Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants

Abstract

Transposable elements, particularly LTR-retrotransposons, comprise the primary vehicle for genome size expansion in plants, while DNA removal through illegitimate recombination and intrastrand homologous recombination serve as the most important counteracting forces to plant genomic obesity. Despite extensive research, the relative impact of these opposing forces and hence the directionality of genome size change remains unknown. In Gossypium (cotton), the 3-fold genome size variation among diploids is due largely to copy number variation of the gypsy-like retrotransposon Gorge3. Here we combine comparative sequence analysis with a modeling approach to study the directionality of genome size change in Gossypium. We demonstrate that the rate of DNA removal in the smaller genomes is sufficient to reverse genome expansion through Gorge3 proliferation. These data indicate that rates of DNA loss can be highly variable even within a single plant genus, and that the known mechanisms of DNA loss can indeed reverse the march toward genomic obesity.

Fig. 1.

Neighbor-joining analysis of 724 PCR amplified Gorge3 reverse transcriptase sequences. Green = A-genome, G. herbaceum, purple = K-genome, G. exiguum, blue = D-genome, G. raimondii, and orange = Gossypioides kirkii. Cotton specific clades are indicated in gray.

Fig. 2.

Lineage-specific nature and timing of Gorge3 transposition in Gossypium. (A) Neighbor-joining analyses for PCR amplified Gorge3 sequences are presented, with lineage-specific sequences in color and sequences originating before diversification in black. (B) The curves represent the distribution of pairwise comparisons among lineage-specific sequences for each genome. The bottom axis represents the percent divergence, the top axis is the estimated transposition time, and the y axis is the density of pairwise comparisons at a given time point.

Fig. 3.

Phylogenetic relationships and estimated rates of Gorge3 gain and loss among diploid members of Gossypium. Branch lengths are to scale. Numbers above the branches represent the estimate of the exponential rate of change in Gorge3 DNA with confidence intervals in brackets. Taxa are shown at tips with entire genome size as well as the amount (in Mb) of extant DNA from Gorge3 elements.

Fig. 4.

Probability distributions for estimated parameters. We generated 1,000 replicate datasets for the current Gorge3 copy number by sampling uniformly between our 95% confidence intervals. (A) The frequency distribution of exponential rate parameters is shown for the four genomes. Orange: G. kirkii, Light blue: D, Green: A, Blue: K. Rates above 0 indicate that the number of Gorge3 elements is increasing, while numbers below 0 indicate that they are decreasing. In no case does the distribution overlap a rate of 0. (B) The frequency distribution of estimated number of Gorge3 elements in the common ancestor of the four genomes.