Plant Systematics and Evolution

, Volume 303, Issue 8, pp 1043–1060 | Cite as

Concerted evolution rapidly eliminates sequence variation in rDNA coding regions but not in intergenic spacers in Nicotiana tabacum allotetraploid

  • J. Lunerová
  • S. Renny-Byfield
  • R. Matyášek
  • A. Leitch
  • A. Kovařík
Original Article
Part of the following topical collections:
  1. Polyploidy in Shallow and Deep Evolutionary Times

Abstract

Nicotiana tabacum (tobacco) is a natural allotetraploid that formed from two diploid progenitors (N. sylvestris—S-genome, N. tomentosiformis—T-genome) within past 0.2 million years. Previous classical studies have shown that its 35S rDNA has been largely homogenised towards T-genome-like homeologs. However, the degree of conversion at single nucleotide resolution remains unknown. Here, we analysed intragenomic variation of rDNA at high resolution in natural tobacco, synthetic tobacco and the progenitors employing genomic, molecular and cytogenetic methods. In synthetic tobacco, we identified 13 highly (≥10% units) polymorphic sites in the 18S-5.8S-26S coding region. In contrast, only a single polymorphic site was detected in natural tobacco, indicating that gene conversion has removed most of the polymorphisms over shallow evolutionary times. However, the non-coding 26S-18S intergenic spacer (IGS) was highly polymorphic in both natural (57 polymorphic sites) and synthetic tobacco (128 polymorphic sites). In natural tobacco, most (64%) IGS polymorphisms were inherited from the N. tomentosiformis progenitor, while 36% appeared de novo indicating rapid rates of sequence divergence of IGS. FISH revealed that the T-genome-like units (harbouring N. tomentosiformis-type IGS) occurred on all four loci in tobacco variety 095-55, including those loci derived from N. sylvestris progenitor, while the variety SR-1 retained 1–2 S-genome loci unconverted and transcriptionally silenced. We discuss potential caveats associated with experimental and in silico approaches used for determination of rDNA polymorphisms. We also hypothesise that polyploidy-associated gene conversion may eliminate mutated and non-functional genes that have accumulated in progenitor genomes, thereby contributing to success of polyploidy species.

Keywords

Concerted evolution Genetic variation Nicotiana tabacum Polyploidy rDNA 

Notes

Acknowledgements

The research was funded by the Czech Science Foundation (P501/17/11642S and P506/16-02149J) and NERC.

Compliance with ethical standards

Conflicts of interest

The authors declare no conflicts of interest.

Human or animal participants

The present research does not involve human or animal participants. All authors have approved the manuscript.

Supplementary material

606_2017_1442_MOESM1_ESM.pdf (175 kb)
Online Resource 1. Sequence assembly of full length rDNA units from the GenBank clones. These sequences were used as references to build NGS consensus. (PDF 174 kb)
606_2017_1442_MOESM2_ESM.pdf (9.5 mb)
Online Resource 2. Sequence alignments of Nicotiana 35S rDNA (18S-ITS1-5.8S-ITS2-26S-IGS) reference and NGS consensus sequences. (a) A low resolution view. Coding regions and promoters are annotated with brown and red arrows, respectively. Regions of probes hybridisation are annotated with green arrows. Reference sequences used for haplotypic analysis and cDNA reads mapping are in cyan blue. PCR amplicons used in RT-CAPS analysis (Fig. 5) are in violet. Polymorphic restriction sites are in dark blue. (b) Nucleotide level-resolution view. (PDF 9768 kb)
606_2017_1442_MOESM3_ESM.xlsx (187 kb)
Online Resource 3. Data sets. Sheet 1 – List of DNA polymorphisms in N. sylvestris units. The polymorphic sites included single-nucleotide substitutions (SNV), insertions (INS), deletions (DEL) and multi-nucleotide variations (MNV). Sheet 2 – List of DNA polymorphisms in N. tomentosiformis units, as in sheet 1. Sheet 3 - List of DNA polymorphisms in N. tabacum var. SR-1 units, as in sheet 1. Sheet 4 - List of DNA polymorphisms in synthetic tobacco line TR1-A, as in sheet 1. Sheet 5 - List of DNA polymorphisms in an electronic N. sylvestris and N. tomentosiformis hybrid, as in sheet 1. Sheet 6 – Pairwise comparisons of NGS consensus and GenBank clones. Sheet 7 – Lengths of rDNA units and subregions. Sheet 8 – Summary of SNPs in the IGS region. Sheet 9 - Haplotypic analysis of rDNA subregions. Sheet 10 – Comparison of rDNA alleles between N. tabacum and N. tomentosiformis. Sheet 11 – ITS1 amplicon sequencing – cDNA. Sheet 12 – ITS1 amplicon sequencing – gDNA. Sheet 13 – Summary of ITS1 amplicon sequencing. (XLSX 187 kb)
606_2017_1442_MOESM4_ESM.pdf (362 kb)
Online Resource 4. Alignment of ITS1 consensus sequences from N. sylvestris (SYL58) and N. tomentosiformis (TOM58). (PDF 362 kb)
606_2017_1442_MOESM5_ESM.pdf (402 kb)
Online Resource 5. Analysis of tandem repeats in the A-subregion of IGS in N. tabacum, N. tomentosiformis, N. sylvestris. (PDF 401 kb)
606_2017_1442_MOESM6_ESM.pdf (536 kb)
Online Resource 6. Positions of restriction endonuclease recognition sites and regions of 26S probe hybridisation (rectangle) in rDNA units. (PDF 536 kb)

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© Springer-Verlag GmbH Austria 2017

Authors and Affiliations

  1. 1.Institute of BiophysicsAcademy of Sciences of the Czech Republic, v.v.i.BrnoCzech Republic
  2. 2.School of Biological and Chemical SciencesQueen Mary University of LondonLondonUK

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