The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae)

Abstract

Background: In studies looking at individual polyploid species, the most common patterns of genomic change are that either genome size in the polyploid is additive (i.e. the sum of parental genome donors) or there is evidence of genome downsizing. Reports showing an increase in genome size are rare. In a large-scale analysis of 3008 species, genome downsizing was shown to be a widespread biological response to polyploidy. Polyploidy in the genus Nicotiana (Solanaceae) is common with approx. 40 % of the approx. 75 species being allotetraploid. Recent advances in understanding phylogenetic relationships of Nicotiana species and dating polyploid formation enable a temporal dimension to be added to the analysis of genome size evolution in these polyploids.

Methods: Genome sizes were measured in 18 species of Nicotiana (nine diploids and nine polyploids) ranging in age from <200,000 years to approx. 4.5 Myr old, to determine the direction and extent of genome size change following polyploidy. These data were combined with data from genomic in situ hybridization and increasing amounts of information on sequence composition in Nicotiana to provide insights into the molecular basis of genome size changes.

Key results and conclusions: By comparing the expected genome size of the polyploid (based on summing the genome size of species identified as either a parent or most closely related to the diploid progenitors) with the observed genome size, four polyploids showed genome downsizing and five showed increases. There was no discernable pattern in the direction of genome size change with age of polyploids, although with increasing age the amount of genome size change increased. In older polyploids (approx. 4.5 million years old) the increase in genome size was associated with loss of detectable genomic in situ hybridization signal, whereas some hybridization signal was still detected in species exhibiting genome downsizing. The possible significance of these results is discussed.

Fig. 1.

Summary of phylogenetic relationships of Nicotiana species with proposed origins of polyploids. Data used in analyses include plastid and internal transcribed spacer loci. Figure modified and adapted from Knapp et al. (2004) using more recent phylogenetic information taken from glutamine synthase (J. J. Clarkson et al., unpubl. res.). Uncertainty concerning one of the parental genome donors for sections Polydicliae and Suaveolentes is indicated by question marks.

Fig. 2.

Direction of genome size evolution in Nicotiana polyploids varying in age from <200 000 years (A–C), approx. 1 Myr (D) to approx. 4·5 Myr (E) old. The observed versus expected 1C DNA amounts in nine polyploids were based on comparison between genome sizes determined for diploid and polyploid species using genome size data taken from Table 1. Putative diploid parental genome donors used for comparison of the various polyploids are based on a range of molecular and cytogenetic results (see text).

Fig. 3.

Comparison between 1C DNA amounts reported by Narayan (1987) (closed triangles) and those given in Table 1 of this paper (open triangles).

Fig. 4.

GISH to (A) Nicotiana nudicaulis and (B) N. nesophila root-tip metaphase probed with N. sylvestris genomic DNA (digoxigenin labelled, FITC detected, yellow/green) and N. obtusifolia (biotin labelled, Cy3 detected, red). Chromosomes were counterstained with DAPI (blue). Scale bar = 10 µm.