Horizontal gene transfer in parasitic plants

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Highlights

  • Parasitic plants are exemplary systems for studying the dynamics of HGT.

  • Parasitic plants show high rates of HGT, especially involving mitochondrial genomes.

  • HGT provides a new perspective on the evolution of novelty in parasitic plants.

  • HGT can serve as the ‘ghost of transfers past’ to infer former host associations.

Horizontal gene transfer (HGT) between species has been a major focus of plant evolutionary research during the past decade. Parasitic plants, which establish a direct connection with their hosts, have provided excellent examples of how these transfers are facilitated via the intimacy of this symbiosis. In particular, phylogenetic studies from diverse clades indicate that parasitic plants represent a rich system for studying this phenomenon. Here, HGT has been shown to be astonishingly high in the mitochondrial genome, and appreciable in the nuclear genome. Although explicit tests remain to be performed, some transgenes have been hypothesized to be functional in their recipient species, thus providing a new perspective on the evolution of novelty in parasitic plants.

Introduction

Parasitism has evolved multiple times across the tree of life. Parasitic plants obtain some or all of their water and nutrients, including carbohydrates and minerals, through a specialized feeding apparatus called the haustorium, which attaches to roots or shoots of their hosts (Figure 1). Parasitic plants exhibit a range of diversity, including species with the ability to photosynthesize (hemiparasites) and those that cannot (holoparasites). Despite the direct haustorial connection parasitic plants establish with their hosts, most grow predominantly exterior to their hosts. The exceptions include a small group of endophytic holoparasites, which emerge only during sexual reproduction (Figure 1). These species otherwise grow embedded in their hosts and have no discernable roots, shoots, or leaves, persisting largely as a mycelium-like body consisting of a greatly reduced strand of cells [1].

Owing to their extreme vegetative reduction and modified reproductive morphology, the phylogenetic placement of parasitic plants among their free-living relatives was long a mystery. This is especially true for the endophytic holoparasites, most of which have been historically grouped together to include species variously placed today in Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae. Recent phylogenetic investigations, however, have greatly challenged this traditional view of classification by demonstrating that these families are not closely related. Instead, the most comprehensive analyses indicate that parasitism in angiosperms has evolved at least 11 times from free-living ancestors [2].

These insights have greatly stimulated research relating to genome evolution in parasitic plants [3••, 4], and the investigation of the adaptations that have enabled the origin of parasitism [5••, 6, 7]. One of the most exciting discoveries to emerge from this body of research is the finding that parasitic plants and their hosts undergo horizontal gene transfer (HGT)  the exchange of genetic materials between distantly related, non-mating organisms. More generally, the hypothesis of HGT in autotrophic plants was invoked in two landmark studies [8, 9], in which gene phylogenies were identified as strongly incongruent with well-established species relationships based on various lines of molecular and morphological evidence. In this regard, phylogenies that are incongruent with accepted species relationships have been deemed the ‘gold standard’ for deducing HGT [10] (Figure 2). Since that time, HGT has been identified in a variety of autotrophic plant clades [10, 11••, 12], most notably in bryophytes [13], ferns [14, 15•], basal angiosperms [16, 17••], and grasses [18].

Section snippets

Parasitic plants are exemplary systems for studying HGT

Following the two initial discoveries of HGT in autotrophic plants, investigations in parasitic plants have provided important insights into HGT [14, 19, 20, 21]. Several studies ranging from single to hundreds of genes demonstrate that the parasitic mode of life may enable HGT in plants, which is thought to be facilitated by the intimate physical association between the parasite and its host [19]. This intimacy makes parasitic plants a potential model system for HGT related research. Here, the

Parasitic plants show high rates of HGT

Evidence of HGT has been identified in 10 of the 11 parasitic lineages to date (Table 1) and overwhelmingly involve mitochondrial DNA, which is consistent with most studies from autotrophic plants [17••, 22]. This is likely due to several unique properties of mitochondria, including their ability to actively uptake DNA [23], and to undergo frequent fusion and fission [24]. Additionally, plant mitochondrial genomes possess massive intergenic regions [25], allowing for foreign genes to be

Mechanisms and functionality of transgenes in parasitic plants

One outstanding question involves the uptake mechanisms of foreign DNA. Although vectors remain unclear, fungi, bacteria, and viruses have been invoked [9, 10]. More recently, transposable elements have also been implicated as a vector for HGT in autotrophic plants [36]. Although many nutrients and macromolecules, including mRNAs, are trafficked between host and parasite [5••, 37, 38], the evidence points primarily to direct uptake of DNA, rather than mRNA. This is demonstrated in various

Detecting former host associations with HGT

Perhaps one of the most exciting possibilities offered by HGT in parasitic systems is their ability to provide insights into current and past host associations. In a recent broad survey of Rafflesiaceae mitochondrial genomes [3••], gene transfers fell within two distinct categories  transfers that were ancient, perhaps dating back to the late Cretaceous, and those that were more recent. For the ancient transfers, transgenes were broadly shared and maintained synteny across related parasitic

Conclusions and future directions

Studies to date indicate that parasitic plants represent an active area of HGT. These symbioses are ideal for studying this phenomenon owing to the intimacy of their symbiotic interactions, and our ability to more confidently invoke HGT when phylogenies are incongruent with accepted species relationships. In general, HGT in parasitic plants is reflective of what we see in autotrophic plants [10, 11••]: gene transfers involving mitochondrial genomes are high, and appreciable in nuclear genomes.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

CCD and ZX were supported by National Science Foundation (NSF) Assembling the Tree of Life grant DEB-0622764 and NSF DEB-1120243 (to CCD). Members of the Davis laboratory provided helpful feedback on an early draft of this paper.

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