Biogeogr 38:2066–2077

    Article  Google Scholar 

  • Leitch IJ, Hanson L, Lim KY et al (2008) The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Ann Bot 101:805–814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis RS, Nicholson JS (2007) Aspects of the evolution of Nicotiana tabacum L. and the status of the United States Nicotiana Germplasm Collection. Genet Resour Crop Evol 54:727–740

    Article  Google Scholar 

  • Li Z, Pinson SRM, Paterson AH, Park WD, Stansel JW (1997) Genetics of hybrid sterility and hybrid breakdown in an intersubspecific rice (Oryza sativa L.) population. Genetics 145:1139–1148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manabe T, Marubashi W, Onozawa Y (1989) Temperature-dependent conditional lethality in interspecific hybrids between Nicotiana suaveolens Lehm. and N. tabacum L. In: Proceedings of the 6th international congress of SABRAO, pp 459–462

  • Marubashi W, Onosato K (2002) Q chromosome controls the lethality of interspecific hybrids between Nicotiana tabacum and N. suaveolens. Breed Sci 52:137–142

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Otto F (1990) DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. In: Darzynkiewickz Z, Crissman HA (eds) Methods in cell biology. Academic Press, San Diego, pp 105–110

    Google Scholar 

  • Purdie RW, Symon DE, Haegi L (1982) Solanaceae. Flora of Australia 29:1–208

  • Rebernig CA, Lafon-Placette C, Hatorangan MR, Slotte T, Köhler C (2015) Non-reciprocal interspecies hybridization barriers in the Capsella genus are established in the endosperm. PLoS Genet 11:e1005295

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rieseberg LH, Blackman BK (2010) Speciation genes in plants. Ann Bot 106:439–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott RJ, Spielman M, Bailey J, Dickinson HG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125:3329–3341

    CAS  PubMed  Google Scholar 

  • Sekine D, Ohnishi T, Furuumi H et al (2013) Dissection of two major components of the post-zygotic hybridization barrier in rice endosperm. Plant J 76:792–799

    Article  CAS  PubMed  Google Scholar 

  • Stebbins GL (1966) Reproductive isolation and the origin of species. Processes of organic evolution. Prentice-Hall, Upper Saddle River, pp 85–112

    Google Scholar 

  • Sun Y, Skinner DZ, Liang GH, Hulbert SH (1994) Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA. Theor Appl Genet 89:26–32

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tezuka T (2012) Hybrid lethality in the genus Nicotiana. In: Mworia JK (ed) Botany. InTech, Rijeka, pp 191–210

    Google Scholar 

  • Tezuka T (2013) Hybrid lethality in Nicotiana: a review with special attention to interspecific crosses between species in sect. Suaveolentes and N. tabacum. In: Wallner F (ed) Herbaceous plants: cultivation methods, grazing and environmental impacts. Nova Science Publishers, New York, pp 69–94

    Google Scholar 

  • Tezuka T, Marubashi W (2004) Apoptotic cell death observed during the expression of hybrid lethality in interspecific hybrids between Nicotiana tabacum and N. suaveolens. Breed Sci 54:59–66

    Article  CAS  Google Scholar 

  • Tezuka T, Marubashi W (2006) Hybrid lethality in interspecific hybrids between Nicotiana tabacum and N. suaveolens: evidence that the Q chromosome causes hybrid lethality based on Q-chromosome-specific DNA markers. Theor Appl Genet 112:1172–1178

    Article  CAS  PubMed  Google Scholar 

  • Tezuka T, Marubashi W (2012) Genes in S and T subgenomes are responsible for hybrid lethality in interspecific hybrids between Nicotiana tabacum and Nicotiana occidentalis. PLoS One 7:e36204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tezuka T, Kuboyama T, Matsuda T, Marubashi W (2010) Seven of eight species in Nicotiana section Suaveolentes have common factors leading to hybrid lethality in crosses with Nicotiana tabacum. Ann Bot 106:267–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tezuka T, Matsuo C, Iizuka T, Oda M, Marubashi W (2012) Identification of Nicotiana tabacum linkage group corresponding to the Q chromosome gene(s) involved in hybrid lethality. PLoS One 7:e37822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • USDA ARS National Genetic Resources Program (2010) Germplasm Resources Information Network—(GRIN) [Online Database]. National Germplasm Resources Laboratory, Beltsville, Maryland. https://www.ars-grin.gov/npgs/index.html. Accessed Apr 2015

  • Wheeler HM (1935) Studies in Nicotiana. II. A taxonomic survey of the Australasian species. Univ Calif Publ Bot 18:45–68

    Google Scholar 

  • Yamada T, Marubashi W, Niwa M (1999) Detection of four lethality types in interspecific crosses among Nicotiana species through the use of three rescue methods for lethality. Breed Sci 49:203–210

    Article  Google Scholar 

  • Yamada T, Marubashi W, Niwa M (2000) Apoptotic cell death induces temperature-sensitive lethality in hybrid seedlings and calli derived from the cross of Nicotiana suaveolens × N. tabacum. Planta 211:614–622

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was partly supported by JSPS KAKENHI Grants (JP20880024 and JP25870627) from the Japan Society for the Promotion of Science.

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Correspondence to Takahiro Tezuka.

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He, H., Iizuka, T., Maekawa, M. et al. Nicotiana suaveolens accessions with different ploidy levels exhibit different reproductive isolation mechanisms in interspecific crosses with Nicotiana tabacum. J Plant Res 132, 461–471 (2019). https://doi.org/10.1007/s10265-019-01114-w

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