Horizontal transfer of expressed genes in a parasitic flowering plant

Abstract

Background: Recent studies have shown that plant genomes have potentially undergone rampant horizontal gene transfer (HGT). In plant parasitic systems HGT appears to be facilitated by the intimate physical association between the parasite and its host. HGT in these systems has been invoked when a DNA sequence obtained from a parasite is placed phylogenetically very near to its host rather than with its closest relatives. Studies of HGT in parasitic plants have relied largely on the fortuitous discovery of gene phylogenies that indicate HGT, and no broad systematic search for HGT has been undertaken in parasitic systems where it is most expected to occur.

Results: We analyzed the transcriptomes of the holoparasite Rafflesia cantleyi Solms-Laubach and its obligate host Tetrastigma rafflesiae Miq. using phylogenomic approaches. Our analyses show that several dozen actively transcribed genes, most of which appear to be encoded in the nuclear genome, are likely of host origin. We also find that hundreds of vertically inherited genes (VGT) in this parasitic plant exhibit codon usage properties that are more similar to its host than to its closest relatives.

Conclusions: Our results establish for the first time a substantive number of HGTs in a plant host-parasite system. The elevated rate of unidirectional host-to- parasite gene transfer raises the possibility that HGTs may provide a fitness benefit to Rafflesia for maintaining these genes. Finally, a similar convergence in codon usage of VGTs has been shown in microbes with high HGT rates, which may help to explain the increase of HGTs in these parasitic plants.

Figure 1

Accepted relationships between the twelve taxa included in our phylogenomic analyses[[26]]. The nine reference taxa for which complete genome sequences are available are labeled in black. Holoparasitic Rafflesia cantleyi is a member of Malpighiales (clade shown in red), and its obligate host Tetrastigma rafflesiae is a member of Vitaceae (clade shown in blue). The approximate divergence time between the parasite and host clade is 115 Ma [19]. Open flower of Rafflesia cantleyi shown in left inset (~0.5 m in diameter); floral bud in right inset shown attached to Tetrastigma rafflesiae host vine with leaves of the latter in foreground.

Figure 2

Percentage of HGT transcripts in parasitic Rafflesia cantleyi and its obligate host Tetrastigma rafflesiae . These species are similarly contrasted against two autotrophic species that are closely related to Rafflesia, Manihot esculenta and Ricinus communis. Placements consistent with HGT in the latter two non-host, non-parasitic malpighialean taxa as defined for Rafflesia provide an estimate of the rate of non-HGT related factors that contribute to phylogenetic discordance. Species belonging to the Malpighiales and Vitaceae clade are shown in red and blue, respectively. The total number of transcripts used as denominators to calculate percentages are shown in parentheses.

Figure 3

Percentage of VGT transcripts from Rafflesia cantleyi , Manihot esculenta , and Ricinus communis that exhibit coding properties (nucleotide, codon, and dinucleotide usage) more similar to Vitis vinifera than to each other. The coding affinity for each gene was determined by calculating the smallest χ² distance to genes from other genomes in the cluster. The total number of VGT transcripts used as denominators to calculate percentages are shown in parentheses.