Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta - PubMed (original) (raw)

Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta

Joel R McNeal et al. BMC Plant Biol. 2007.

Abstract

Background: Plastid genome content and protein sequence are highly conserved across land plants and their closest algal relatives. Parasitic plants, which obtain some or all of their nutrition through an attachment to a host plant, are often a striking exception. Heterotrophy can lead to relaxed constraint on some plastid genes or even total gene loss. We sequenced plastid genomes of two species in the parasitic genus Cuscuta along with a non-parasitic relative, Ipomoea purpurea, to investigate changes in the plastid genome that may result from transition to the parasitic lifestyle.

Results: Aside from loss of all ndh genes, Cuscuta exaltata retains photosynthetic and photorespiratory genes that evolve under strong selective constraint. Cuscuta obtusiflora has incurred substantially more change to its plastid genome, including loss of all genes for the plastid-encoded RNA polymerase. Despite extensive change in gene content and greatly increased rate of overall nucleotide substitution, C. obtusiflora also retains all photosynthetic and photorespiratory genes with only one minor exception.

Conclusion: Although Epifagus virginiana, the only other parasitic plant with its plastid genome sequenced to date, has lost a largely overlapping set of transfer-RNA and ribosomal genes as Cuscuta, it has lost all genes related to photosynthesis and maintains a set of genes which are among the most divergent in Cuscuta. Analyses demonstrate photosynthetic genes are under the highest constraint of any genes within the plastid genomes of Cuscuta, indicating a function involving RuBisCo and electron transport through photosystems is still the primary reason for retention of the plastid genome in these species.

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Figures

Figure 1

Figure 1

Circular map of the complete plastid genome of Ipomoea purpurea. The genome comprises an 88,172 bp LSC, a 12,110 bp SSC, and two 30,882 bp IRs. Position one of the annotated sequence begins at the LSC/IRA junction and increases numerically counterclockwise around the genome. Genes on the inside of the circle are transcribed clockwise, those on the outside, counterclockwise. Asterisks mark genes with introns (2 asterisks mark genes with 2 introns), Ψ indicates a pseudogene. INSET-Genomes scaled to relative size: Ipomoea (outermost), Cuscuta exaltata (middle), and C. obtusiflora (innermost).

Figure 2

Figure 2

Circular map of the complete plastid genome of Cuscuta exaltata. The genome comprises an 82,721 bp LSC and a 9,250 bp SSC separated by two 16,701 bp IRs. Inversion end-points are shown with lines connecting the inner circle to the outer. Position one of the annotated sequence begins at the LSC/IRA junction and increases numerically counterclockwise around the genome. Genes are denoted as in Figure 1.

Figure 3

Figure 3

Circular map of the complete plastid genome of Cuscuta obtusiflora. The genome comprises a 50,201 bp LSC and a 6,817 bp SSC separated by 14,131 bp IRs. Position one of the annotated sequence begins at the LSC/IRA junction and increases numerically counterclockwise around the genome. Genes are denoted as in Figure 1.

Figure 4

Figure 4

Pairwise d N/d S of Nicotiana and Ipomoea vs. Panax ginseng for all shared protein-coding genes. Genes are ranked left to right by increasing d N/d S for Nicotiana. Genes lost in Cuscuta exaltata and C. obtusiflora are indicated below the graph.

Figure 5

Figure 5

Rates of substitution and selection across 4 functionally-defined classes of genes. A- d N estimates and standard errors vs Panax for Atropa, Nicotiana, Ipomoea, C. exaltata, and C. obtusiflora. B-d S vs Panax for the same taxa. C. Pairwise d N/d S for the same taxa vs. Panax; Ipomoea, C. exaltata, and C. obtusiflora vs. Nicotiana; C. exaltata and C. obtusiflora vs. Ipomoea, and C. exaltata vs. C. obtusiflora.

Figure 6

Figure 6

Phylogenetic trees created using Maximum Likelihood GTR+gamma for each functionally defined gene class. Branches with significantly higher (LRT, p < 0.01) rates of synonymous substitution per site are thickened. Branches with significantly higher d N/d S are marked with one (p < 0.01), two, (p < 0.001), or three asterisks (p < 0.0001). Values of d S and d N/d S on relevant branches are given in Table 3.

Figure 7

Figure 7

Amino acid _p_-distance for Epifagus, Ipomoea, C. exaltata, and C. obtusiflora vs.Panax across most genes present in Epifagus. Most genes are less altered relative to the outgroup in Epifagus than in Cuscuta obtusiflora, and the non-transcriptional/translational genes remaining in Epifagus (clpP and accD) are particularly divergent in C. obtusiflora.

Figure 8

Figure 8

d N/d S for all genes, all taxa (including Epifagus) vs.Panax. Most genes evolve more quickly in Ipomoea than in Nicotiana (tobacco), indicating relaxed constraint on plastid genes even before evolution of parasitism in Convolvulaceae. Constraint is further relaxed in Cuscuta exaltata and is most relaxed in Cuscuta obtusiflora, although photosynthetically related genes remain highly constrained. In general, genes present in Epifagus virginiana are under higher levels of constraint than in Cuscuta obtusiflora, despite the retention of photosynthetic genes in Cuscuta.

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