Chromosomal evolution in the plant family Solanaceae

Abstract

Background: Over the past decades, extensive comparative mapping research has been performed in the plant family Solanaceae. The recent identification of a large set of single-copy conserved orthologous (COSII) markers has greatly accelerated comparative mapping studies among major solanaceous species including tomato, potato, eggplant, pepper and diploid Nicotiana species (as well as tetraploid tobacco). The large amount of comparative data now available for these species provides the opportunity to describe the overall patterns of chromosomal evolution in this important plant family. The results of this investigation are described herein.

Results: We combined data from multiple COSII studies, and other comparative mapping studies performed in tomato, potato, eggplant, pepper and diploid Nicotiana species, to deduce the features and outcomes of chromosomal evolution in the Solanaceae over the past 30 million years. This includes estimating the rates and timing of chromosomal changes (inversions and translocations) as well as deducing the age of ancestral progenitor species and predicting their genome configurations.

Conclusions: The Solanaceae has experienced chromosomal changes at a modest rate compared with other families and the rates are likely conserved across different lineages of the family. Chromosomal inversions occur at a consistently higher rate than do translocations. Further, we find evidences for non-random positioning of the chromosomal rearrangement breakpoints. This finding is consistent with the similar finding in mammals, where hot spots for chromosomal breakages have apparently played a significant role in shaping genome evolution. Finally, by utilizing multiple genome comparisons we were able to reconstruct the most likely genome configuration for a number of now-extinct progenitor species that gave rise to the extant solanaceous species used in this research. The results from this study provide the first broad overview of chromosomal evolution in the family Solanaceae, and one of the most detailed thus far for any family of plants.

Figure 1

Phylogenetic relationships and estimated divergence time of selected solanaceous species. The phylogenetic tree with molecular dating is based on Additional File 1. The external node Nicotiana represents the most recent common ancestor of N. tomentosiformis and N. acuminata, an extinct species possibly living at 7.5MYA [11]. Estimated age of the 4 ancestral species (ATPt, ATE, ATP and ATN) is placed next to the corresponding interval node (highlighted with a black dot).

Figure 2

Comparing maps of multiple species using the tomato genetic map as common reference. (a) Species 1 and 2 both share the same gene order with tomato. (b) Species 1 and 2 both have an inversion and a translocation relative to tomato. Markers in blue and yellow segments come from two other tomato chromosomes. Breakpoint region (indicated by a black bar) of the translocation between species 1 and tomato is the interval of markers "g" and "i", and similarly that between species 2 and tomato is the interval of markers "h" and "i". (c) Species 1 and 2 each have an independent inversion relative to tomato. Breakpoint regions are indicated by black bars next to the tomato map.

Figure 3

An example of chromosomal rearrangements between the genomes of eggplant and tomato. The eggplant chromosome E4 combines two segments (E4a and E4b) orthologous to tomato T4 and T10 respectively, indicating a translocation between the two genomes. The breakpoint is located between markers TG386 and T677 (highlighted in red), and the region is indicated by a black bar beside E4. Orthologous marker pairs are connected by lines. A dash line indicates a marker of low mapping confidence on either or both maps that is not used for deduction of inversions. Vertical arrows beside E4 depict inversions in E4 with respect to T10.

Figure 4

Comparative maps of several solanaceous species and the deduced genome arrangement of MRCAs. T1-12, Pt1-12, E1-12, P1-12 and N1-12 represent 12 chromosomes of tomato, potato, eggplant, pepper and Nicotiana genomes respectively. Designation of chromosome segments (a-c) is detailed in Additional File 2. ATPt1-12, ATE1-12 and ATP1-12 represent 12 chromosomes of ATPt, ATE and ATP genomes. White dots indicate the approximate centromere location of the tomato chromosomes. Maps of the other species are depicted in a comparative way to the tomato map as follows. A black arrow indicates an inversion relative to tomato (a grey arrow for an uncertain inversion). A black bar indicates the breakpoint region of a translocation relative to tomato (a grey bar for an uncertain translocation). Two black bars connected by a curve indicate that the segment in between is excised in a translocation while the remained parts stay together, e.g. E10a is embedded in E3b. "1+" (or "2+") on a single arrow indicates that the region has experienced at least one (or two) inversions but the exact number remains to be determined. Position and length of arrows and bars are approximate. See the close-up figure in Additional File 3.

Figure 5

Chromosomal evolution in the family Solanaceae. The actual karyotype (chromosome 1-12) of tomato, potato, eggplant, pepper and Nicotiana, and the deduced karyotype of their MRCAs are presented. Each tomato chromosome is assigned a different color, and the orthologous counterparts in the other species are painted with the corresponding color, which therefore depicts the translocations differentiating these species. Black arrows on chromosomes represent the inversions that these species have experienced subsequent to divergence from their MRCA, i.e. inversions in tomato and potato relative to ATPt, inversions in eggplant and ATPt relative to ATE, and inversions in ATE and pepper relative to ATP. Position and length of the arrows are approximate (see Additional Files 2 for details). Grey arrows on the pepper chromosomes represent inversions between pepper and ATE but it remains to be determined along which lineage these inversions occurred. White dots indicate approximate centromere location of the tomato chromosomes [30] and putative centromere location of the eggplant and pepper chromosomes based on their synteny with tomato [9,10]. Broken chromosomes in the ATE and ATP genomes represent unknown karyotypes, in other words, organization of these chromosome segments remains to be determined.